June 21, 2013

Aging, intelligence, cooperation, and ecology

The age-specific force of natural selection and biodemographic walls of death "Nonlinear interactions cause the collapse of Hamilton-style predictions in the most commonly studied case..."

GWAS of 126,559 Individuals Identifies Genetic Variants Associated with Educational Attainment "A linear polygenic score from all measured SNPs accounts for ≈2% of the variance in both educational attainment and cognitive function."

Fusing enacted and expected mimicry generates a winning strategy that promotes the evolution of cooperation "reducing conflict intensities among human populations necessitates (i) instigation of social initiatives that increase the perception of similarity among opponents"

Global human appropriation of net primary production doubled in the 20th century

Several scales of biodiversity affect ecosystem multifunctionality

March 29, 2013

Persistent polymorphisms, enhancing mutation, new fossils, cooperation & conservation

All five of my Darwinian Agriculture lectures at the International Rice Research Institute are now available on YouTube.

Here are some interesting papers published this week.

Multiple Instances of Ancient Balancing Selection Shared Between Humans and Chimpanzees " In addition to the major histocompatibility complex, we identified 125 regions in which the same haplotypes are segregating in the two species [neither version has displaced the other in either species in 6 million years], all but two of which are noncoding [i.e., they probably control other genes rather than coding for a protein]." The most likely explanation for such prolonged co-existence is that individuals with less-common alleles may be resistant to pathogens that have evolved to attack those with more-common alleles.

Accelerated gene evolution through replication-transcription conflicts" "We propose that bacteria, and potentially other organisms, promote faster evolution of specific genes through orientation-dependent encounters between DNA replication and transcription."

Palaeontology: Tubular worms from the Burgess Shale"

Preservation of ovarian follicles reveals early evolution of avian reproductive behaviour"

Both information and social cohesion determine collective decisions in animal groups

Governance regime and location influence avoided deforestation success of protected areas in the Brazilian Amazon

Wild Pollinators Enhance Fruit Set of Crops Regardless of Honey Bee Abundance

March 8, 2013

Cooperation, inducible defense, cancer, and more

Here are some papers that look interesting this week.

Prairie Dogs Disperse When All Close Kin Have Disappeared "cooperation among kin is more important than competition among kin for young prairie dogs"

Variants at serotonin transporter and 2A receptor genes predict cooperative behavior differentially according to presence of punishment "Participants with a variant at the serotonin transporter gene contribute more, leading to group-level differences in cooperation, but this effect dissipates in the presence of punishment."

Plant mating system transitions drive the macroevolution of defense strategies
the repeated, unidirectional transition from ancestral self-incompatibility (obligate outcrossing) to self-compatibility (increased inbreeding) leads to the evolution of an inducible (vs. constitutive) strategy of plant resistance to herbivores."

Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics "we reconstructed the phylogeny of the fragments for each patient, identifying copy number alterations in EGFR and CDKN2A/B/p14ARF as early events, and aberrations in PDGFRA and PTEN as later events during cancer progression"

Non-optimal codon usage is a mechanism to achieve circadian clock conditionality"
"natural selection against optimal codons to achieve adaptive responses to environmental changes"

Gene Transfer from Bacteria and Archaea Facilitated Evolution of an Extremophilic Eukaryote "> 5% of protein-coding genes of G. sulphuraria were probably acquired horizontally"

Recent land use change in the Western Corn Belt threatens grasslands and wetlands
"a recent doubling in commodity prices has created incentives for landowners to convert grassland to corn and soybean cropping... onto marginal lands characterized by high erosion risk and vulnerability to drought."

November 9, 2012

Cooking key to cognition; corals recruit bodyguards; etc.

Metabolic constraint imposes tradeoff between body size and number of brain neurons in human evolution "This limitation was probably overcome in Homo erectus with the shift to a cooked diet."

Corals Chemically Cue Mutualistic Fishes to Remove Competing Seaweeds "Mutualistic gobies and corals appear to represent a marine parallel to terrestrial ant-plants, in that the host provides shelter and food in return for protection from natural enemies."

Bateman in Nature: Predation on Offspring Reduces the Potential for Sexual Selection "substantial yearly variation in the Bateman slope [number of offspring as a function of the number of mates] due to predation on fawns was evident."

Drift-barrier hypothesis and mutation-rate evolution "selection appears to reduce the mutation rate... to a level that scales negatively with both the effective population size (Ne)... and the genomic content "

For a list of my upcoming talks around the world, see my new Darwinian Agriculture Blog.

September 14, 2012

This week: fossils, epidemics, cooperation, and aging

Arthropods in amber from the Triassic Period "arthropods some 100 Ma older than the earliest prior records in amber"

Unifying the spatial epidemiology and molecular evolution of emerging epidemics "spatial parameters of an emerging epidemic [can] be directly estimated from sampled pathogen genome sequences"

Evolution of cooperation and skew under imperfect information "full cooperation may not be achievable due to private information over individuals' outside options"

No third-party punishment in chimpanzees "Dominants retaliated when their own food was stolen, but they did not punish when the food of third-parties was stolen, even when the victim was related to them. "

Ageing: Mixed results for dieting monkeys
Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study "Our study suggests a separation between health effects, morbidity and mortality"

August 10, 2012

Fossils, convergent evolution, cooperation, and "groundwater footprints"

New fossils from Koobi Fora in northern Kenya confirm taxonomic diversity in early Homo "The new fossils confirm the presence of two contemporary species of early Homo, in addition to Homo erectus, in the early Pleistocene of eastern Africa."

A transitional snake from the Late Cretaceous period of North America "...snakes evolved from burrowing lizards. The skull is intermediate..."

Community-wide convergent evolution in insect adaptation to toxic cardenolides by substitutions in the Na,K-ATPase The same molecular change to a sodium pump, previously seen in Monarch butterflies, was found in four insect species (separated by 300 million years of evolution) feeding on plants making the same natural insecticides.

Heterogeneous networks do not promote cooperation when humans play a Prisoner's Dilemma "1,229 volunteers chosen among last year's high school students"

Water balance of global aquifers revealed by groundwater footprint" "80 per cent of aquifers have a groundwater footprint that is less than their area" but "the global groundwater footprint is currently about 3.5 times the actual area of aquifers", putting water supplies for 3.5 million people at risk. My book briefly compares the ecological footprints of conventional and organic farms.

July 8, 2012

Evolution of cooperation in Ottawa

Mike Travisano discusses experimental evolution of multicellularity.

My talk here at the Evolution meetings inn Ottawa was taking 12 minutes in practice but I finished in 10. Nervous? Maybe, because I was arguing that most past measurements of fitness benefits to legumes from rhizobia are suspect, which would throw lots of results into question.

Typically, people who want to compare benefits from two different rhizobial strains inoculate host plants with each strain separately, then compare plant growth. But plants in the field are almost always nodulated by multiple strains. I showed that a plant inoculated with a slow-nodulating but highly efficient strain (which eventually provides lots of nitrogen, relative to its carbon cost) may provide no more growth than a less-efficient but faster nodulating strain, when each is inoculated alone. The problem is that plants with only the slow, efficient strain will be short of nitrogen at first, with compound-interest effects on growth. In the field, though, there will always be some fast-nodulating rhizobia. So it's not a matter of nodules vs. no nodules, but of how efficient those nodules are. So we inoculate plants with the two strains being compared, in different ratios, then measure plant growth as a function of the percent of nodules containing the focal strain. With this method, a computer model and actual data agree that an increase in growth with nodule occupancy by the focal strain indicates a more-efficient strain.

Maren Friesen suggested a similar method in a recent paper in New Phytologist. Unfortunately, her main conclusions were based on the old, one-strain-per-plant method.

Megan Frederickson gave a stimulating talk on cheating in symbionts. We have shown that soybean, alfalfa, and peas all impose fitness-reducing sanctions on rhizobia that fail to fix nitrogen, once established inside root nodules. Frederickson asked what maintains such sanctions? If they work, "cheaters" will be rare, so there will be only weak selection on legumes to maintain sanctions. She suggested that something else (such as a generalized response of sending more resources to parts of a root that supply more nitrogen) must select for the responses we call sanctions.

I agree that cheaters would be rare under consistent sanctions, which could relax selection to maintain sanctions. But sanctions may not be that consistent. See Toby Kiers' "measured sanctions" paper. And maybe only a fraction of less-beneficial rhizobia are cheaters, that is, strains that benefit from diverting resources from nitrogen fixation to their own reproduction. Many may be defective mutants, that fix less nitrogen but don't benefit thereby. Sanctions would keep any individual strain of defective mutant rare, but there could be many different strains.

Frederickson's talk stimulated a lot of useful discussion afterwards and I am looking forward to seeing her paper.

March 21, 2012

Cumulative culture and cooperation in humans and other primates

Two recent papers compare the problem-solving abilities of humans and other primates. Individual humans are smarter than individual chimps, of course. But our most-impressive intellectual feats depend on the accumulation of cultural knowledge over many generations. A blacksmith might make some of her own tools, but she didn't invent most of them, or smelt the iron from ore she mined herself. Computer programmers, in turn, depend on technology that built on the work of blacksmiths and many others.

I once read a story in which Earth was visited by aliens with vastly superior technology. Initially, humans assumed that the aliens must be much smarter than we are. It turned out that most of them were pretty stupid, easily duped by humans. It's just that their civilization was older, so they'd had time to invent spaceships and such, even with fewer geniuses than we have. How much of our technological superiority to nonhuman primates is due to superior individual problem-solving ability, and how much to cumulative culture?

"Identification of the Social and Cognitive Processes Underlying Human Cumulative Culture" was published in Science by L.G. Dean and others. They compared the ability of groups of 3-4 year-old human children, chimps with capuchin monkeys, in solving a "puzzle box", where retrieving the most-valued food reward depended on solving three successive levels of increasing difficulty. Only one chimp of 33 got to level 3, while many humans did. Why?

Humans copied others more than chimps or monkeys did. Chimps tended to copy the moves needed to get to the first level, but not beyond that, so it didn't help much to let them see a chimp that had been trained to reach level 3. All 23 clear cases of "teaching" (2/3 verbal and 1/3 via gestures) were by humans. Humans were more generous in other ways also: 47% shared food with others, while none of the chimps or monkeys did. Chimp mothers stole from their own offspring. In summary:

"The children responded to the apparatus as a social exercise, manipulating the box together, matching the actions of others, facilitating learning in others through verbal instruction and gesture, and engaging in repeated prosocial acts of spontaneous gifts of the rewards they themselves retrieved. In contrast, the chimpanzees and capuchins appeared to interact with the apparatus solely as a means to procure resources for themselves, in an entirely self-serving manner, largely independent of the performance of others, and exhibiting restricted learning that appeared primarily asocial in character."
Human adults may be different, however, with rich (or well-educated?) adults acting more like chimps. See last week's post.

The second paper also compares cooperation in humans and other primates. "Old World monkeys are more similar to humans than New World monkeys when playing a coordination game" was recently published by Sarah Brosnan and others in Proceedings of the Royal Society B. Pairs of humans, rhesus monkeys, and capuchin monkeys played the Assurance (or Stag Hunt) game, using computer joysticks to enter their moves. An individual choosing Hare gets a reward whatever the other player does. But if both choose Stag, they each get double the reward.

All of the human pairs talked, but only some talked about the game. Of those that did, all 22 pairs ended up playing mostly cooperatively -- but not 100%, even after seeing the potential benefit. Those who talked about other topics played mostly noncooperatively, forgoing the benefits of cooperation.

The two monkey species differed. For both species, if individuals could see the other's move, they learned to "cooperate" and got high rewards. (They could see each other, but did they realize they were playing with each other, rather than with the computer?) The capuchins played more randomly when they didn't know the other's move, whereas two pairs of rhesus monkeys quickly learned to trust their partner and cooperate (or, anyway, to play as if they did). Rhesus monkeys are native to Africa, rhesus monkeys to South America. So, as the authors put it:

"Old World primates outperformed New World primates,
rather than humans outperforming non-humans."
They speculate that, perhaps:
"...humans' abilities are built on a shared foundation that extends back at least as far as the split with Old World monkeys [which was longer ago than the split between apes and old-world monkeys, let alone the split between humans and other apes]."
An interesting hypothesis, but I would like to see data for more species.

February 10, 2012

Measuring fitness benefits to rhizobia from symbiosis with legumes

This week's paper is "Measuring the fitness of symbiotic rhizobia", published in the journal Symbiosis by Will Ratcliff, who earned a PhD with me, Kyra Underbakke, who did a prize-winning science fair project in our lab when she was in high school and has done undergraduate research with us since then, and me.
Alfalfa nodules containing nitrogen-fixing rhizobia. Photo by Alex May.

Rhizobia are soil bacteria, best known for infecting the roots of legume plants, reproducing inside swellings called nodules, and converting nitrogen gas from the soil atmosphere into forms their plant hosts can use. Since about 2000, I've been asking why they do these things.

Every "why" question in biology has the same general answer, although details differ. Living things do what they do largely because they inherited a tendency to do so, from ancestors whose survival and reproduction depended on doing something similar. So rhizobia infect legume roots and "fix" (take up) nitrogen inside nodules because ancestors who did that had greater fitness (proportional representation in the next generation), relative to otherwise similar bacteria that didn't do these things. (Many of the ancestors of a given rhizobial cell may have spent their lives in soil, never infecting a legume root. But those that did had so many more descendants that the trait has persisted.)

Infecting a root and reproducing inside a nodule seems like a no-brainer, which is convenient, since rhizobia don't have brains. But why use resources to fix nitrogen that the rhizobia could have used for more reproduction, instead. We hypothesized (Denison 2000, West et al. 2002), and then confirmed experimentally (Kiers et al. 2003, Oono et al. 2011), that legumes (in particular, soybeans, alfalfa, and pea plants) treat nodules that fail to fix nitrogen differently, in ways that presumably keep the legumes from wasting resources, and incidentally reduce the reproduction of rhizobia inside. We have called these plant responses "sanctions", without any implication that plants are self-aware or that sanctions will change the behavior of rhizobia, except via evolutionary decreases in the frequency of rhizobial "cheaters" over generations.

Moderate cheating (fixing less nitrogen than the best strains, but still some) may or may not trigger sanctions (Kiers et al. 2006, Simms et al. 2006, Heath and Tiffin 2009). But how can we tell? Some researchers have found a correlation between rhizobia/nodule and nodule weight, then looked to see whether strains that are more beneficial make larger nodules, presumably containing more rhizobia. We've based our conclusions on actual counts of rhizobia, worrying that correlations might be misleading.

For example, Gubry-Rangin and colleagues (Gubry-Rangin et al. 2010) found that nodules containing a strain that couldn't fix nitrogen were smaller (consistent with the host imposing sanctions), yet they contained similar numbers of rhizobia as nodules containing a good nitrogen fixer (so those sanctions might not always affect rhizobial evolution the way we've hypothesized). They noted that:

"These results may therefore contrast with the positive correlation between the size and the viable rhizobia found in M. truncatula (Heath & Tiffin 2007). As discussed by Oono et al. (2009), this relationship may vary among different rhizobia..."

This week's paper provides additional evidence of this. There was a good correlation between nodule weight and rhizobia/nodule for each of the two strains in the figure, individually, but this relationship differed between strains.
Even actual measurements of numbers of rhizobia/nodule may not be a complete measure of the fitness benefits rhizobia gain from symbiosis. We found that a rhizobial strain that was less beneficial to its plant host accumulated more resources (specifically, polyhydroxybutyrate or PHB) per rhizobial cell. How much more? Enough to reproduce without external resources. Correcting for PHB showed that the less-beneficial strain gained twice as much fitness from symbiosis as the better strain, whereas ignoring PHB would have led to the incorrect conclusion that there was no difference in fitness between the strains.

There may be more to this story. Having enough PHB to reproduce without external resources only matters if external resources are limiting. Under starvation conditions, rhizobia can definitely use PHB to survive and even to reproduce (Ratcliff et al. 2008). But do nodules containing higher-PHB rhizobia release more rhizobia to the soil (because they use the PHB to reproduce inside dying nodules) or do rhizobia released still have extra PHB? If the latter, how much does this extra PHB affect survival and reproduction in soil? If the National Science Foundation funds our next grant proposal, we will find out. If they don't, I still appreciate their support of my past research.


Denison R. F. 2000. Legume sanctions and the evolution of symbiotic cooperation by rhizobia. American Naturalist 156:567-576.

Gubry-Rangin C., M. Garcia, and G. Bena. 2010. Partner choice in Medicago truncatula-Sinorhizobium symbiosis. Proceedings of the Royal Society B 277:1947-1951.

Heath K. D., P. Tiffin. 2009. Stabilizing mechanisms in a legume-rhizobium mutualism. Evolution 63:652-662.

Kiers E. T., R. A. Rousseau, and R. F. Denison. 2006. Measured sanctions: legume hosts detect quantitative variation in rhizobium cooperation and punish accordingly. Evolutionary Ecology Research 8:1077-1086.

Kiers E. T., R. A. Rousseau, S. A. West, and R. F. Denison. 2003. Host sanctions and the legume-rhizobium mutualism. Nature 425:78-81.

Oono, R., R.F. Denison, E.T. Kiers. 2009. Tansley review: Controlling the reproductive fate of rhizobia: How universal are legume sanctions? New Phytologist 183:967-979.

Oono, R., C. G. Anderson, and R. F. Denison. 2011. Failure to fix nitrogen by non-reproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates. Proceedings of the Royal Society B 278:2698-2703.

Ratcliff,W.C., K. Underbakke, R.F. Denison. 2012. Measuring the fitness of symbiotic rhizobia. Symbiosis 55: 85-90.

Ratcliff W. C., S. V. Kadam, and R. F. Denison. 2008. Polyhydroxybutyrate supports survival and reproduction in starving rhizobia. FEMS Microbiology Ecology 65:391-399.

Simms E. L., D. L. Taylor, J. Povich, R. P. Shefferson, J. L. Sachs, M. Urbina, and Y. Tausczik. 2006. An empirical test of partner choice mechanisms in a wild legume-rhizobium interaction. Proceedings of the Royal Society B 273:77-81.

West S. A., E. T. Kiers, E. L. Simms, and R. F. Denison. 2002. Sanctions and mutualism stability: why do rhizobia fix nitrogen? Proceedings of the Royal Society B 269:685-694.

December 8, 2011

This week's picks

Just when I was starting to get back into the lab, the proofs for my book on Darwinian Agriculture arrived. It's due out in June or July, but I have to check everything and do the index by January. So I only have time to read the abstracts of these interesting-looking papers.

Equitable decision making is associated with neural markers of intrinsic value
"making equitable interpersonal decisions [behaving fairly] engaged neural structures involved in computing subjective value, even when doing so required foregoing material resources... not simply a response to external pressure"
[In other news, people enjoy sex. In both cases, natural selection has shaped our brains based on what maximized contributions to gene pools, in past environments. I wonder how many generations it would take for this to change, in environments where fairness doesn't help you win mates or allies, or where sex is decoupled from reproduction?] "Four participants [of 19] produced no generous/equitable choices; their data could not be modeled and were excluded." [Any difference in the ancestral environments of these four? Or were they finance majors?]

Conflict, sticks and carrots: war increases prosocial punishments and rewards
[On the other hand...] "during wartime, people are more willing to pay costs to punish non-cooperative group members and reward cooperative group members."

Trade-off between warning signal efficacy and mating success in the wood tiger moth
"yellow males had lower mating success than white males" but birds don't eat them.

Global human mandibular variation reflects differences in agricultural and hunter-gatherer subsistence strategies

Fitness consequences of plants growing with siblings: reconciling kin selection, niche partitioning and competitive ability
Impact of epistasis and pleiotropy on evolutionary adaptation

November 28, 2011

Experimental evolution of metabolism, sex, and multicellularity

Update: links to our open-access Proceedings of the National Academy of Sciences paper on experimental evolution of multicellularity, including PDF and great videos, can be found at the Microbial Population Biology (Micropop) website.

The Nov. 18 issue of Science has a news feature by Elizabeth Pennisi on recent research using experimental evolution, including some work on the evolution of multicellularity, led by Mike Travisano and Will Ratcliff, in which I've been involved.

Two interesting experimental evolution projects are underway in Canada. In Montreal, Graham Bell has been evolving algae that get their energy from a simple organic molecule, acetate, instead of from light. At first, the algae could barely survive without light, but after five years (still a fraction of the time that Richard Lenski has been evolving E. coli) he has hundreds of independent lines that have evolved a variety of ways to grow on acetate in the dark.

In Toronto, Aneil Agrawal is subjecting the sex life of rotifers to experimental evolution. Like aphids, Daphnia, and some other species, rotifers normally reproduce asexually, resorting to sex only under stress. Populations consisting of females, producing other females asexually, grow twice as fast as populations that are half male. (In my forthcoming book, Darwinian Agriculture, I discuss how reindeer herders increase production by harvesting mostly male calves for meat, so that most adults are females producing more calves, rather than males fighting over females.) But sexual reproduction shuffles genomes in ways that may be beneficial under different conditions. Agrawal and his postdoc Lutz Becks found that the balance between sexual and asexual reproduction evolved in response to environmental conditions. In stable environments, sex eventually disappeared. Once you've evolved the perfect genotype for some particular stable environment, why scramble that genotype through sex?

Meanwhile, we've been exploring the transition to multicellularity.
Cellular differentiation in multicellular clusters evolved from unicellular yeast (photo by Will Ratcliff).

Unicellular life apparently had the earth to itself for over a billion years before even simple multicellular life evolved. So you might think that this major evolutionary transition requires some complicated series of genetic changes that would only happen rarely. Alternatively, maybe the first simple multicellular organisms weren't that different, genetically, from their unicellular ancestors -- they just couldn't out-compete their unicellular parents until conditions were right.

Individual cells would have greater access to nutrients in their environment than cells in the middle of a cluster, but what advantages might clusters have, under what conditions?

Continue reading "Experimental evolution of metabolism, sex, and multicellularity" »

September 9, 2011

This week's picks

A Gene for an Extended Phenotype "The viral gene that manipulates climbing behavior of the [Gypsy moth] host was identified"

The Foot and Ankle of Australopithecus sediba [hominin fossil from 1.78 and 1.95 million years ago] "may have practiced a unique form of bipedalism and some degree of arboreality"

Assured fitness returns in a social wasp with no worker caste "experimentally orphaned brood... continue to be provisioned by surviving adults... no evidence that naturally orphaned offspring received less food than those that still had mothers in the nest."

The sudden emergence of pathogenicity in insect-fungus symbioses threatens naive forest ecosystems "symbioses between wood-boring insects and fungi... are shifting from non-pathogenic saprotrophy in native ranges to a prolific tree-killing in invaded ranges... when several factors coincide"

Ultra-fast underwater suction traps "this unique trapping mechanism conducts suction in less than a millisecond and therefore ranks among the fastest plant movements known"

The taming of an impossible child - a standardized all-in approach to the phylogeny of Hymenoptera using public database sequences "combines some well-established programs with numerous newly developed software tools"

August 19, 2011

Reciprocity maintains cooperation between plants and mycorrhizal fungi

Mycorrhizal fungi attach to plant roots and trade phosphorus (and sometimes other benefits) for photosynthates. But is it really "trade"? In other words, if one partner defects, will the other continue its contribution? A recent paper in Science, by Toby Kiers and colleagues, shows that the term, "trade" is justified.(Kiers et al. 2011)

Earlier, as my first PhD student, Toby showed that symbiotic rhizobia, living inside soybean root nodules, can't stop supplying the plant with nitrogen without suffering a decrease in their own fitness.(Kiers et al. 2003) We called the plant response "sanctions", although this could be misinterpreted as an attempt by the plant to improve the behavior of the rhizobia. We assume that the behavior of a given rhizobial genotype is programmed by its DNA, but sanctions against less-beneficial strains will decrease their frequency in subsequent generations. More recently, Ryoko Oono demonstrated a subtler form of sanctions against potentially reproductive rhizobia when their nonreproductive clonemates stop fixing nitrogen.(Oono et al. 2011)

Different strains of rhizobia on the same plant are (mostly) segregated in different root nodules, so "shutting down" one nodule preferentially hurts a single strain of rhizobia. But multiple strains of mycorrhizal fungus typically infect the same root. Can plants preferentially allocate resources to the most-beneficial fungi? Jim Bever and colleagues showed that they can, when different strains are attached to different parts of the root, but apparently not when the strains are more mixed.(Bever et al. 2009) Results from Kiers' group, however, suggest that mixing is not a problem.

They grew Medicago truncatula (a model species related to alfalfa) with mixtures of mycorrhizal fungi that they classified as more- or less-beneficial. To track photosynthate allocation, they let plant photosynthesis take up carbon dioxide containing the heavier 13C isotope of carbon. To see which fungi got more of this carbon, they used a clever technique.

They extracted RNA from the fungi and separated it into lighter and heavier (more-recent-plant-carbon) fractions, using a centrifuge. Then they used difference in the RNA base sequences of their different fungi to measure their relative representation in the light and heavy fractions. Fungi with greater representation in the heavy fraction were getting more recently supplied carbon from the plant, so they were benefiting more from symbiosis. A more-beneficial fungal species got more carbon than either of two less-beneficial species. This result is consistent with host sanctions (or, since each fungus interacts with multiple plants, with a "biological market" where individuals trade more with those that offer the best deal).

It's hard to measure all of the benefits a mycorrhizal fungus provides, however, so they also manipulated the exchange of specific resources. The species they classified as more beneficial got more carbon when it had access to more phosphorus, and presumably supplied it to the plant. A less-beneficial species didn't get more carbon when it had access to more phosphorus, perhaps because it didn't give much of the phosphorus to the plant. Similarly, the cooperative strain apparently responded to differences in carbon supply from the plant, allocating more phosphorus to where it was getting more carbon. So sanctions appear to go both ways.


Bever J. D., S. C. Richardson, B. M. Lawrence, J. Holmes, and M. Watson. 2009. Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism. Ecology Letters 12:13-21.

Kiers E. T., M. Duhamel, Y. Yugandgar, J. A. Mensah, O. Franken, E. Verbruggen, C. R. Felbaum, G. A. Kowalchuk, M. M. Hart, A. Bago, T. M. Palmer, S. A. West, P. Vandenkoornhuyse, J. Jansa, and H. Bücking. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880-882.

Kiers E. T., R. A. Rousseau, S. A. West, and R. F. Denison. 2003. Host sanctions and the legume-rhizobium mutualism. Nature 425:78-81.

Oono R., C. G. Anderson, and R. F. Denison. 2011. Failure to fix nitrogen by non-reproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates. Proceedings of the Royal Society B 278:2698-2703.

August 12, 2011

This week's picks

Reciprocal Rewards Stabilize Cooperation in the Mycorrhizal Symbiosis Toby Kiers, who previously demonstrated host sanctions against cheating rhizobia, now shows that plants give less carbon to less-beneficial mycorrhizal fungi. I hope I can find time to discuss this paper in more detail soon.

Natural variation in Pristionchus pacificus dauer formation reveals cross-preference rather than self-preference of nematode dauer pheromones "strains may have evolved to induce dauer formation precociously in other strains in order to reduce the fitness of these strains"

Nest Inheritance Is the Missing Source of Direct Fitness in a Primitively Eusocial Insect

Polyandrous females benefit by producing sons that achieve high reproductive success in a competitive environment

Kin selection in den sharing develops under limited availability of tree hollows for a forest marsupial

Aging of the cerebral cortex differs between humans and chimpanzees "significant aging effects in humans were... individuals that were older than the maximum longevity of chimpanzees. Thus... brain structure shrinkage in human aging is evolutionarily novel and the result of an extended lifespan"

Bacterial persistence by RNA endonucleases

Host-parasite local adaptation after experimental coevolution of Caenorhabditis elegans and its microparasite Bacillus thuringiensis

Sperm chemotaxis, fluid shear, and the evolution of sexual reproduction

August 7, 2011

Nitrogen-fixing cereals?

This week's paper was published in Science (Beatty and Good 2011). It discusses the prospects for developing cereals, like wheat or rice, that can use ("fix") atmospheric nitrogen. This paper was brought to my attention both by my wife, Cindy, by Andy McGuire. As my first graduate student, at UC Davis, Andy tested the use of legume "green manures", which form symbioses with nitrogen-fixing rhizobia bacteria, to supply nitrogen to a subsequent wheat crop. (McGuire et al. 1998)

This week's paper suggests three approaches. Maybe we could engineer cereals to host rhizobia in root nodules, similar to those found on legumes. Maybe we could encourage looser associations between cereals and bacteria to fix nitrogen in or on the plant, even without nodules. Or, maybe we could engineer the plants themselves to fix nitrogen.

The authors note that the proposed cereal-root nodules would need to provide a low-oxygen environment, to protect the key enzyme, nitrogenase. Just keeping oxygen low isn't that difficult. Legume nodules have a physical barrier to gas diffusion that limits oxygen influx to the nodule interior, and it might not be that hard to do something similar in cereals. But rhizobial nitrogen fixation is powered by respiration, which requires lots of oxygen. So rhizobia need a high oxygen flux, in addition to a low oxygen concentration. Diffusion is slow at the low concentrations beyond the diffusion barrier, so diffusion of free oxygen within rhizobia-infected cells can't meet demand. Much of the oxygen is carried by diffusion of a plant hemoglobin, whose high concentration makes the inside of legume root nodules red.

And that's not the end of the challenges we would need to overcome to put functional root nodules on cereals. Suppose the diffusion barrier were just thick enough that respiratory uptake drops oxygen concentration from atmospheric (21 kPa) to the targeted near-zero concentration (1 kPa, say) across the diffusion barrier. What if the respiration rate drops to 90% of it's current value? (A slight decrease in soil temperature could have this effect, as could a shortage of photosynthate.) The concentration drop across the barrier is proportional to the flux (Fick's Law of Diffusion, similar to Ohms law for electricity), so the concentration drop would now be 18 kPa instead of 20 kPa. So the nodule-interior oxygen would now be 3 kPa instead of 1 kPa. 3 kPa is probably high enough to destroy nitrogenase.

Evolution has solved this problem, too, at least in legumes. As conditions change, legumes adjust the gas permeability of their nodules to keep oxygen low enough to protect nitrogenase, but high enough for respiration to meet their nitrogen-fixation needs. When sheep graze clover plants, the resulting photosynthate shortage decreases nodule respiration, so you might expect nodule-interior oxygen levels to rise, perhaps endangering nitrogenase. But clover plants decrease their nodule gas permeability decreases so much that nodule-interior oxygen actually decreases, rather than increasing (Hartwig et al. 1987, Denison and Okano 2003). Cereal root nodules would need something similar.

If we could engineer cereal crops to allow infection by rhizobia and support their reproduction inside root nodules that actively regulate oxygen supply, maybe the rhizobia would fix nitrogen there... at first.

But, like all living things, rhizobia evolve. Any mutation that reduced rhizobial investment in nitrogen fixation would free resources for additional rhizobial reproduction. If there were only one rhizobial genotype per plant, this "cheating" would be self-defeating, because a nitrogen-starved plant would have less photosynthate to support rhizobia. But, with multiple genotypes per plant, we have a "tragedy of the commons", favoring cheaters.(Denison 2000, West et al. 2002)

Legume evolution has found at least a partial solution to this problem, too, although there's probably room for improvement. Although moderate levels of cheating may be tolerated (Kiers et al. 2006), major diversion of resources from nitrogen fixation to rhizobial reproduction triggers host "sanctions", which reduce the fitness of rhizobial cheaters (Kiers et al. 2003, Oono et al. 2011). If we don't want nitrogen-fixing cereals to waste photosynthate supporting nonfixing rhizobia, they would need to impose sanctions, too. Or maybe growing them in rotation with sanction-imposing legumes hosting the same rhizobia would be enough to keep rhizobial cheaters rare.

What about the second option, cereals without nodules, but associating with nitrogen fixers? To meet a significant fraction of a cereal's nitrogen needs, we would need to regulate oxygen supply, as in nodules. And we would soon face the same problem of cheaters (Kiers and Denison 2008), so we'd also need some form of sanctions. If we're have to duplicate the functions of nodules anyway, why not copy nodules, rather than starting from scratch?

Engineering the cereals themselves to fix nitrogen, without rhizobia, would solve the problem of cheaters. The article suggests that it might be possible to add nitrogen fixation to plant mitochondria, the current site of respiration, or to chloroplasts, responsible for photosynthesis. Photosynthesis generates oxygen, which would tend to destroy nitrogenase. But the authors say that "some cyanobacteria perform photosynthesis and nitrogen fixation in the same space but at separate times" - maybe chloroplasts could somehow shield nitrogenase from oxygen during the day, when they're photosynthesizing, and activate nitrogenase only at night. This seems possible, at least in theory. But could it be done soon enough to help avert looming food shortages?

The article closes with the hope that "if nitrogen supply and carbon metabolism can be closely coupled, excess nitrogen would not be lost to the environment." That is already true of legumes, which shut down nodules when they have as much nitrogen as they need (Denison and Harter 1995). But this feedback control evolved - legumes that wasted photosynthate on "extra" nitrogen fixation were out-competed by more-frugal mutants - it would not be an "automatic" outcome of any of the approaches proposed.

So, again, any attempt to develop nitrogen-fixing cereals would benefit from copying what legume nodules already do. It's too bad that we don't yet know the mechanisms that regulate oxygen supply in legume nodules, impose sanctions on rhizobial cheaters, or adjust nitrogen-fixation rate to match nitrogen needs. Regulation of nodule gas permeability appears to be involved in all three, but we don't know how gas permeability is regulated. It's too bad that nobody wants to fund that kind of research any more.


Beatty P. H., A. G. Good. 2011. Future Prospects for Cereals That Fix Nitrogen. Science 333:416-417.

Denison R. F. 2000. Legume sanctions and the evolution of symbiotic cooperation by rhizobia. American Naturalist 156:567-576.

Denison R. F., Y. Okano. 2003. Leghaemoglobin oxygenation gradients in alfalfa and yellow sweetclover nodules. Journal of Experimental Botany 54:1085-1091.

Denison R. F., B. L. Harter. 1995. Nitrate effects on nodule oxygen permeability and leghemoglobin. Nodule oximetry and computer modeling. Plant Physiology 107:1355-1364.

Hartwig U., B. Boller, and J. Nösberger. 1987. Oxygen supply limits nitrogenase activity of clover nodules after defoliation. Annals of Botany 59:285-291.

Kiers E. T., R. F. Denison. 2008. Sanctions, cooperation, and the stability of plant-rhizosphere mutualisms. Annual Review of Ecology, Evolution, and Systematics 39:215-236.

Kiers E. T., R. A. Rousseau, and R. F. Denison. 2006. Measured sanctions: legume hosts detect quantitative variation in rhizobium cooperation and punish accordingly. Evolutionary Ecology Research 8:1077-1086.

Kiers E. T., R. A. Rousseau, S. A. West, and R. F. Denison. 2003. Host sanctions and the legume-rhizobium mutualism. Nature 425:78-81.

McGuire A. M., D. C. Bryant, and R. F. Denison. 1998. Wheat yields, nitrogen uptake, and soil water content following green manure vs. fallow. Agronomy Journal 90:404-410.

Oono R., C. G. Anderson, and R. F. Denison. 2011. Failure to fix nitrogen by non-reproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates. Proceedings of the Royal Society B 278:2698-2703.

West S. A., E. T. Kiers, E. L. Simms, and R. F. Denison. 2002. Sanctions and mutualism stability: why do rhizobia fix nitrogen? Proceedings of the Royal Society B 269:685-694.

August 1, 2011

Are we doomed?

New Statesman asked a bunch of scientists this question. Bjørn Østman blogged that:

"it is likely that the human population will be decimated some time in the future, perhaps even as soon as within the next hundred years. A cataclysmic event caused by global climate change, perhaps? If anyone survives at all, I predict it will be in a number of smaller populations separated from each other geographically.... Assuming that the environmental changes caused by the global cataclysmic event are severe enough that the separated populations won't be able to interact (i.e., have sex) for long enough, the different populations will continue to diverge from each other, and speciation will eventually occur. 6-7, say, million years hence..."
I can't tell if this is supposed to be a joke, but I can't imagine humans surviving, yet staying isolated that long. And I can't imagine climate-change-related catastrophe reducing world population below a billion or so. To eliminate all but a few isolated populations would take a major extraterrestrial impact, global nuclear war, or maybe some disease.

I don't think humans are likely to go extinct within the next few thousand years. But is civilization doomed?

Can we define civilization as a continuum? At the high end:
* there is some form of collective decision-making that respects factual information and serves everyone's long-term interests, to the extent possible,
* literacy is nearly universal, as is access to accurate scientific and historical information, and to differing opinions on politics, religion, etc.
* original research to increase scientific understanding and improve technology is encouraged
* criticizing the government or the dominant culture is not a crime
* those accused of crime are entitled to some form of due process based on public examination of the evidence

At the low end:
* good and services are exchanged mostly through voluntary trade, at least within groups, but groups war among themselves and individuals can be executed for "witchcraft", "blasphemy", or "sedition."

The question is, if some natural or man-made disaster (a major epidemic, say, or failure of moderates to vote) reduces civilization to a given level, somewhere between these extremes, which direction will it tend to change, over the next thousand years or so? Will within-group processes tend to increase or decrease civilization? Some current trends in the US are not encouraging.

What about between-group processes? Will countries that respect science and other secular values be strong enough (economically? militarily?) to impose their values on countries that rely on "God, guns and guts", or will it be the other way around?

July 23, 2011

Beneficial infections?

Endophytes are microbes (often fungi) that infect plants without causing obvious disease. Some endophytes appear to benefit their plant hosts. How do they do this, and why? I will introduce these questions before discussing this week's paper,(Redman et al. 2011) which shows dramatic benefits to rice from particular endophytes.

How might endophytes benefit plants? Mycorrhizal fungi extend out into the soil, where they can get phosphorus and other resources to give their plant hosts. In contrast, endophytes are typically found completely inside the plant, so any resources they "give" the plant must be modified versions of resources they got from the plant in the first place. Nitrogen is a possible exception -- rhizobia bacteria convert atmospheric nitrogen to forms plants can use, but the oxygen-sensitivity of the key enzyme apparently restricts this process to controlled-oxygen environments, such as legume root nodules.

Although endophytes don't have access to external resources, they can make chemicals the plant can't, such as toxins that protect the plant from being eaten. Or, they might make chemicals that the plant could make itself, but in larger amounts than the plant would otherwise make, at least at a particular time and place. For example, endophytes can make plant hormones, which could stimulate growth.

But what do we mean by "stimulate?" If all of the phosphorus, nitrogen, and carbon in the endophyte comes from the plant, any stimulation must result from the plant using its own resources differently than it would without the endophyte. In other words, the endophyte is manipulating the plant. For whose benefit? That leads to my second question.

Why do endophytes benefit plants? That is, why have endophyte strains that benefit their hosts more sometimes out-competed strains that benefit their hosts less, over the course of endophyte evolution? Mutant endophyte strains that don't make plant-defense toxins or (beneficial?) plant-manipulating hormones must arise. Making these chemicals uses resources the endophyte could otherwise use to reproduce more inside the plant. For strains that make beneficial chemicals to persist over evolution, they must have some advantage that outweighs this cost. I can imagine several ways in which beneficial endophytes might have an advantage.

The first is "group selection", with the group being all the endophytes inside an individual plant. Plants with more-beneficial endophytes grow more than plants with less-beneficial endophytes, and larger plants support more endophytes. If each plant contains only a single genotype of endophyte, this mechanism should work well. But defense of cacao leaves from pathogens was provided by a diverse community of endophytes.(Arnold et al. 2003) If a healthier shared host was the only benefit each endophyte received, wouldn't "free-rider" mutants that invest less in host defense tend to spread?(Denison et al., 2003b; Kiers and Denison 2008)

Maybe the endophytes make antifungal toxins mainly to kill each other, and defense against fungal pathogens is just a valuable side-effect. Such "byproduct mutualism" is an example of the second reason that more-beneficial endophytes may persist.

The third hypothesis is a minor variation on by-product mutualism. Endophyte infection is so common that plants may have evolved to depend on products produced by endophytes, even if the plants (or their ancestors) could produce those products themselves. For example, why might a plant be genetically programmed to make too little of some hormone that would maximize its reproduction? Perhaps because most of its ancestors were infected by endophytes producing that same hormone, so for the plant to make even more of it would have reduced fitness.

Third, maybe individual plants containing multiple strains of endophyte somehow favor the most-beneficial strains, reversing the benefit "free-riders" would otherwise have. Host sanctions against less-beneficial rhizobia(Kiers et al. 2003, Simms et al. 2006, Oono et al. 2011) and mycorrhizal fungi(Bever et al. 2009) have been reported, but is anything similar possible with endophytes?

Fourth, some apparent benefits to plants from endophytes may be misleading. Increased root growth may look like a benefit, but remember that the carbon and nitrogen in that root come from the plant, not the endophyte. So, at least in the short term, increased root growth usually comes at the expense of decreased shoot growth or more rapid depletion of reserves. For example, root-associated microbes that increase root growth of wheat can decrease final yield.(Kapulnik et al. 1987) Even if an endophyte-induced change in resource allocation increases seed production of plants growing individually in pots in a greenhouse, the same change might decrease seed production under competitive conditions in the field.

Now to this week's paper.(Redman et al. 2011) PLoS One is open access, so you can read the whole paper on-line. Regina Redman and colleagues inoculated rice with three different fungal endophytes, which had been isolated from plants growing under salt- or temperature-stress conditions. The fungi produced the plant hormone, IAA (auxin), at least in culture. This is consistent with manipulation of the host as a mechanism, although they didn't detect IAA in the plants themselves.

Although their focus was on stress tolerance, results under nonstress conditions were particularly interesting. Right after germination, infected and noninfected seedlings look similar (their Fig. 2). But after three days, the dry weight of three-day old seedlings not infected with endophytes averaged 60 milligrams (dry weight), while endophyte-infected seedlings averaged 105 mgDW (their Fig. 1). Both weights must include contributions from early photosynthesis, since rice seeds typically weigh only 20-30 mg. Somehow, the endophyte must have increased photosynthesis.

But how could the endophyte increase photosynthesis, if all the resources in the endophyte came from the plant? Actually, right after inoculation, the endophyte would still have some nitrogen and phosphorus acquired during culture. But would they have enough to share to significantly enhance early seedling growth?

Alternatively, the endophyte might have manipulated the plant into using its own resources differently than it would have without the endophyte. (We could call this manipulation "signaling" if the endophyte is providing the plant with useful information for mutual benefit,(Ratcliff and Denison 2011) but what information would an endophyte entirely inside a plant have that the plant itself wouldn't?)

For example, plants can photosynthesize faster if they open the stomatal pores in their leaves more, but that also uses up the soil water around their roots faster, increasing the risk of running out. Could an endophyte-induced increase in stomatal opening over-ride the plant's own water-use strategies? Sure, but what are the chances that the endophyte's strategy is better for the plant? That would seem unlikely, at least under the conditions where the plant evolved. But we wouldn't necessarily expect plant strategies that evolved in the field to be ideal in the greenhouse. A small change in either direction would have a 50% chance of being an improvement. Maybe the endophyte got lucky.

I've suggested increased stomatal opening as one way the endophyte could have increased seedling photosynthesis. Later in growth, however, endophyte-infected plants used less water than those without endophytes and took longer to wilt after watering (their Fig. 3). It's not clear, however, how much of the water use went through stomata, as opposed to evaporating from the soil surface. The endophyte-infected plants were much bigger than the noninfected plants by then, so they would have shaded the soil surface more.

As an alternative to greater stomatal opening, that about allocation to roots? Photos suggest that the noninfected seedlings initially invested more resources in shoots than in roots, whereas the endophyte-infected ones invested more in roots. If the endophytes infect mainly via the root, it's easy to understand why they might manipulate the plant to make more root. But why would plants have evolved to make too little root, when not infected by endophytes? Again, I see two likely possibilities. Maybe the plant's greater allocation to shoot is optimal for the conditions where it evolved(Denison et al. 2003, Denison in press) (germinating underwater in rice fields) but this gives too little root growth under the experimental conditions used in this study. This seems the most likely explanation. Alternatively, rice may be adapted to the presence of endophytes that produce similar hormones to those used in this study, so they have evolved to make hormone amounts that are suboptimal when not infected by endophytes.

Late in growth there were differences between treatments in reactive oxygen species, and the endophyte-infected plants had higher seed yields. The paper also shows beneficial effects on rice growth under low-temperature stress. But I would like to understand the benefits of the endophyte to three-day-old unstressed seedlings before getting into such details.

For practical applications, a more-complete understanding of how endophytes benefit plants would be useful, either to help us identify even better endophytes or to breed crops that get the same benefits with whatever endophytes they usually have now. Understanding endophyte evolution could be equally important. If it is some form of group selection that gives more-beneficial endophytes an edge over free-riders, can we maintain that process in agriculture? If some plant are imposing sanctions on less-beneficial endophytes, we certainly want to preserve that plant trait in our crop-breeding programs, or look for it in wild species and traditional crop cultivars.(Denison et al., 2003a, Denison in press) On the other hand, if endophytes are manipulating their plant hosts in ways that always benefit the endophyte, but which benefit the plant only under certain conditions, then we need to test endophytes under conditions more similar to how the crops will be grown in the field. In any case, this is a very interesting paper which (with related papers from the same group) could lead to exciting new approaches to improving crop production.


Arnold A. E., L. C. Mejia, D. Kyllo, E. I. Rojas, Z. Maynard, N. Robbins, and E. A. Herre. 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proceedings of the National Academy of Sciences USA 100:15649-15654.

Bever J. D., S. C. Richardson, B. M. Lawrence, J. Holmes, and M. Watson. 2009. Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism. Ecology Letters 12:13-21.

Denison R. F. in press. Darwinian agriculture: how understanding evolution can improve agriculture. Princeton University Press, Princeton.

Denison R. F., E. T. Kiers, and S. A. West. 2003a. Darwinian agriculture: when can humans find solutions beyond the reach of natural selection? Quarterly Review of Biology 78:145-168.

Denison R. F., C. Bledsoe, M. L. Kahn, F. O'Gara, E. L. Simms, and L. S. Thomashow. 2003b. Cooperation in the rhizosphere and the "free rider" problem. Ecology 84:838-845.

Kapulnik Y., Y. Okon, and Y. Henis. 1987. Yield response of spring wheat cultivars (Triticum aestivum and T. turgidum) to inoculation with Azospirillum brasilense under field conditions. Biology and Fertility of Soils 4:27-35.

Kiers E. T., R. F. Denison. 2008. Sanctions, cooperation, and the stability of plant-rhizosphere mutualisms. Annual Review of Ecology, Evolution, and Systematics 39:215-236.

Kiers E. T., R. A. Rousseau, S. A. West, and R. F. Denison. 2003. Host sanctions and the legume-rhizobium mutualism. Nature 425:78-81.

Oono R., C. G. Anderson, and R. F. Denison. 2011. Failure to fix nitrogen by non-reproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates. Proceedings of the Royal Society B :doi: 10.1098/rspb.2010.2193.

Ratcliff W. C., R. F. Denison. 2011. Alternative actions for antibiotics. Science 332:547-548.

Redman R. S., Y. O. Kim, C. J. D. A. Woodward, C. Greer, L. Espino, S. L. Doty, and R. J. Rodriguez. 2011. Increased Fitness of Rice Plants to Abiotic Stress Via Habitat Adapted Symbiosis: A Strategy for Mitigating Impacts of Climate Change. PLoS ONE :e14823.

Simms E. L., D. L. Taylor, J. Povich, R. P. Shefferson, J. L. Sachs, M. Urbina, and Y. Tausczik. 2006. An empirical test of partner choice mechanisms in a wild legume-rhizobium interaction. Proceedings of the Royal Society B 273:77-81.

July 15, 2011

Evolution of human cooperation

Two papers this week help explain why humans cooperate, even with nonrelatives. Cooperation with relatives (activities that tend to decrease one's own reproductive success, while increasing that of others likely to share many of one's genes) is predicted by "selfish gene" theory, as formalized in Hamilton's rule. I've assumed that cooperation with nonrelatives is a beneficial side-effect of behavioral genes that evolved when most of our neighbors were relatives, as is still the case in parts of the Amazon and West Virginia. But other explanations have been proposed.

One hypothesis is that "human cooperation evolved as a result of high levels of lethal competition (i.e. warfare) between genetically differentiated groups." In other words, some groups of unrelated individuals happened, by chance, to have a higher fraction of individuals whose genes tended to increase within-group cooperation -- particularly, willingness to risk injury in battles with other groups -- and the overall frequency of those genes increased as victorious groups killed groups that happened to have a lower frequency of "cooperation genes." This process would tend to be undermined by within-group evolution (assuming selfish individuals tend to have more descendants) and by migration between groups. The latter could include abductions.

But are genetic differences between groups big enough for this "group selection" mechanism to work? In "Genetic differentiation and the evolution of cooperation in chimpanzees and humans", recently published in Proceedings of the Royal Society, Kevin Langergraber and colleagues compared genetic differences among competing aboriginal human groups with differences among competing chimpanzee groups. They found that genetic differences among chimpanzee troops were at least as great as differences among human groups. So, if humans are more cooperative than chimps -- budget deadlocks in the US Congress and my state legislature call this into question -- it's probably not because group selection is more effective in humans than in chimps, in increasing the frequency of genes favoring cooperation. The authors suggest that "both genetic and cultural differentiation between groups played a role in the evolution of altruistic cooperation."

What sorts of cultural differences among groups might be important? This week's second paper, recently published in PNAS by Sarah Mathew and Robert Boyd, claims that "Punishment sustains large-scale cooperation in prestate warfare." This paper addresses the issue mentioned briefly above, the problem of within-group increases in selfishness (if selfish individuals have more descendants) undermining increases in cooperation from between-group processes. In particular, they asked whether individuals that deserted during battles between groups were punished.

The researchers obtained data for 88 raids involving the Turkana tribe, and found that: 1) the chance of a man being killed is >1% for each raid he participates in, 2) desertion or acts of cowardice occur in at least 45% of raids, and 3) these acts often lead to severe beatings, after group discussion. Getting beaten could certainly cause an individual to change his behavior, but what effect, if any, do such sanctions have on the frequency of genes that affect willingness to take risks in battle? Do those who fight bravely end up with more wives and, more important, more descendants? Unfortunately, "distinguishing the effect of behavior during warfare from the effect of other factors that affect a person's value as a social or mating partner is beyond the scope of the present study."

May 10, 2011

PDF available for our Perspective in Science

Science has kindly allowed us to link to a PDF of our recent Perspective, but only from one web page. So I've linked to it from last week's post.

April 28, 2011

Are antibiotics weapons, signals, cues, or manipulation?

"Do you expect me to talk?"
"No, Mr. Bond, I expect you to die!"
Sometimes, there are more than two possibilities.

Many bacteria make antibiotics which, in high doses, kill other bacteria. But microbiologists have noticed that, at lower doses, antibiotics may change gene expression or alter behavior, without killing. So, they suggest, maybe antibiotics are mainly "tools of communication," rather than weapons.

Maybe, but those are not the only possibilities. Will Ratliff and I have just published a short Perspective in Science suggesting that two other possibilities are more likely. A PDF is freely available here, courtesy of the journal.

If communication (or "signaling") implies mutual benefit, what about nonlethal effects of antibiotics that benefit receiver or sender, but not both? For example, a bacterium that detects an antibiotic may hide in a biofilm to escape from the antibiotic, just as a zebra that smells lions hides in a herd to escape predators. If hiding in the biofilm benefits the bacterium that detected the antibiotic, but not the bacterium that made it, we would call the antibiotic a "cue."

Or, suppose a bacterium making antibiotics benefits by scaring competitors into dispersing (or hiding in biofilms)? This could benefit the producer, by reducing competition, but harm the receiver. We would call that "manipulation."

To distinguish among these possibilities, we need to measure actual fitness consequences, to producer and receiver, of bacterial responses to antibiotics.

April 8, 2011

This week's picks

Workers influence royal reproduction
"worker aggressive and non-aggressive behaviour towards queens predicted which queen monopolized reproduction. In contrast, among-queen interactions were rare and did not predict queen reproduction. Furthermore, parentage analysis showed workers favoured their mother when present"
[Maybe "inclusive fitness" is useful after all!]

Updated chronology for the Miocene hominoid radiation in Western Eurasia
"Eurasian pongines [orangutans and extinct relatives] and African hominines [humans, chimps, bonobos, and extinct relatives] might have independently evolved in their respective continents from similar kenyapithecin ancestors [apes living 14 million years ago], resulting from an early Middle Miocene [5-23 MYA] intercontinental range extension followed by vicariance [geographic separation, reducing or eliminating interbreeding so allowing evolutionary divergence]. "

Ribozyme-Catalyzed Transcription of an Active Ribozyme "we recombined traits evolved separately in different ribozyme [catalytic enzyme made of RNA rather than protein] lineages. This yielded a more general polymerase ribozyme that was able to synthesize a wider spectrum of RNA sequences, as we demonstrate by the accurate synthesis of an enzymatically active RNA, a hammerhead endonuclease ribozyme. "

An evolutionary process that assembles phenotypes through space rather than through time "assortative mating between fast-dispersing individuals at the invasion front results in an evolutionary increase in dispersal rates in successive generations"

Fork-tailed drongos use deceptive mimicked alarm calls to steal food
"false alarm calls when watching target species handling food, in response to which targets flee to cover abandoning their food"

Moving calls: a vocal mechanism underlying quorum decisions in cohesive groups
"a sharp increase in the probability of changing foraging patch when the number of group members joining the chorus increased from two up to three"

Differences in the temporal dynamics of phenotypic selection among fitness components in the wild "The consistency in direction and stronger long-term average strength of selection through mating success and fecundity suggests that selection through these fitness components should cause more persistent directional evolution relative to selection through survival."

Rapid Spread of a Bacterial Symbiont in an Invasive Whitefly Is Driven by Fitness Benefits and Female Bias "Rickettsia sp. nr. bellii swept into a population of an invasive agricultural pest, the sweet potato whitefly, Bemisia tabaci, in just 6 years. Compared with uninfected whiteflies, Rickettsia-infected whiteflies produced more offspring, had higher survival to adulthood, developed faster, and produced a higher proportion of daughters. The symbiont thus functions as both mutualist and reproductive manipulator. "

The evolutionary biology of child health "cancer, the primary cause of non-infectious childhood mortality, mirrors child growth rates from birth to adolescence, with paediatric cancer development impacted by imprinted genes"

Tradeoffs associated with constitutive and induced plant resistance against herbivory "Across all 58 plant species, we demonstrate a tradeoff between constitutive and induced resistance, which was robust to accounting for phylogenetic history of the species. Moreover, the tradeoff was driven by wild species and was not evident for cultivated species."

Towards a quantitative understanding of the late Neoproterozoic carbon cycle
"all of the main features of the carbonate and organic carbon isotope record can be explained by the release of methane hydrates from an anoxic dissolved organic carbon-rich ocean into an atmosphere containing oxygen levels considerably less than today"

March 31, 2011

This week's picks

Chimpanzees help conspecifics obtain food and non-food items "...given that the donor cannot get the food herself.... the key factor... is the recipients' attempts to either get the food or get the attention of the potential donor."

On the earliest evidence for habitual use of fire in Europe
"...spectacular cases of Neandertal pyrotechnological knowledge..."

Sizing up your enemy: individual predation vulnerability predicts migratory probability
"trade-off between seasonal fluctuations in predation risk and growth potential... Smaller, high-risk individuals migrate with a higher probability"

Plant-ants feed their host plant, but above all a fungal symbiont to recycle nitrogen
"In many ant-plant symbioses, a fungal patch grows within each domatium."

More closely related species are more ecologically similar in an experimental test
"Species also competed more with close relatives than with distant relatives in field soils; however, in potting soil this pattern reversed..."

Assassin bug uses aggressive mimicry to lure spider prey "vibrations from bugs had a temporal structure and amplitude... similar to vibrations generated by leg and body movements of prey and distinctly different... from courting males or leaves..."

Social and Ecological Synergy: Local Rulemaking, Forest Livelihoods, and Biodiversity Conservation "participation in forest governance institutions by local forest users is strongly associated with jointly positive outcomes"

Oxygen isotopes of East Asian dinosaurs reveal exceptionally cold Early Cretaceous climates "cold local climatic conditions linked to the paleolatitudinal position of northeastern China and global icehouse climates..."

Adaptation to local ultraviolet radiation conditions among neighbouring Daphnia
"we separated the effects of shared population ancestry and environmental variables in predicting phenotypic divergence among populations."

March 25, 2011

Inclusive fitness defended

Last year, I critiqued a paper arguing that inclusive fitness (reproduction by individuals who are more likely than the overall population to share alleles with a focal individual) isn't a useful concept. I disagreed, as did a lot of other blogging scientists.

This week, a significant fraction of the world's leading evolutionary biologists published letters in Nature in support of inclusive fitness, both as it applies to social insects and more generally. But the Templeton Foundation apparently liked the paper belittling the inclusive fitness concept and is giving the one of the authors millions of dollars to study "teleology and ultimate purpose in the context of evolutionary biology." More discussion at Why Evolution is True and The Loom.

February 24, 2011

This week's picks

Responses to the Assurance game in monkeys, apes, and humans using equivalent procedures "...only a subset of humans achieved these efficient outcomes, and pairs of both other species did so as well"

The origin and dynamic evolution of chemical information transfer
"chemicals are emitted, which can unintentionally provide information (cues) and... act as direct precursors for the evolution of intentional communication (signals)."
"In most cases, the excrements are cues, but the behavioural modulations... constitute signals helping to draw receivers' attention to the cues "
"males prefer flower bouquets to the sexual pheromone of local females, presumably because [the orchid] exploits pre-existing sensory biases of their pollinators"

Classic Selective Sweeps Were Rare in Recent Human Evolution
"amino acid and putative regulatory sites are not significantly enriched in alleles that are highly differentiated between populations"

Archaeal phylogenomics provides evidence in support of a methanogenic origin of the Archaea and a thaumarchaeal origin for the eukaryotes
"the Thaumarchaea (including Nitrosopumilis maritimus in our analysis) forms an independent group distinct from the Crenarchaea or Euryarchaea"

Footprints pull origin and diversification of dinosaur stem lineage deep into Early Triassic "...a few million years after the Permian/Triassic mass extinction (252.3 Ma)"

Optimal antiviral treatment strategies and the effects of resistance
"contrary to previous results, it is always optimal to treat at the maximum rate provided that this treatment occurs at the right time. "

Resolving the infection process reveals striking differences in the contribution of environment, genetics and phylogeny to host-parasite interactions
"transparent Daphnia hosts and fluorescently-labelled spores of the bacterium"

February 10, 2011

Evolution of cooperation, disease, relatives, birds...

Some recent papers that look interesting:

The evolution of host protection by vertically transmitted parasites

Cooperation among non-relatives evolves by state-dependent generalized reciprocity

Before senescence: the evolutionary demography of ontogenesis

Costs of memory: lessons from 'mini' brains

Land inheritance establishes sibling competition for marriage and reproduction in rural Ethiopia

Major global radiation of corvoid birds originated in the proto-Papuan archipelago

Within and transgenerational immune priming in an insect to a DNA virus

Multiple strategies in structured populations

Long-term isolation of a highly mobile seabird on the Galapagos

January 26, 2011

Plants punish cheaters' relatives

This week's paper is the fourth from Ryoko Oono's PhD thesis. "Failure to fix nitrogen by non-reproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates" was just published on-line in Proceedings of the Royal Society.
Rhizobia are bacteria that can live either in soil or in root nodules, like those shown above. Legume plants (alfalfa, soybean, the lupines loved by Monty Python and many wild species) let rhizobia in because the rhizobia (usually) convert atmospheric nitrogen into forms the plant can use.

But what if the rhizobia don't deliver? What if, once established inside a nodule, they use plant resources only for their own reproduction? In my most-cited paper, Toby Kiers showed that soybean plants impose fitness-reducing "sanctions" on rhizobia that fail to fix nitrogen. Ellen Simms' lab found similar results with wild lupines. But Ryoko had three good reasons to question whether certain legumes, including alfalfa and pea, impose sanctions similar to soybean's.

Continue reading "Plants punish cheaters' relatives" »

January 12, 2011

Making symbiotic rhizobia more efficient

This week I'll discuss a recent paper by Ryoko Oono, one of five from her PhD work. (If you want to hire her as a postdoc, better hurry!) Comparing Symbiotic Efficiency between Swollen versus Nonswollen Rhizobial Bacteroids, published in Plant Physiology, is available for anyone to read on-line.

Here's a little background. Rhizobia are soil bacteria, best known for infecting the roots of legume plants (clover, lupine, bean, pea, alfalfa, and many others) and multiplying inside root nodules, where they "fix" nitrogen gas from the atmosphere, converting it into forms their plant hosts can use, instead of relying on fertilizer.

Thumbnail image for AlfalfaNodules2.jpg

Left: Alfalfa nodules; copyright Inga Spence, used by permission. Below left: nonswollen bacteroids. Below right: swollen bacteroids.
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Apparently, rhizobia in the soil never fix nitrogen. Inside root nodules, however, some of them develop into bacteroids, which use some of the plant-supplied carbon they consume to power nitrogen fixation. They may also hoard some carbon for their own future survival and reproduction, a possible source of conflict with their host.

In nodules of some legume hosts, including pea and alfalfa, bacteroids are swollen (above right) and have lost the ability to reproduce. In other hosts, bacteroids don't look that different from the free-living rhizobia, and retain the ability to reproduce. Why this difference?

Continue reading "Making symbiotic rhizobia more efficient" »

December 12, 2010

Conditional cooperation and forest management

A while ago, I asked readers which of several papers they would most like me to discuss. The only request was for a paper which, though related to my own interests in the evolution of cooperation, isn't exactly evolutionary biology, "Conditional cooperation and costly monitoring explain success in forest commons management". I decided to discuss it anyway. Anyone particularly interested in the tragedy of the commons might also find some older posts in my moribund blog, The Comedy of the Trojans, worth reading.

Continue reading "Conditional cooperation and forest management" »

November 15, 2010

Lengthy comment on group selection

Someone left a comment on an old post about group selection, here. Its length and use of an apparent pseudonym make me suspect cut-and-paste, in which case I'll delete it. IT WAS SO I DID.

See also this recent post.

November 12, 2010

So many papers, so little time

Here are the papers I'm considering this week. Any requests? Otherwise, I'll probably discuss one of my own recent papers, on the implications of evolutionary tradeoffs for agriculture and human health.
Why genes overlap in viruses

Identification of an ant queen pheromone regulating worker sterility

DDS, 4,4′-diaminodiphenylsulfone, extends organismic lifespan

Evolutionary history of partible paternity in lowland South America

The evolution of cultural adaptations: Fijian food taboos protect against dangerous marine toxins

Conditional Cooperation and Costly Monitoring Explain Success in Forest Commons Management

Periodic climate cooling enhanced natural disasters and wars in China during AD 10-1900

A climate for contemporary evolution

The evolution of menopause in cetaceans and humans: the role of demography

Prosocial behaviour emerges independent of reciprocity in cottontop tamarins

Fossilized glycolipids reveal past oceanic N2 fixation by heterocystous cyanobacteria

October 26, 2010

Mutualisms in a changing world: an evolutionary perspective

That's the title of a review article recently published in Ecology Letters. Authors include Toby Kiers, who did a PhD with me a few years ago, and Judy Bronstein, who visited UC Davis when I was just starting to work on evolution of cooperation and told me about some key papers in the field.

"I use this term ["struggle for existence"] in a large and metaphorical sense including dependence of one being on another, and including (which is more important) not only the life of the individual, but success in leaving progeny" -- Darwin

Climate change, pollution, hunting, and introduced species can have direct effects on endangered species, but what about indirect effects? For example, a wild plant species, growing alone, might produce fewer seeds when exposed to higher temperatures. But if higher temperature hurts the plant's competitors or pests enough, the resulting indirect decreases in competition or pest damage might outweigh direct negative effects. On the other hand, a plant that depends on animals for seed dispersal could suffer more seed predation, as shown below, if climate change or over-hunting reduces disperser numbers, even if climate change and hunting have no direct effect on the plant itself.
Coleoptera larva attacks the fruit of Iriartea deltoidea in western Amazonia. Over-hunting of seed dispersers has resulted in huge caches of undispersed seeds at parental trees, vulnerable to attack by various pests. Photo: Patricia Alvarez.

This week's paper adds evolution to the already complex problem of mutualism (cooperation between species) in changing environments. For example, what if the timing of flowering and the emergence of a pollinating insect both depend on temperature, but in different ways? Then climatic change may reduce pollination, at least in the short run. Both species will continue to evolve, however, which could bring them back into sync -- unless the pollinators switch to a different host whose flowering time fits their new schedule!

Continue reading "Mutualisms in a changing world: an evolutionary perspective" »

October 8, 2010

Why do leaves really track the sun?

This week I'll discuss one of my own papers, "Individual fitness versus whole-crop photosynthesis -- solar tracking tradeoffs in alfalfa", which was recently published in the Evolutionary Applications special issue on Agriculture.
The alfalfa leaf at the right is brightly illuminated because it is facing directly towards the sun, an orientation it maintains by turning slowly over the day. By tracking the sun, this leaf captures more sunlight, so it might be expected to photosynthesize more. On the other hand, the leaf is partly shaded by another leaf, which casts a bigger shadow because it, too, is tracking the sun. This increased shading of lower leaves by upper leaves would tend to reduce overall photosynthesis.

Does increased shading outweigh the photosynthetic benefits of tracking?

Continue reading "Why do leaves really track the sun?" »

September 22, 2010

Garbage in, garbage out, in modeling symbiosis

Every year or two, someone publishes a computer model showing how easy it would be for cooperation between species to evolve, if only the world were fundamentally different than it actually is. In particular, many models incorrectly assume that there is only one symbiont genotype per host individual.

The latest paper to make this incorrect assumption was published in Proceedings of the National Academy of Science, and titled "Economic contract theory tests models of mutualism." The paper admits that:

"the fact that legumes are often infected by multiple strains of rhizobia [symbiotic bacteria that provide plants with nitrogen] remains a problem, because our model assumes only one type of agent."
Similarly, each individual plant typically interacts with several different mycorrhizal fungi and many different pollinators. How much difference does this make? Enough difference to completely reverse their conclusions that "positive feedback between host fitness and symbiont fitness is sufficient to prevent cheating."
We showed in 2002 that symbionts that benefit their hosts more would out-compete those that benefit their hosts less (even in the absence of "host sanctions", discussed below), if there were only one symbiont genotype per host (above right). That is the situation incorrectly assumed by Weyl et al. (2010). In the real world, however, with multiple symbionts per host, strains that divert more host resources to their own reproduction would win (above left). For rhizobia, if nitrogen is readily available in the soil (s=0.5), then as few as two strains per host is enough to undermine cooperation, unless hosts impose sanctions on cheaters. Source: West et al. (2002) "Sanctions and mutualism stability: why do rhizobia fix nitrogen?" Proc. Roy. Soc. B 269:685-694.

Weyl et al. (2010) is one of the 100+ papers to cite our 2002 paper, but the critical importance of multiple symbionts per host doesn't seem to have sunk in. If you're looking for a model that represents an actual advance on our 2002 paper, rather than an embarassing retreat, I recommend Maren Friesen's "Mixed infections may promote diversification of mutualistic symbionts: why are there ineffective rhizobia?", J. Evol. Biol. 23:323.

West et al. (2002) also showed that then-hypothetical "host sanctions" imposed by legume plants against symbiotic rhizobia that fail to provide them with nitrogen can prevent the evolutionary breakdown in rhizobial cooperation shown above. Toby Kiers subsequently showed that soybean plants, at least, do actually impose such sanctions on individual root nodules that fail to provide the host with nitrogen ("Host sanctions and the legume-rhizobium mutualism", Nature 425:78). But, Friesen and Mathias asked, what if some nodules contain more than one genotype of rhizobia? Depending on the frequency of mixed nodules, they showed that rhizobial "cheaters" can coexist with more-beneficial strains.

August 31, 2010

There's much more to Hamilton's rule than haplodiploidy

Updated 27 October 2010: Evidence for kin selection's role in the evolution of eusociality in insects includes ancestral-state reconstruction showing that all eusocial species are descended from ancestors with monogamous queens, which increased within-colony relatedness. See this earlier post.

A recent paper in Nature, challenging an obsolete explanation for the evolution of eusociality (characterized by nonreproductive individuals, like worker bees), may be misinterpreted as evidence against Hamilton's rule.

Hamilton's rule, you may recall, is that alleles (gene variants) for altruistic behavior (increasing another's fitness in ways that reduce one's own) will spread if, on average:
c < b r
that is, if the fitness cost to the altruist is less than the fitness benefit to the recipient, times the extent to which the recipient is more likely (relative to the population with which they compete) to have the same altruism allele. Often, this increased likelihood of sharing the same gene is due to genetic relatedness.

The haplodiploid genetic system used by ants and bees means that a worker can be more likely to share alleles with her sisters (r=0.75, relative to unrelated individuals) than with her own offspring (r=0.5). It was once suggested that this could explain why worker ants care for their sisters (the queen's daughters) rather than having offspring of their own. But then someone pointed out that Hamilton's r between a sister and a brother is only 0.25. So, if the queen has equal numbers of sons and daughters, there's no reason for workers to favor siblings over their own offspring. The central point in this new paper, that haplodiploidy doesn't necessarily lead to eusociality, is therefore both consistent with Hamilton's rule and old news.

I'm not sure how long we've known this, but The Selfish Gene, published more than 30 years ago, mentions the low Hamilton's r of 0.25 for brothers and focuses, not on any link between haplodiploidy and eusociality, but rather on conflict between workers and queen over the sex ratio of the latter's offspring. In particular, Dawkins discussed work by Trivers and Hare, who used Hamilton's rule to predict a 3:1 female:male ratio in most ants but a 1:1 ratio in slave-making species, predictions that were confirmed by field observations.

Carl ZImmer's discussion of this paper in the New York Times includes comments from Andy Gardner, a leading evolutionary theorist:

"This is a really terrible article." One problem Dr. Gardner points to is the Harvard team's claim that the past 40 years of research on inclusive fitness has yielded nothing but "hypothetical explanations."
"This claim is just patently wrong," Dr. Gardner said. He points to the question of how many sons and daughters mothers produce among the many insights inclusive fitness has brought.

Jerry Coyne (author of Why Evolution is True) didn't like the paper either.
Nor did Richard Dawkins.
Or Jeremy Joder.

July 31, 2010

Evolutionary history of yucca moths

I've written a few posts about ancestral-state reconstruction, where we use molecular or other information from living species to infer the traits of their shared ancestors. But I really like this post in which PhD student Jeremy Yoder describes his own work.

There's a nice diagram showing the general approach, then he looks at yucca moths and their relatives to figure out what their ancestors did. Yucca moths, like fig wasps, lay their eggs in flowers. Their larvae eat seeds, but the moths pollinate the flowers, so it's not too bad a deal overall. Their ancestors, he concludes, fed inside developing flowers, but without pollinating them. Maybe the world is getting a little more cooperative, after all.

July 1, 2010

Earliest multicellular life? Maybe not.

This week's paper is "Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago", published in Nature by Abderrazak El Albani and colleagues. These two-billion-year-old fossils are clearly the remains of something living, based on appearance, different carbon isotope composition from the surrounding rock. But are they colonies of unicellular organisms, or something more organized?

The authors note the resemblance to "bacterial colonies growing on surfaces" which they say are known to "coordinate their behavior" often via "repulsive chemotaxis." In other words, cells detect the presence of neighbors and tend to disperse in ways that can generate patterns similar to those seen in these fossils. Sometimes, bacteria may coordinate their activities in more sophisticated ways, which wouldn't leave fossil traces.

A commentary on the article is titled "Origins of multicellularity", but most people would expect more from a multicellular organism than a little coordination among cells. We expect differentiation, for example, where different cells specialize for different functions. Trichoplax is thought to have four different cell types, including cells with flagella that move these simple multicellular animals along, and cells that excrete digestive enzymes. In larger animals, a few cells specialize in reproduction, a potential source of conflict, especially if there are genetic differences among cells. I don't think we can tell from these fossils whether there was any such specialization.

A consistent size and shape is another criterion for true multicellularity, met by Volvox, for example. The fossils don't look any more consistent in size and shape than one would expect from bacterial colonies. On the other hand, Trichoplax individuals seems to vary somewhat, but I wouldn't argue against calling them multicellular organisms.

Interestingly, the authors found traces of the chemical sterane, which is typically found in eukaryotes. But apparently there's some possibility that it could have diffuses into the fossil rock from younger materials.

I've been reading about multicellularity recently and was particularly impressed by a 1998 paper by Boraas et al., in Evolutionary Ecology, and titled "Phagotrophy by a flagellate selects for colonial prey: a possible origin of multicellularity". (I would link to the paper, but the publisher Springer has this stupid system that sends you to their main web page.) Boraas et al. exposed unicellular algae to predators and evolved multicellular clumps in only 10-20 generations. The first clumps contained hundreds of cells, but eventually they evolved an 8-cell phenotype, too big for the predators to eat, but with better access to nutrients for each cell than if they were in a larger clump. Surprisingly, nobody seems to have done further evolution experiments with this system.

June 25, 2010

Are scientists smarter than squirrels?

"Monkey-watchers often use the word "aunt" for an adopting female." -- Richard Dawkins, The Selfish Gene
The willingness of animals to adopt and care for orphans has been shaped by past natural selection. Often, Dawkins suggested, adoption represents "misfiring of a built-in rule... a mistake that happens too seldom for natural selection to have 'bothered' to change the rule by making the maternal instinct more selective." This seems a reasonable explanation for the failure of bird parents to kick "brood parasites" out of their nests, a situation I discussed recently.

But this week's paper, by Jamieson Gorrell and colleagues, seems to show that squirrels have a more-sophisticated understanding of selfish-gene theory than I would have expected. "Adopting kin enhances inclusive fitness in asocial red squirrels" was recently published in the new online journal Nature Communications. The authors analyzed five cases of orphaned squirrels being adopted, all by close relatives, and two cases where they were left to die, even though a relative had a territory nearby. In each case, they asked whether adopting would likely increase or decrease the frequency of the adopter's genes in future generations.

Closely related individuals tend to share gene variants (alleles) even if those alleles are rare in the overall population, so adopting a younger sister or a nephew who would otherwise die could increase one's genetic representation in future generations. On the other hand, adding an orphan to one's litter puts one's own offspring at somewhat greater risk. The authors were able to estimate this risk and compare it to the increased survival chances of the adoptee, weighted by its relatedness to the foster mother. If this benefit exceeds the risk, then Hamilton's rule (the fundamental equation of social evolution) predicts adoption. All of the adoptions that did occur met this criterion -- two cases were right on the line -- whereas the two potential adoptions that didn't occur failed the Hamilton's-rule test. Yet another example of squirrels solving challenging problems.

At least, that's what the data seemed to show. But the "relatedness" term in Hamilton's rule isn't necessarily equal to the relatedness we could calculate from a family tree or from genetic similarity. It would be, if helping an orphan had no negative effect on anyone outside one's current litter. But if there are more red squirrels than red-squirrel territories, then a surviving orphan may end up displacing another squirrel. So the question is, how closely related is that displaced squirrel likely to be to the adoptive mother? In the cases studied, 1/4 to 1/2 of the lactating females nearby were kin to the adopting mother. If that's a representative sample, then a surviving orphan might often end up displacing another squirrel that was as closely related to the mother as the orphan was. In such cases, the mother would have exposed her own litter to increased risk, without doing much to increase her genetic representation in future generations. Even so, the adoptive mothers aren't acting as maladaptively as Dawkins suggested (as if they adopted orphans at random), but their behavior wouldn't be optimal (by Hamilton's rule) unless there were unoccupied territories available nearby. Thanks to Dr. Carin Bondar, whose blog alerted me to this interesting paper.

Meanwhile, over at Science, Jeff Smith and colleagues propose "A generalization of Hamilton's rule for the evolution of microbial cooperation." When one cooperative act (releasing an expensive enzyme, say) benefits all microbes nearby, it's common to assume we can add up all the costs and benefits over a population. But what if twice the enzyme gives three times the benefit? The authors developed some high-powered math to deal with such problems and concluded that certain kinds of cheaters would have a harder time getting established than we would have expected from the simpler version of Hamilton's rule. Scientists are definitely smarter than squirrels, but they can't jump as well.

June 4, 2010

Cancer's deep evolutionary roots

This week's paper, "Phylostratigraphic tracking of cancer genes suggests a link to the emergence of multicellularity in metazoa" was published in BMC Biology by Tomislav Domazet-Lošo and Diethard Tautz. Each of our cells is descended from an unbroken lineage going back to the first living cell. Most cells in an adult, however, are at the end of the line and will have no descendants. Exceptions include sex cells, stem cells, and cancer cells.

We consider cancer an aberration, but think back to the first multicellular life, which may have resembled Trichoplax. A Trichoplax has an upper and a lower layer of cells, and not much in between. They can reproduce by dividing in half, producing two offspring with hundreds of cells each (video). Or they can bud off propagules containing a small number of cells. They also seem to be able to reproduce sexually, from a fertilized single-cell egg, although complete development from an egg hasn't been documented. A Trichoplax can reform from separated cells, sometimes combining cells from two individuals. In such a chimeric organism, cells with different genotypes could compete for resources and reproductive opportunities, undermining collective success. Similar problems can occur when social amoebae get together to form a stalk for their spores. Even in a genetically uniform organism, a mutant cell could start reproducing (perhaps generating many propagules) at the expense of the whole. Today, we call cells that reproduce at the expense of the whole cancers, but something similar would presumably have been a problem for the earliest multicellular organisms.

Presumably? The authors of this week's paper used "phylostratigraphic tracking" to see when the ancestors of our cancer-suppressing genes evolved. Sure enough, there was an evolutionary burst of such genes right around the time when multicellular animals first evolved.

May 21, 2010

It's not all junk -- and it evolves!

We've known for a long time that most human DNA doesn't code for protein, that much of that noncoding DNA is junk (former genes that no longer do anything, multiple copies of selfish "jumping DNA", etc.), but that some noncoding DNA performs useful functions. Click "junk DNA" at right for past posts on this topic. This week's paper, Adaptive Evolution of an sRNA That Controls Myxococcus Development (published in Science by Yuen-Tsu N. Yu, Xi Yuan, and Gregory J. Velicer), is an example of how such functions can evolve.

Myxococcus xanthus is a "social bacterium", whose behavior somewhat resembles that of the "social amoeba", Dictyostelium. When starved, the individual bacterial cells get together in a mound and form spores. Previously, Velicer's group found a mutant that doesn't do this. Then a second mutation arose in that line that restored the original behavior. Now they report the molecular basis for this restored spore-forming ability. The product of the key gene turns out to be small RNA molecule. Its normal function is apparently to block aggregation and spore formation, except when starved. The new mutation essentially knocks out this function, restoring the ability to make spores, but without the normal link to starvation.

May 19, 2010

15 minutes of fame

Science writer Carl Zimmer has posted his "Meet the Scientist" podcast interview with me on the Microbe World web page.

A story about our PLoS One paper was 2010's most-viewed research report on the University of Minnesota web page.

Separately, my PhD student, Will Ratcliff, was one of four students featured on the University of Minnesota web page. In the video (upper right, labeled "Multimedia"), he alternates with three social scientists.

May 6, 2010

Do legume hosts benefit from suppressing rhizobial reproduction?

This week's paper is by my PhD student Ryoko Oono, with major contributions from Imke Schmitt (University of Minnesota faculty) and Janet Sprent, who was an expert on legume-rhizobium evolution long before I started working on the problem.

"Multiple evolutionary origins of legume traits leading to extreme rhizobial differentiation" has been published on-line in New Phytologist.

Rhizobia are soil bacteria, but a lucky few accept invitations from legume plants to infect their roots, multiply a million-fold or more inside a nodule, and then convert ("fix") atmospheric nitrogen into a form that the plant can use. When the plant dies (or sometimes sooner), an unknown fraction of the rhizobia in each nodule escape back into the soil.

Below left is what rhizobia look like in the soil and in the nodules of some legume hosts, including soybean. In other hosts, including pea, they swell up and/or change their shape (below right, same scale) as they differentiate into the nitrogen-fixing bacteroid form. The swollen form is apparently nonreproductive (like worker bees), but copies of their genes can still end up back in the soil. This is because some of their clonemates in the same nodule haven't become bacteroids yet and so retain the ability to reproduce, like queen bees.
The extreme differentiation shown above right is imposed by the legume host. But why? Are swollen bacteroids somehow more beneficial to the plant? Or are bacteroid swelling and their losing the ability to reproduce side-effects of some other process that may or may not benefit the plant?

Ryoko reasoned that, if a plant trait has evolved repeatedly over the course of evolution, then it is probably beneficial to the plant. On the other hand, a trait that has been abandoned repeatedly is probably harmful. But has either of these happened?

Continue reading "Do legume hosts benefit from suppressing rhizobial reproduction?" »

April 16, 2010

Sanctions and cheating in pollination and protection mutualisms

The most-cited paper from my lab is one by Toby Kiers, showing that soybean plants impose fitness-reducing sanctions on "cheating" rhizobia, which multiply inside root nodules but then fail to provide their hosts with nitrogen. This week I will briefly discuss two recent papers on the role of sanctions in two different kinds of mutually beneficial interactions between species.

Toby is also one of the coauthors on the first paper by Ryutaro Goto and others. The author/year citation (Goto 2010 ) reminds me of programming computers in Fortran, but the full title is "Selective flower abortion maintains moth cooperation in a newly discovered pollination mutualism." The second paper, by David Edwards and others, discusses ants that protect trees from browsing animals. This paper asks, "Can the failure to punish promote cheating in mutualism?"

Clochidion trees in Japan are pollinated by moths. Like the moths that pollinate yuccas and the wasps that pollinate figs, these moths lay eggs as they pollinate, and their larvae then consume some seeds. What keeps the moths from laying too many eggs in a given flower?

Continue reading "Sanctions and cheating in pollination and protection mutualisms" »

February 25, 2010

Evolution of symbiosis

This week's paper is "Experimental Evolution of a Plant Pathogen into a Legume Symbiont" published recently in PLoS Biology by Marta Marchetti and colleagues.

It's not hard to convert a highly beneficial rhizobium, which infects legume roots and provides them with nitrogen, into a slightly harmful one -- just knock out the nitrogen-fixation gene and you get a bacterium that has some cost to its host but provides no benefit in return. But how hard is it for a bacterium that causes disease to evolve into a beneficial bacterium?

One process that sometimes happens in nature is the wholesale "horizontal" transfer of a gene (or many linked genes) from one microbe to another. So the authors of this week's paper started by transferring the symbiotic plasmid (a loop of DNA with genes for infecting roots and then fixing nitrogen) into a plant pathogen.

Continue reading "Evolution of symbiosis" »

January 17, 2010

Altruistic punishment by fig trees?

As I was getting ready to write about some of the talks at the Applied Evolution Summit, I received a very interesting paper: Host sanctions and pollinator cheating in the fig tree - fig wasp mutualism, which was recently published in Proceedings of the Royal Society by Charlotte Jander and Allen Herre.

Fig-tree fruits are lined with many little flowers. Female wasps crawl inside to lay their eggs, often carrying pollen from the fig where they, themselves, hatched from an egg. Different fig species host different wasp species. Some wasp species are like many other pollinators, carrying pollen only by accident; fig trees pollinated by these species have to make lots of pollen. Other figs are pollinated by wasps that actively collect pollen and actively pollinate flowers inside fig fruits; these fig species can make less pollen, which frees resources to make more seeds.

But there is presumably some cost to the wasps of transporting pollen. Why not save this cost, travel light, and lay eggs in a fig fruit without pollinating its flowers? This is essentially the same question people in my lab have asked about rhizobia, the bacteria that provide legume plants with nitrogen: once rhizobia have reproduced inside a root nodule, why stick around and invest resources in pulling nitrogen out of the atmosphere and converting it to a form the plant can use?

The questions are similar and so are the answers....
Wasp inside a fig; photo by Charlotte Jander.

Continue reading "Altruistic punishment by fig trees?" »

August 27, 2009

Are antibiotics a weapon or a signal?

(Guest blog by my PhD student, Will Ratcliff)

If we get a nasty bacterial infection, we all know to go to the doctor for antibiotics. Few of us stop to think of where these antibiotics come from, which is too bad, because their origin is rooted in the stuff of a James Bond film: bloodsport and espionage. Scientists put a few different microbes on a Petri plate, let them duke it out, and then steal the chemical secrets of the victorious strain. Antibiotics are thus considered by most microbiologists to be pure weaponry, honed by natural selection for the most effective killing (or disabling) of competitors at the lowest cost.

But some recent papers suggest a new hypothesis: antibiotics are actually signaling molecules that happen to be toxic at high doses (Mlot 2009). As evidence for this view, researchers note that microbes exposed to antibiotics at sublethal concentrations don't simply shrug off the insult and go about their business: they react. Some bacteria turn on their SOS response, some make biofilms, some fail to make biofilms, some get less virulent (Shank and Kolter 2009), and yet others more virulent (Linares et al. 2006). These responses appear to vary among species without a general pattern.

So are antibiotics serving as a weapon or a signal?

Let's start at square one: what do they mean by signal? Many of the papers in this literature seem to use signal to mean "molecule produced by species A that elicits a response in species B other than death". But to evolutionary biologists, it matters why species A produces the signal and why species B reacts as it does....

Continue reading "Are antibiotics a weapon or a signal?" »

August 7, 2009

Ants versus fungi

Ants that grow fungi for food have to control other fungi that attack their gardens, but what about fungi that attack the ants themselves? Two papers published recently reveal surprising sophistication in both ants and fungi.

Sandra Anderson and colleagues discuss "The life of a dead ant: the expression of an adaptive extended phenotype" in American Naturalist. Richard Dawkins coined the term "extended phenotype" to refer to a consistent effect of a gene inside an individual on something outside that individual. For example, it might be possible to link differences in the shape of webs made by different spiders to genetic differences among those spiders. This week's paper shows that ants infected by certain fungi show complex behavior that benefits the fungi. Ants infected by fungi with different genes would probably not show this behavior, but the genes involved have not yet been identified.

Before the fungus-infected ants die, they attach themselves (by biting) to the underside of leaves that are ideally located for fungal reproduction: on the cooler and moister north side of trees, near (but not on) the ground. The researchers showed that these locations were favorable for fungal reproduction by moving infected ants higher in the canopy or down to the ground. Ants on the ground mostly disappeared, but fungi grew abnormally in those that remained. Fungi were unable to compete their life-cycle on ants moved higher in the canopy.

I can imagine a fungus producing an ant hormone (or perhaps destroying a particular neuron) to make its ant host bite a leaf, but getting ants to bite leaves in a particular humidity and temperature range and then hold on until dying seems pretty sophisticated. It would be easier if the ants spent most of their time in that zone anyway, but the one ant colony they found was much higher, about 15 meters.

The second paper shows greater sophistication on the part of the ants. "Adaptive social immunity in leaf-cutting ants" was published by Tom Walker and William Hughes in Biology Letters. The paper is freely available on-line.

These social ants protect each other from fungal infection by grooming each other, much like meerkats or baboons. Ants exposed to the fungus got groomed about twice as long as ants exposed to a control solution without the fungus, or about three times as long if their nest had been exposed to the same fungus two days before. (Another example of learning in insects.) Ants placed in nests that were previously exposed to the fungus were twice as likely to survive for two weeks after they were inoculated.

July 31, 2009


Just as I was starting to dip into retirement savings to keep my lab going, we got word that both of the grant proposals we sent to the NSF in the latest round were funded, one of them with money from Obama's stimulus funding. We won't be paying ourselves any billion-dollar bonuses, but I may be able to get two months salary this year after all. Both proposals are resubmissions, significantly improved based on suggestions and criticisms from past reviewers. Both projects will use rhizobia, bacteria best known for providing legume plants with nitrogen, but the second project may have eventual applications in medicine (e.g., curing persistent infections) rather than agriculture. The summaries below are intended for a nonscientific audience, such as members of Congress.

"Suppression of rhizobial reproduction by legumes:
implications for mutualism"

(with Prof. Michael Sadowsky, largely based on ideas and preliminary results from grad student Ryoko Oono -- see this recent review article we wrote with Toby Kiers)

Rhizobia are bacteria that can live in soil, but also symbiotically, inside root nodules on plants like soybean or alfalfa. Although many rhizobia provide their host plants with nitrogen, saving farmers billions in fertilizer costs, less beneficial strains cause problems in some areas. Some hosts, including alfalfa and pea, make rhizobia swell up as they start to provide nitrogen. Unlike the nonswollen rhizobia from soybean or cowpea nodules, swollen rhizobia apparently lose the ability to reproduce, but does rhizobial swelling somehow benefit the plant?

To find out, the investigators will map this trait on the family tree for crops and wild plants that host rhizobia, to see if causing swelling evolved more than once, suggesting a positive benefit to the plants. Three dual-host rhizobia (plus mutants that differ in their ability to hoard resources) will be used to measure effects of rhizobial swelling on costs and benefits to the plants. Plant defenses against rhizobia that provide little or no nitrogen, already demonstrated in soybean, will be tested in species that impose bacterial swelling.

This research will increase understanding of a symbiosis that supplies nitrogen to agricultural and natural ecosystems, with implications for other important symbioses. Results could guide the development of crops that selectively enrich soils with the best rhizobia, decreasing future fertilizer requirements. Educational opportunities will be provided for undergraduates, at least one graduate student, and a postdoctoral researcher. Two female high school students have already won trips to the International Science Fair for research done in the principal investigator's laboratory, where such mentoring will continue to be a priority.

Evolution of persistence in the model bacterium, Sinorhizobium
(with Prof. Michael Travisano, largely based on ideas, preliminary data, and writing by grad student Will Ratcliff, with some ideas from Andy Gardner and colleagues -- see the second paper discussed in this post -- and possible relevance to our work on evolution of aging.)

Some bacteria can enter a nongrowing "persister" state that allows them to survive antibiotics and other treatments that normally kill them. By suspending growth, they may also free resources for their genetically identical clonemates.

Most species form only a few persisters. This makes persisters hard to study, despite their importance in long-term infections. However, certain harmless bacteria from plant roots can form up to 40% persisters. These will be used to determine whether persisters benefit mainly from enhanced stress resistance or by increasing the growth of their clonemates.

Successful completion of this research will provide two main benefits: First, this research will determine the conditions that favor the spread of persister-forming bacterial strains over nonpersister strains, and the genetic basis of persistence. This can provide direct medical benefits by aiding the development of novel management strategies, drug targets, and eventually treatments for patients infected with persister-forming bacteria. Second, some conclusions may apply to other species that are difficult to eradicate because they, too, form dormant, stress-resistant stages. These include many agricultural weeds and some species of mosquito. One key advantage of the proposed approach is speed: experiments that would take decades with weeds or mosquitoes can be conducted in months with bacteria. This research will provide training opportunities and jobs for undergraduates, high school students, and a post doctoral researcher.

I am planning to accept another grad student for autumn 2010.

July 20, 2009

Join my lab?

I hope to welcome one or possibly two new graduate students in autumn 2010.

As I noted on the Ecology, Evolution and Behavior web page, much of my research can be seen as following up on ideas first discussed by W.D. Hamilton. This includes our work on the evolution of cooperation (Nature 425:78-81) and on longevity-versus-reproduction tradeoffs as a possible explanation for the health benefits of eating low doses of plant toxins (PLoS One 4:e6055). Often, my grad students use crop plants and/or noncharismatic microfauna (bacteria, yeast, etc.), so if aesthetics is more important to you than science, choose a different major professor. I am also interested in agricultural implications of past and ongoing natural selection (Q. Rev. Biol. 2003 and forthcoming book), although I don't currently have any grant funding for this work.

I also accept students in the Plant Biology grad program, which has been unusually generous in financial support for grad students, providing first-year and summer stipends, paying for meeting travel, etc. (Budget cuts could change this.) Also, unlike most Plant Biology programs, their vision extends beyond molecular biology of Arabidopsis, with significant strength in evolution and in legume (especially Medicago) symbiosis. So students interested in plants should consider both programs.

July 17, 2009

Biofilms as selfish herds

"Scientists once thought that wolves chase deer and may even try to eat them, that sharks attack other fish, and that cold weather can kill penguins. But recent research has shown that these so-called threats are actually beneficial, because they encourage togetherness."

OK, I made the above "quotation" up, but the logic is the same as in a recent story in Science about antibiotics:

"there's scant evidence that bacteria or fungi deploy antibiotics to kill or ward off other microbes... These molecules, they assert, may be less weapons for competition or combat than tools of communication... When certain bacteria are exposed to nystatin, the microbes form slimelike communities known as biofilms... this may be just one of the molecule's natural roles."
For a bacterial cell, there are both disadvantages and advantages to crowding together in a biofilm. There may be more competition for available nutrients in a biofilm, but there may be more nutrients to compete for. One reason is that an individual bacterium may not be able to excrete enough enzymes to release nutrients from a solid surface; a bunch of bacteria growing in a biofilm may do better.

But why use antibiotics as signals to form biofilms, when bacteria can produce and detect plenty of nontoxic signals? See previous posts on "quorum sensing", but also this discussion.

The most logical reason to form a biofilm in the presence of an antibiotic is to escape from the antibiotic! I am reminded of this quotation about cattle in lion country:

" Yet although the ox has so little affection for, or individual interest in, his fellows, he cannot endure even a momentary severance from his herd. If he be separated from it by strategem or force, he exhibits every sign of mental agony; he strives with all his might to get back again and when he succeeds, he plunges into its middle, to bathe his whole body with the comfort of closest companionship."

The quotation is from Francis Galton, but I got it from Bill Hamilton's 1971 paper, "Geometry for the selfish herd." Other examples in this classic paper -- "Evilutionary Biologist" John Dennehy has written a nice summary -- include reindeer at the edge of a herd suffering much more attack from parasitic insects and gulls nesting at the edge of a colony suffering much more predation.

I am reading a couple of interesting papers relevant to biofilms and may have time to write about them this weekend. As for the real-world role of antibiotics as antibiotics, see this recent post.

May 30, 2009

Whom do cheating bacteria cheat: host plants or other bacteria?

Bacteria known as pseudomonads produce and release chemicals (defensive toxins) that protect plants from fungi that would otherwise attack their roots. In return, the roots release various organic compounds that serve as food for the bacteria.

The "in return" part has always bothered me. Each root system is associated with millions of bacteria. In a 2003 paper (Cooperation in the rhizosphere and the "free rider" problem. Ecology 84, 838-845), we pointed out that this system is a potential tragedy of the commons. Mutant bacteria that don't make root-protecting chemicals free up resources for their own reproduction, so we might expect them to out-compete more-beneficial strains. If these "cheaters" become common enough, the host plant might be killed by fungi, but that would hurt the beneficial strains around that root system just as much as it hurt the cheaters. We suggested that the bacteria make these toxic chemicals to protect themselves, with protection of roots as a side effect. Research by others, including some of the authors of this week's paper, has provided data consistent with this hypothesis. For example, toxins made by pseudomonads protect them from predators.

More recently (in Annual Review of Ecology, Evolution, and Systematics), Toby Kiers and I suggested that cooperation between microbes and plants is better understood as cooperation among microbes. For example, by providing their host plant with the nitrogen it needs to grow, rhizobia (root-nodule bacteria) help all the other rhizobia infecting the same plant.

This week's paper shows that defensive toxin production by pseudomonads is similar. Toxin production by pseudomonads may benefit the plant and may benefit individual cells, but it also benefits other pseudomonads nearby. "Predators promote defence of rhizosphere bacterial populations by selective feeding on non-toxic cheaters" was published in The ISME Journal by Alexandre Jousset and colleagues in Germany and Switzerland. These pseudomonads produce various toxins, especially when there are many of them in close proximity. This dependence of toxin production on bacterial density is an example of quorum sensing. Mutants "defective" in quorum sensing have been shown to grow (i.e., reproduce by dividing) faster, because they save the cost of toxin production. Can these "cheaters" free-load on defensive toxin producers nearby, essentially hiding behind their chemical defenses?

Continue reading "Whom do cheating bacteria cheat: host plants or other bacteria?" »

May 22, 2009

Oxytocin and the genetics of altruism

Where to publish a paper on the genetics of altruism? In an open-access journal, of course! One day after publishing the fossil primate paper that's creating so much excitement -- it's a great fossil, but too old to tell us anything about our recent ancestors, shared with other apes, or the less-recent ones shared with monkeys -- PLoS One published "The Oxytocin Receptor (OXTR) Contributes to Prosocial Fund Allocations in the Dictator Game and the Social Value Orientations Task", by Salomon Israel and colleagues. Like all papers in open-access journals, the full text is available on-line.

These researchers measured altruism in 200 students, based on how each chose to divide a pool of money with another unknown individual. Their hypothesis, based on various past studies, was that the hormone oxytocin is important for social interactions in general and for human altruism in particular. For example, Zak and colleagues showed that sniffing oxytocin made people offer a more generous split when the recipient had the chance to retaliate for a low offer (the "Ultimatum Game"), although not when there was no chance to retaliate, as in the Dictator Game used in the current study.

The researchers tested for statistically significant relations between and different variants of the oxytocin receptor gene, which codes for the protein that responds to this hormone signal in the brain, and "prosocial responses" (generosity) in the Dictator Game and a more-complex version, the SVO. Interestingly, none of the genetic differences they looked at were in the protein-coding part of the gene (orange). Most were in an intron, which would be transcribed from DNA into messenger RNA but then cut out before the mRNA is translated into protein. So I assume these genetic differences could affect how much oxytocin receptor protein is made where and when, but not the structure of the protein itself.

Continue reading "Oxytocin and the genetics of altruism" »

May 1, 2009

Sibling rivalry in plants

This week I will discuss two papers, both dealing with plants and competition, in the context of genetic relatedness that might be expected to moderate competition:
"Growing with siblings: a common ground for cooperation or for fiercer competition among plants?" by Ruben Milla and colleagues (Proceedings of the Royal Society), and
"Do plant parts compete for resources? An evolutionary viewpoint" by Victor Sadras and me (New Phytologist).

Earlier I discussed a paper by Susan Dudley and Amanda File showing that some plants grow less root when interacting with related than with unrelated neighbors. Spending less resources on roots could have freed resources for more seed production, but they didn't measure that. Now Milla and colleagues have.

Continue reading "Sibling rivalry in plants" »

April 17, 2009

Mindless manipulation

This week I'll discuss a recent paper from our lab. But first, here are links to three other papers that look interesting:

Evidence from the domestication of apple for the maintenance of autumn colours by coevolution Some insect pests avoid trees whose leaves turn red in autumn and do poorly on those trees, but can trees "lie" or is there an unbreakable link between red color and poor quality as a host, perhaps because "aphids grow better on trees that drop their leaves later [because they have enough nitrogen they can risk losing high-N leaves in frost?], which are known to have fewer autumn colours [because, by the time they lose chlorophyll, UV levels are too low to require the protection provided by red anthocyanins?]."?

Functional morphology of the ankle and the likelihood of climbing in early hominins Modern chimps use their ankles, when climbing trees, in ways some early hominins (1-4 million years ago) probably couldn't, based on fossils.

Cooperation and virulence of clinical Pseudomonas aeruginosa populations
Patients with pneumonia are sicker when bacterial cells cooperate by producing individually costly virulence factors, but bacterial populations evolved "cheaters" that don't make these factors within 9 days.

In our paper, "Rhizobitoxine producers gain more poly-3-hydroxybutyrate in symbiosis than do competing rhizobia, but reduce plant growth", published online in The ISME Journal, my PhD student Will Ratcliff describes experiments showing how symbiotic nitrogen-fixing bacteria can manipulate their plant hosts.

Continue reading "Mindless manipulation" »

March 3, 2009

Mixed infections, for better or worse

If being infected is bad, is being infected by two different pathogens at once even worse? Not necessarily, as this week's paper shows. "Quorum sensing and the social evolution of bacterial virulence" was published in Current Biology by Kendra Rumbaugh and colleagues. Their results contradict an earlier prediction, although not the fundamental evolutionary principle behind that prediction.

Continue reading "Mixed infections, for better or worse" »

January 2, 2009

Ford Denison, amateur scientist

My NSF grant will run out soon, so I get to spend the year in which we celebrate the 200th anniversary of Darwin's birth and the 150th anniversary of The Origin of Species as an amateur scientist, like Darwin himself. I'm not as smart or as rich as he was, but I do have imaginative and hard-working students and much better equipment.

I'm working on two grant proposals and several papers while dreaming of getting back to writing my book, so no detailed paper analysis this week. But Nature is highlighting 15 major papers on evolution they have published in the last few years.

December 21, 2008

Spatial structure and the evolution of cooperation between microbes and plants

Evolutionary theory suggests that cooperation should often be unstable, even when it benefits all concerned. Toby Kiers and I discussed this problem and some possible solutions in a recent review article in Annual Review of Ecology and Evolution. Meanwhile, Jim Bever and colleagues have published some important experimental data in Ecology Letters, helping to explain cooperation between plants and fungi, a little too late to include in our review. Their paper is titled: "Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism."

Many bacteria and fungi associated with plant roots benefit more from healthy plants than from dead or dying ones. If each individual plant were colonized by only one strain of bacteria or fungus, then strains that helped their host plants (by providing them with nitrogen or phosphorus, for example) would indirectly help themselves, gaining an evolutionary edge over their competitors of the same species. These beneficial strains would become more common in each generation. In other words, cooperation would evolve.

The problem is that each plant is typically associated with several strains of each species of bacteria or fungus. Strains that invest less in helping the plant have more resources to spend on their own reproduction. If less-generous strains benefit equally from the contributions of more-generous strains on the same plant, then less-generous strains will become more common over generations. In other words, "cheating" will evolve.

Continue reading "Spatial structure and the evolution of cooperation between microbes and plants" »

November 28, 2008

We cooperators need to stick together

Experiments on the evolution of cooperation can be simpler with microbes than with animals. Microbes do sometimes cooperate. For example, some amoebae get together and form a stalk (consisting of hundreds of individual cells) to elevate spores (many more individual cells) above the soil. Bacteria may collectively produce and release enough extracellular enzymes to make food available for all, when none of them could make enough enzyme alone. But why should an amoeba volunteer to be in the stalk (an evolutionary dead end) rather than becoming a spore? And why not save the cost of making expensive extracellular enzymes, by free-loading on enzyme production by others? Out of the goodness of their hearts? They don't have hearts.

Cooperation is easiest to understand among microbes that share the same allele (one of several alternative versions of a gene) for cooperation. Kin-selection theory says that an allele leading to some individually costly activity may spread if it preferentially benefits others with the same allele, relative to those with different alleles. Cooperation among relatives, who are more likely to share a given allele, is therefore easy to understand.

But can microbes recognize kin, i.e., whether another microbe has the same alleles? Sometimes, apparently. In this week's paper, Elizabeth Ostrowski and colleagues report in PLoS Biology that Kin discrimination increases with genetic distance in a social amoeba.

Continue reading "We cooperators need to stick together" »

October 18, 2008

Cooperative fish, cheating ants

Cooperation is widespread in nature, despite theoretical predictions that "cheating" mutants could displace cooperators over just a few generations of evolution. We don't apply human moral standards to other species, of course, but define cheating as contributing less, while benefiting from activities of others. The evolutionary persistence of cooperation is usually attributed to reciprocity (trading resources or services) or to kin selection: cooperation among relatives, such as parental care, can persist even without reciprocity. Fish that clean parasites from other fish are a standard example of reciprocity -- they get to eat the parasites -- whereas nonreproductive worker ants are a standard example of kin selection. I will briefly discuss one recent paper on each of these.

Redouan Bshary and coauthors report in Nature that "Pairs of cooperating cleaner fish provide better service quality than singletons." Cleaner fish often prefer to eat client mucus (yum!) than client parasites, but clients don't like this and tend to leave. When a male and female cleaner work together, the client fish may leave if either of them takes a bite of mucus. Females, in particular, were less likely to do this when cleaning with their male partner rather than alone. The authors also did an experiment to see whether cleaner fish would eat a less-preferred food (fish flakes, perhaps analogous to client parasites) if eating their more-preferred food (prawns, perhaps analogous to client mucus) resulted in the food plate being taken away. They did, especially the females. This may have been because the male often chased her if she ate a prawn, costing them both the rest of their meal. Overall, pairs appear to provide better service to clients, because they are better-behaved together than alone, especially the female.

Shigeto Dobata and coauthors reported on "Cheater genotypes in the parthenogenetic ant Pristomyrmex punctatas" in Proceedings of the Royal Society. Social insects, such as ants and bees, usually have reproductive queens and nonreproductive workers. Worker genes are transmitted to the next generation by the queen, who is typically the workers' mother and therefore shares most of their genes. Pristomyrmex punctatas is different. An individual ant may reproduce (usually when young) and also work. Some individuals are more like queens, however. These are larger, reproduce more, and do little or no work for the colony. If these nonworking ants were close relatives of the workers, this behavior could perhaps be maintained by kin selection. It could be an example of division of labor for mutual benefit, a less-extreme version of the more-familiar worker/queen division. So Dobata and coauthors analyzed the DNA of hundreds of ants to see how they were related. They found that these nonworking ants were much less closely related to workers than queens usually are. Most of the ants (working or not) reproduced parthenogenetically, essentially cloning themselves without sex. Working hard while unrelated individuals profit from your work doesn't usually work out over the long run, but these nonworking ants have been seen in the field for over 25 years. Is this an evolutionary dead end? A similar situation with Cape honey bees, whose colonies are parasitized by unrelated "pseudoqueens" usually leads to colony extinction. I look forward to reading more about this interesting ant species.

September 6, 2008

Conflict builds cooperation

I just heard an interesting talk by Joan Silk on lasting friendships among female baboons, in which grooming and mutual support during conflicts are both important. Here's a link to some of her papers. This week's paper is on a somewhat-related topic, but in birds rather than apes.

"Duration and outcome of intergroup conflict influences intragroup affiliative behaviour" was just published in Proceedings of the Royal Society by Andrew Radford, of the University of Bristol.

Woodhoopoes are African birds (videos here) that live in small groups, typically a breeding pair and some close relatives. Conflicts over territory with neighboring groups (mostly yelling at each other) are common, often more than once a day. Neighbors rarely take over each other's territories, but if they win the shouting match they stay and forage for awhile. Do such conflicts and their outcomes affect group solidarity?

Continue reading "Conflict builds cooperation" »

July 26, 2008

Would the host want anyone to starve?

This week’s paper (Ratcliff, et al., in press) is from my lab.

The relationship between a legume plant and the rhizobium bacteria living in its root nodules is usually beneficial to both. Rhizobia convert nitrogen from the atmosphere into a form their plant host can use to make proteins. Rhizobia benefit from infecting plants because they reproduce more inside nodules than they would in the soil. They can also acquire certain resources in nodules. In particular, they can accumulate large amounts of energy-rich PHB – up to 50% of their own weight!

But there can also be conflicts of interest between rhizobia and their host plants. Resources used to make PHB could have been used, instead, to acquire more nitrogen for the plant. Therefore, mutant rhizobia that don’t make PHB provide their hosts with more nitrogen (Cevallos, et al., 1996). So why do most rhizobia make PHB? Our hypothesis has been that the rhizobia themselves benefit from having more PHB. This contrasts with an earlier hypothesis that rhizobia store PHB so that they can use the energy for the benefit of the plant. Consistent with our hypothesis, mutants defective in PHB metabolism reproduce less (Cai, et al., 2000). However, mutations can have complex interacting effects, making it hard to be sure that differences in PHB were the only cause of differences in reproduction. So Will Ratcliff decided to compare rhizobia that were genetically identical but had different amounts of PHB per cell.

Continue reading "Would the host want anyone to starve?" »

July 17, 2008

More talks from Evolution 2008

I'm done with two grant proposals, revising a book chapter, and checking the final version of a review article. I still have a pile of interesting reading and writing to do before I can get back into the lab - actually, I did help Ryoko set up an experiment yesterday - but no more looming deadlines for awhile. So, here are two more summaries of talks from Evolution 2008.

Do I know you?

The ability to tell other individuals apart by their faces is presumably maintained by natural selection, so you can recognize and avoid bad guys. But is there also selection for looking different enough to be recognizable? Or is it better to blend in with the crowd, so you can get away with stuff?

Michael Sheehan and Elizabeth Tibbetts are studying individual recognition in wasps (Tibbetts and Dale, 2007). Their hypothesis is that distinctive-looking individuals benefit, because they get in fewer fights over dominance.

Continue reading "More talks from Evolution 2008" »

June 29, 2008

Evolution 2008: sexy plants, battling bacteria, durable cooperation

About 1500 scientists attended Evolution 2008 here last week. The four-day meeting was filled with 15-minute talks (usually ten at once, in different rooms), plus two evening poster sessions (like a science fair, for grownups, with discussions rather than judging), scenically located on a pedestrian bridge over the Mississippi. Reports that "scientists are abandoning evolution" appear to be exaggerated.

Here are summaries of some of the talks I enjoyed.

Continue reading "Evolution 2008: sexy plants, battling bacteria, durable cooperation" »

May 31, 2008

Traditional values in bees

The beehive was an early Mormon icon, symbolizing hard work and cooperation. To an evolutionary biologist, however, a beehive could symbolize reproductive skew, a situation where some individuals reproduce much more than others. Extreme reproductive skew is one of the defining characteristics of eusocial species, of which honey bees are a prime example. Reproductive skew can differ between the sexes. In honey bees, the queen lays most of the eggs, and most females don't reproduce at all. Polygamous species and groups show the opposite pattern: males vary much more in reproductive success than females do. Maybe an inverted beehive would have been a better symbol. Note that the cells in our bodies behave somewhat like a eusocial bee colony; any children we have are directly descended from a few sex cells, while brain cells and skin cells play the supporting role of worker bees.

This week's paper, "Ancestral monogamy shows kin selection is key to the evolution of eusociality" was published in Science by William Hughes and others. Like humans, some bees are monogamous, meaning that the queen mates with only one male, so her daughters (the workers) are all sisters. In other bee species, the queen mates with several males, so her daughters are half-sisters. Relatedness generally favors cooperation, although there are some possible complications, discussed below.

This week's paper asks how mating behavior affects the evolution of eusociality. They reasoned that, if mating system doesn't matter, then today's eusocial species could be descended from either monogamous, polygamous, polyandrous (each female has multiple mates), or promiscuous ancestors. Alternatively, eusociality may evolve more easily with one of these mating systems than with the others.

Continue reading "Traditional values in bees" »

May 25, 2008

Pest control for ants


(Top) A small leafcutter worker atop a leaf guards her sister against attacks by parasitic flies. Ants carrying leaves cannot use their mandibles for defense, so they carry hitchhikers to ward off the parasites. (Bottom) The fungus garden in a nest of Atta leaf-cutter ants. Notice the diversity of ant sizes within a colony, from the large red soldier ants to the minute orange ants tending to the garden. Atta ants have some of the most sophisticated caste systems among the social insects. -- photos and captions from Alex Wild (

This week’s paper, “Black yeast symbionts compromise the efficiency of antibiotic defenses in fungus-growing ants" by Ainslie Little and Cameron Currie, was just published in Ecology. Elsa Youngsteadt interviewed me, among others, for a story in Science about this research.

I’ve never done research on the fungal “farms" of ants and termites, but I’ve been interested in them every since a camera company bought a close-up photo (not Photoshopped like this one) of an ant carrying a leaf along a barbed wire “bridge" on its way back to its nest, from my mycologist father, William Denison. Dad was best known for pioneering research in the tops of tall trees, but never had to fight a shaman, as far as I know.

Continue reading "Pest control for ants" »

April 9, 2008

Welcome, fellow Dr. Tatiana fans!

Olivia Judson's latest column includes a good summary of work in my lab on cooperation between soybean plants and the rhizobium bacteria that (typically) provide them with nitrogen. As she points out, "cheating" is less likely to evolve in symbiont populations if they are transmitted in eggs or seeds, relative to symbionts that are acquired from the environment. In the former, if the host dies before reproducing, the symbiont dies, too. Symbionts without brains (bacteria, say) can't anticipate the effects of their actions; it's just that those whose genetically programmed behavior increases host survival become more common over generations.

Similarly, low symbiont diversity within an individual host may favor symbiont investment in costly activities that benefit the host. If each host has many different symbionts, on the other hand, then helping the host indirectly benefits competing symbionts sharing that host.

Rhizobium bacteria reach new host plants through soil, not via seeds, and they can do so even if the host dies without reproducing. Furthermore, each individual plant has multiple strains of rhizobia, which should undermine cooperation. Why then, do most rhizobia use their limited energy supply to fix nitrogen, giving most of it to the host plant? Why not use that energy for their own reproduction, instead?
Although there are several rhizobium strains per plant, they are typically segregated into individual root nodules. So, Toby Kiers and I reasoned, if plants monitor individual nodules and do something nasty to those that provide less nitrogen, that would act as a form of natural selection against cheating rhizobia. A computer model by Stuart West came to similar conclusions. To test this hypothesis, we forced some nodules to cheat, by surrounding them with an argon-oxygen atmosphere lacking nitrogen gas. Control nodules on the same plant got normal air, which is 80% nitrogen. Would rhizobia freed from the burden of fixing nitrogen redirect resources into their own reproduction? Would the plant impose sanctions on nonfixing nodules? If the answers to these questions are yes and yes, what would be the overall effect of cheating on rhizobium reproductive success?

Continue reading "Welcome, fellow Dr. Tatiana fans!" »

March 1, 2008

Knowing when not to cheat

This week's paper is Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae published in Nature by Lorenzo Santorelli and colleagues at Rice University and Baylor College of Medicine, both in Texas.

The evolution of cooperation is a central problem in the history of life. Darwin explained how sophisticated adaptations -- "the structure of the beetle which dives through the water... the plumed seed which is wafted by the gentlest breeze" -- can evolve in a series of small improvements over generations. But some of the major transitions in evolution are harder to explain, because It seems that they should have been opposed, rather than supported, by natural selection. The origin of multicellular life is a good example. It's not that hard to imagine independent cells working together in loose groups for mutual benefit - huddling together for defense, say - but why would a cell give up the ability to reproduce, as most of the cells in our bodies have done?

Continue reading "Knowing when not to cheat" »

January 22, 2008

Altruistic punishment? Maybe not.

Punishing cheaters selects against cheating, but what selects for punishing? Are the answers different, depending on whether the species involved have brains? A recent internet experiment suggests that altruistic punishment, perhaps unique to humans, doesn't promote cooperation as effectively as previously thought.

My own research focuses on cooperation in species without brains. We showed that "sanctions" imposed by legume plants limit the evolution of "cheating" rhizobium bacteria (those that divert more plant resources to their own reproduction, relative to other rhizobia, by investing less in fixing the nitrogen needed by the plant). We think individual plants help themselves by imposing sanctions that limit wasteful resource use by less-beneficial rhizobia - they don't do it for the benefit other legumes.

In theory "altruistic punishment" (paying some cost or taking some risk to punish noncooperators) could help explain why there is more cooperation among unrelated humans than might otherwise be expected. (Cooperation among relatives is explained by kin selection.) But how much are individuals willing to pay to punish noncooperators?
The latest experiments attempting to answer this question were just published on-line in Proceedings of the Royal Society, by Martijn Egas and Arno Riedl: The economics of altruistic punishment and the maintenance of cooperation.

Continue reading "Altruistic punishment? Maybe not." »

January 10, 2008

Ants en't ents

Science advances by disproving previously-tenable hypotheses. For example, "The earth is <10,000 years old" was disproved by annual sediment layers long before we were able to estimate the actual age. Actually, Tom Kinraide and I argued in "Strong inference -- the way of science" that a hypothesis needs to be explanatory as well as falsifiable. So for a young earth to ever have qualified as a hypothesis, it would first have needed to explain at least some real world observations. Right off hand, I can't think of any actual data that an unbiased person would look at and say, "Well, these data would make sense, but only if we assume the earth is <10,000 years old."

Similarly, if someone wanted to convert "intelligent design" from religious whining into a scientific discipline, we'd need some falsifiable hypotheses. Suppose, for example, we hypothesized that current features of plants and animals (not just their single-celled, distant ancestors) were supernaturally-imposed designs to maximize their success. That hypothesis is consistent with the many examples of sophisticated adaptations (err, "design"), but what can we conclude from the many examples of maladaptation ("bad design")? Maladaptation is predicted by evolutionary theory (when current conditions don't match those under which past selection occurred, for example) but if some design team is continuously intervening in evolution, do maladaptations imply that they had a busy week? If so, should we expect the problem to instantly disappear, once they get around to it?

This week's paper is another example of the pattern we see repeatedly in biology: many sophisticated adaptations, but also serious "design flaws." In particular, Acacia trees can be fooled into feeding and housing ants that are harming them.

Breakdown of an Ant-Plant Mutualism Follows the Loss of Large Herbivores from an African Savanna was published this week in Science by Todd Palmer and five coauthors, three of whom I know from my years at UC Davis.

Continue reading "Ants en't ents" »

October 27, 2007

R! How can relatedness be negative?

Hamilton's equation for predicting the evolution of altruism is widely misunderstood. A simple diagram from a classic paper can help.
Source: Jesus and Mo

You sank in the opinion of your fellow-men... by leaving your money in a capricious manner without strict regard to degrees of kin...
There wasn't much good i' being so rich... if she'd got none but husband's kin to leave it to.

- The Mill on the Floss

This week I will discuss two classic papers on how relatedness affects the evolution of social behavior. Altruism towards relatives is widely recognized, but W.D. Hamilton was apparently the first to make quantitative predictions of how relatedness would affect the evolution of altruism. In 1964, he published two papers on "The genetical evolution of social behavior"? (J. Theor. Biol. 7:1-52). Hamilton's rule c < r b is now widely known, but also widely misunderstood. The rule states that a gene causing some altruistic behavior (donating blood, say) may spread if the cost of the activity is low enough, and if it preferentially benefits others who carry the same gene, typically because they are genetically related. The cost to the donor and benefit to the recipient are c and b, both measured in fitness units (average increase or decrease in reproduction, due to the altruistic activity). But what is r?

Wikipedia says r is the "coefficient of relatedness."? This is consistent with J.B.S. Haldane's famous joke: "I would lay down my life for two brothers [1/2] or eight cousins [1/8]."? But this definition is not necessarily right. By the correct definition, r can even be negative!

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September 27, 2007

Cooperation and cheating in microbes: quorum sensing and persisters

Two papers on cooperation this week. If you were trying to help someone, but end up causing problems for them, were you being cooperative? I have no idea, so I like to study cooperation in microbes. Microbes don't have brains, so "intent" isn't a factor. And the only definition of "benefit" that makes sense is an increase in Darwinian fitness or reproductive success, which is often easy to measure in microbes; just count them.
I like these definitions:

Cooperation: a behaviour which provides a benefit to another individual (recipient), and which is selected for because of its beneficial effect on the recipient. [Exhaling CO2 isn't cooperation; it evolved as a side-effect of breathing oxygen, not to benefit plants.]
Cheaters: individuals who do not cooperate (or cooperate less than their fair share), but are potentially able to gain the benefit of others cooperating. ["Equal share" might be less ambiguous.]

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August 22, 2007

Evolution of cooperation reviewed

The theme of the latest issue of Current Biology is "Biology of Societies." There are reviews on the social life of spiders, crows, hyenas, amoebae, and insects, plus the role of cognition in social interactions among humans. If you are interested in the evolution of cooperation, it might be worth a trip to your nearest university library (if you don't have access via the web) to browse this issue.

I particularly liked "Evolutionary Explanations for Cooperation" by Stuart West, Ashleigh Griffin, and Andy Gardner. Their review reprints figures from several recent papers, so you can see some of the data upon which their generalizations are based. I won't try to summarize the whole thing, just some points that may have been neglected in other reviews of this topic.

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August 14, 2007

Cooperation gets complex

This week, instead of discussing a paper, I will summarize some presentations from the Ecological Society of America meetings last week in San Jose, California (a much more interesting place than I expected, including hands-on transformation of bacteria at the Tech Museum).

I ran into two people who admitted to reading this webblog: Madhu Katti and Don Strong, but didn't get to talk to either of them for long. There were usually several interesting sessions going on at once, from 8 AM to late evening, plus lots of informal discussions, but I will limit my summary to a few of the presentations on the evolution of cooperation, my own area of research.

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August 3, 2007

Left behind: social amoebae

This week's paper, published in Science (317:679) is "Immune-like phagocyte activity in the social amoeba" by Guokai Chen, Olga Zhuchenko, and Adam Kuspa of the Baylor College of Medicine.

Cells of the social amoeba, Dictyostyleium discoideum forage individually, but eventually group together into a "slug", which crawls through the soil for days before eventually forming a spore-tipped stalk. Previous work with this species has looked at conflicts of interest over which cells have to sacrifice future reproduction (as spores) and become part of the stalk. This week's paper uncovers another example of apparent altruism in Dictyostelium, which may shed light on the evolution of a key part of our immune system.

As a Dictyostelium slug crawls through the soil, some cells are left behind. Are these just random sluggards? Or do they function like human phagocytes, the immune system cells that gobble up bacteria?

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July 28, 2007

Begging: the question

My wife and I have a bird feeder outside our kitchen window. Yesterday I saw an adult male cardinal feeding some of the seed to an immature cardinal not much smaller than he was. I guess it's hard to say "no", but should he have?

This week's paper, "The adaptive value of parental responsiveness to nestling begging" by Uri Gordzinski and Arnon Lotem, published online in Proceedings of the Royal Society, may have answered this question.

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July 23, 2007

Diversity, stability, productivity, and policing

This week I will discuss two papers, both of which consider possible benefits of biological diversity. In interpreting the data in the experimental paper, on bees, we need to remember that a given set of data can often be consistent with two or more different hypotheses. This point is reinforced in the review article, which discusses the relationship between diversity and stability of ecosystems.

The experimental paper is "Genetic diversity in honey bee colonies enhances productivity and fitness" by Heather Mattila and Thomas Seeley, of Cornell University (Science 317:362). The review article is "Stability and diversity of ecosystems" by Anthony Ives and Stephen Carpenter, of the University of Wisconsin (Science 317:58).

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July 18, 2007

Low-cost cooperation

In the classic cartoon posted on my office door, little Calvin refuses to take a phone message for his father, saying "people always assume you're some kind of altruist." Two papers in the latest PLoS Biology show that some altruistic behaviors can be found in chimps and rats, as well as humans. Should we be surprised?

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June 27, 2007

Individual and kin selection in legume-rhizobium mutualism

OK, I've been critiquing other people's work for a while. Your mission, should you choose to accept it, is to critique something I've written. It's the summary for a grant proposal I'm about to submit. It will be reviewed by ecologists and/or evolutionary biologists, but they're not likely to be specialists in legume-rhizobium symbiosis. So if something isn't clear to an intelligent but nonspecialist audience, you'll let me know, right? If you're not all too busy reading the many interesting evolution articles in today's New York Times, that is. By the way, the great Myxococcus xanthus photo in Carl Zimmer's article is from Supriya Kadam, who did her PhD with Greg Velicer and just finished a year as a postdoc in my lab.

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June 18, 2007

Can plants recognize kin?

This week's paper is "Kin recognition in an annual plant", by Susan Dudley and Amanda File of McMaster University, just published online in Biology Letters.

Researchers in several countries have recently shown that roots respond differently to another root from the same plant than they do to a root from a different plant. Typically, they grow more aggressively towards a neighbor's root than towards one of their own. But what if the neighbor is a close relative?

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June 3, 2007

Scientific controversy: dinosaur-tail soup ?

This week I want to talk about scientific controversies. In politics or religion, any difference of opinion may qualify as a controversy, which some may try to "settle" by killing those with opposing views. Most scientists would agree that unsupported opinion isn't enough to make a scientific controversy. A scientific question is controversial only if people are actually publishing data that seem to lead to different conclusions.

Two papers in press in Proceedings of the Royal Society illustrate current scientific controversies. The first is "A new Chinese specimen indicates that 'protofeathers' in the Early Cretaceous theropod dinosaur Sinosauropteryx are degraded collagen fibers" by Theagarten Lingham-Soliar ( and colleagues at the Universities of KwaZulu-Natal and North Carolina and the Chinese Academy of Sciences.

The title pretty much says it all. (Collagen is what gives shark-fin soup its distinctive texture, hence the title of this entry.) If the conclusions in this paper become generally accepted, how would that change our overall understanding of evolution?

The two elements of evolutionary theory that upset creationists most wouldn't be affected at all, of course. Our confidence that the universe is a million times older than Bible-based estimates, and that humans and chimps share a recent common ancestor, is based on multiple lines of evidence for each, none of it dependent on which dinosaurs had feathers, if any.

But what about the claim that birds are descended from dinosaurs? Let's see what a leading textbook, "Evolutionary Analysis", says. Page 44: Sinosauropteryx had what "some paleontologists believe are primitive feathers." Page 45: they cite several papers, one questioning this conclusion. "More convincing are [true feathers on] the dromesaur fossils." Page 553: "Luis Chiappe (1995) used skeletal characters to infer the phylogeny [family tree] of early bird lineages." The tree shown has protofeathers near the base, followed by true feathers. If the P. Roy. Soc. paper is correct, that would only require revising the earliest branches of his tree.

So this is a real controversy, but it's only a controversy about where feathers appeared in the family tree of dinosaurs and birds. As the paper says, "the wider question of whether or not birds originate from dinosaurs does not concern the present study." The main fossil evidence that they did comes from analysis of skeletons, not feathers. We don't have DNA from dinosaurs, but genetic comparisons among living species suggest that birds are more closely related to crocodiles than to mammals (Science 283:998). So birds-from-dinosaurs still seems likely.

The second paper is "Context dependence in the coevolution of plant and rhizobial mutualists" by Katy Heath ( and Peter TIffin, whose lab is next to mine. Among other things, this paper shows that plants infected by two different strains of rhizobium bacteria often grew less than those infected only with the worst of the two strains. This result may become controversial soon, when Toby Kiers and I publish data apparently showing that plants infected by two different strains can grow more than those infected with only the best strain. Our experiments were done with soybean, whereas theirs used a wild relative of alfalfa, which houses rhizobia in a different type of root nodule (see photos). Also, our two strains were much more different than theirs. So maybe this doesn't really qualify as a controversy, at least not yet.



Nodule photos taken in our lab (c) Inga Spence... licensing from

When there is a controversy, should it be taught? We certainly shouldn't teach a conclusion as certain when it is still (genuinely) controversial. And students should learn about some past scientific controversies, to understand how they were resolved. The triumph of evolution would be a good example. Exposure to some current controversies would be good, too, assuming teachers have time to keep up with the literature, well enough to know what has been settled (at least until convincing new data to the contrary are published) and what is still controversial. I remember Professor Spanswick, at Cornell. telling us "I found the evidence for the chemiosmotic hypothesis convincing, but always presented it as a controversy... until Mitchell won the Nobel Prize for it."

May 20, 2007

Rapid evolution of beneficial infections

Given my location halfway between the Twin Cities of Minneapolis and St. Paul, and my childish love of clever acronyms, I sometimes wish I'd named this blog This Week In Natural Selection. But then I suppose I'd have to review a pair of closely related papers each week. I'm going to do that this week, anyway.

This week's twins were both published in PLoS Biology, so both are freely available on-line. Both have new data on bacteria that infect insects. Both help us understand the conditions under which infecting bacteria evolve to be beneficial, rather than harmful. Finally, both disprove, again, the popular idea that any evolutionary change big enough to matter (except antibiotic resistance, which a creationist commenter once claimed always involves "horizontal transfer" of genes among bacteria, even though resistance often evolves in bacteria in a closed container all descended from a single cell) always involves lots of genes and takes millions of years. Evolution is our present and future, not just our past.

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May 18, 2007

Helpful cheaters?

Paul Rainey has a very interesting essay in the April 5 issue of Nature. Much of what we know about "cheating" in bacteria that form floating mats comes from his research, including collaboration with Michael Travisano, recently hired here at University of Minnesota. See my earlier post, "how disturbed are cheaters", for background on this system. Although cheaters that don't invest in the goop that holds floating mats together can result in mats breaking up and sinking, Rainey's new essay suggests that a similar form of cheating may have contributed to the evolution of multicellular life.

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May 14, 2007

Evolution of babysitting in bluebirds

Major transitions in evolution have often involved loss of independence, as discussed last week. Most female bees work to increase their mother's reproduction, rather than laying eggs themselves. Less extreme examples of helping others reproduce are known in some animals. "Kin selection" favors helping relatives, if the cost of helping is less than the benefit to the one helped, times their relatedness to the helper. This is known as Hamilton's Rule. As Haldane put it, "I would jump into a river to save two brothers or eight cousins." "Cost" and "benefit" are measured in number of offspring and "relatedness" is relative to one's usual competitors. If surrounded by cousins, Hamilton's Rule would lead to helping only siblings.

For helping behavior to have evolved, there must have been genetic variation in helpfulness. This week's paper shows that this is still true for western bluebirds in Oregon.

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May 6, 2007

How disturbed are most cheaters, really?

Yesterday, my wife asked, "why are there so many theoretical papers in evolutionary biology?" I suggested one reason may be that evolutionary theory is better developed, in the sense of making accurate predictions, than theory in much of biology. This week's paper, comparing results from an evolution experiment to predictions of a mathematical model, is a good example.

The paper is about the evolution of cooperation. This is a hot topic and also my own area of research. Humans enforce cooperation, to varying extents. For example, we often punish cheaters, those who try to benefit from cooperative activities of others without contributing anything themselves. Human cheaters are mostly pretty stupid -- don't even think about plagiarizing this blog for a term paper! -- but what about cheaters with no brains at all?

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