June 14, 2013

Nursing Neanderthals, multisexual mutant mice, and the undead

Barium distributions in teeth reveal early-life dietary transitions in primates
"in a Middle Palaeolithic juvenile Neanderthal... exclusive breastfeeding for seven months, followed by seven months of supplementation.... [then] Ba levels in enamel returned to baseline prenatal levels, indicating an abrupt cessation of breastfeeding at 1.2 years of age"

Serotonin signaling in the brain of adult female mice is required for sexual preference
"male mutant mice lacking serotonin have lost sexual preference.... female mouse mutants lacking either central serotonergic neurons or serotonin... displayed increased female-female mounting"

Regeneration of Little Ice Age bryophytes emerging from a polar glacier with implications of totipotency in extreme environments "following 400 y of ice entombment... [bryophyte cells can ] dedifferentiate into a meristematic state (analogous to stem cells) and develop a new plant."

Quorum-sensing autoinducers resuscitate dormant Vibrio cholerae in environmental water samples
[I wonder if this would work with other "unculturable" microbes.]

April 12, 2013

This week's picks

Here are some papers that look interesting this week. See also my Darwinian Agriculture blog

Stable isotope evidence of meat eating and hunting specialization in adult male chimpanzees "sex differences in food acquisition and consumption may have persisted throughout hominin evolution, rather than being a recent development"

New World cattle show ancestry from multiple independent domestication events "pre-Columbian introgression of genes from African cattle into southern Europe"

Key role for a glutathione transferase in multiple-herbicide resistance in grass weeds "When the black-grass A. myosuroides (Am) AmGSTF1 was expressed in Arabidopsis thaliana, the transgenic plants acquired resistance to multiple herbicides"

Potential shortfall of pyramided transgenic cotton for insect resistance management "results from 21 selection experiments with eight species of lepidopteran pests indicates that some cross-resistance typically occurs between Cry1A and Cry2A toxins."

The Upper Limb of Australopithecus sediba "use of the forelimb primarily for prehension and manipulation appears to arise later, likely with the emergence of Homo erectus" [There are several articles on A. sediba in this issue.]

Achieving the triple bottom line in the face of inherent trade-offs among social equity, economic return, and conservation "three very different case studies in California (United States), Raja Ampat (Indonesia), and the wider Coral Triangle region (Southeast Asia). We show that equity tends to trade off nonlinearly with the potential to achieve conservation objectives, such that similar conservation outcomes can be possible with greater equity, to a point."

Decreased water flowing from a forest amended with calcium silicate "An unexpected outcome of the Ca amendment was a change in watershed hydrology; annual evapotranspiration increased by 25%, 18%, and 19%, respectively, for the 3 y following treatment before returning to pretreatment levels. "

Responses of Mn2+ speciation in Deinococcus radiodurans and Escherichia coli to γ-radiation by advanced paramagnetic resonance "extreme radiation resistance of D. radiodurans cells cannot be attributed to SodA"

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 1, 2013

Copying in birds, dolphins, and viruses; evolution & environmental change; evolution of mutation rate

Learning and signal copying facilitate communication among bird species "where only two species regularly interact, one species' [alarm] calls incorporate the call of the other."

Vocal copying of individually distinctive signature whistles in bottlenose dolphins "Copying occurred almost exclusively between close associates such as mother-calf pairs and male alliances during separation... copies were clearly recognizable as such because copiers consistently modified some acoustic parameters of a signal when copying it... no evidence for the use of copying in aggression or deception."

A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity "the only documented bacterial adaptive immune system is the CRISPR/Cas... a phage-encoded CRISPR/Cas system is used to counteract a phage inhibitory chromosomal island of the bacterial host. "

Evolutionary rescue from extinction is contingent on a lower rate of environmental change" "By assessing fitness of these engineered [E. coli] strains across a range of drug concentrations, we show that certain genotypes are evolutionarily inaccessible under rapid environmental change."

Fossil evidence for a hyperdiverse sclerophyll flora under a non-Mediterranean-type climate "sclerophyll hyperdiversity has developed in distinctly non-Mediterranean climates... likely a response to long-term climate stability."

A trade-off between oxidative stress resistance and DNA repair plays a role in the evolution of elevated mutation rates in bacteria "The dominant paradigm for the evolution of mutator alleles in bacterial populations is that they spread by indirect selection for linked beneficial mutations when bacteria are poorly adapted... [but] hydrogen peroxide, generates direct selection for an elevated mutation rate in the pathogenic bacterium Pseudomonas aeruginosa as a consequence of a trade-off between the fidelity of DNA repair and hydrogen peroxide resistance."

December 27, 2012

Antibiotic resistance, camouflage, exinction...

Small changes in enzyme function can lead to surprisingly large fitness effects during adaptive evolution of antibiotic resistance "Using experimental evolution and deep sequencing to monitor the allelic frequencies of the seven most biochemically efficient TetX2 mutants in 10 independently evolving populations, we showed that the model correctly predicted the success of the two most beneficial variants"

Early evolution and ecology of camouflage in insects Lacewings were carrying "trash" (parts of ferns) as camouflage 110 million years ago.

The Evolutionary Landscape of Alternative Splicing in Vertebrate Species "Within 6 million years, the splicing profiles of physiologically equivalent organs diverged such that they are more strongly related to the identity of a species than they are to organ type."

Mass extinction of lizards and snakes at the Cretaceous-Paleogene boundary "The recovery was prolonged; diversity did not approach Cretaceous levels until 10 My after the extinction"

Equatorial decline of reef corals during the last Pleistocene interglacial "poleward range expansions of reef corals occurring with intensified global warming today may soon be followed by equatorial range retractions. "

August 28, 2012

The importance of titles

Years ago, someone reinvented a method I'd published in a journal he regularly read (and published in), without citing my paper. I complained. He pointed out that the title of my article didn't hint at that aspect of the contents.

Since then, I've tried to get the main point of each paper into the title. For example:

When Stress Predicts a Shrinking Gene Pool, Trading Early Reproduction for Longevity Can Increase Fitness, Even with Lower Fecundity

But journal editors don't always cooperate. For example, we wanted to call our recent Perspective in Science (discussed here) "Are Antibiotics Weapons, Signals, Cues, or Manipulation?" The editor insisted on "Alternative Actions for Antibiotics."

We worried that people would glance at the title and think, "Oh, another one of those antibiotics-as-signals articles." A "signal" is information whose transmission benefits sender and receiver. A "cue" is information used in ways that don't necessarily benefit the source. For example, bacteria may respond to low doses of antibiotics by turning on protective mechanisms, by fleeing, or by hiding in a biofilm. I would only call antibiotic production a "signal" if scaring away competitors, rather than killing them, is the main way it increases the producer's fitness.

Just as we feared, a recent paper miscites our work:

"Antibiotics, especially at subinhibitory concentrations, can act as signal molecules aside from their antibacterial effect (Davies et al. 2006; Yim et al. 2007; Ratcliff and Denison 2011)."

Choose your title carefully.

July 30, 2012

Correcting Science and PNAS, evolution of more-deadly suicide bombers, blind composers, transcending tradeoffs, light-responsive rhizobia

Absence of Detectable Arsenate in DNA from Arsenate-Grown GFAJ-1 Cells
GFAJ-1 Is an Arsenate-Resistant, Phosphate-Dependent Organism
Surprise! They don't use arsenic instead of phosphorus after all.

Unobserved time effects confound the identification of climate change impacts "PNAS reported statistical evidence of a weather-driven causal effect of crop yields on human migration from Mexico to the United States. We show that this conclusion is based on a different statistical model than the one stated in the paper."

Evolution of music by public choice in natural selection, variation is random but selection isn't.

Explosive Backpacks in Old Termite Workers ...they weren't going to reproduce anyway, but I wonder how long these "suicide vests" took to evolve.

Compensatory mechanisms for ameliorating the fundamental trade-off between predator avoidance and foraging "enhanced nutritional physiology allows caterpillars to compensate when threatened. However, we report physiological costs of predation risk, including altered body composition (decreased glycogen) and reductions in assimilation efficiency later in development." Similarly, reducing investments in research may not affect economic development much between now and the next election.

Light regulates attachment, exopolysaccharide production, and nodulation in Rhizobium leguminosarum through a LOV-histidine
"illumination of bacterial cultures before inoculation of pea roots increases the number of nodules per plant and the number of intranodular bacteroids."

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.

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.

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"

February 16, 2011

Sleep as a survival strategy

This week's paper, Bacterial persistence and bet hedging in Sinorhizobium meliloti, was just published in Communicative and Integrative Biology. It's a brief but important follow-up to a paper in Current Biology, which I've already discussed.

Bacterial persisters are a serious medical problem. An infection that appears to have been cured by antibiotics sometimes "springs back to life." Evolutionary biologists have focused on cases where the renewed infection is caused by an antibiotic-resistant mutant, a classic example of evolution by human-imposed selection. Sometimes, however, the resurgent bacteria are still susceptible to the original antibiotic, yet bounce back after one or more treatments. What gives?

Many antibiotics only kill bacteria that are actively growing. So, if a few cells go dormant, these persisters may survive until the antibiotic breaks down, even if they aren't otherwise resistant.

Will Ratcliff recently reported that Sinorhizobium meliloti bacteria, best known as the nitrogen-fixing, root-nodule symbiont of alfalfa, can also make dormant cells. When S. meliloti cells divide, under starvation conditions, the elder daughter inherits most of the accumulated wealth (energy-rich polyhydroxybutyrate or PHB) and the younger daughter goes off to seek her fortune. You can see this unequal allocation of PHB in the Nile-red-stained image of a dividing cell, below right.PHB.jpg
This apparent bet-hedging strategy is much more organized and more common than the random, one-in-a-thousand process that seems typical of human pathogens. A rhizobial population that starts with the usual normal distribution of PHB (above left) divides, initially, into one with roughly equal numbers of persisters and growers (above center).

Our original paper showed that about 70% of the high-PHB S. meliloti persisters are still alive after 528 days without food. So the well-known ability of rhizobia to survive in soil for months or years between legume hosts may not depend on their ability to out-compete other soil bacteria for limited food supplies.

But how relevant is this work with rhizobia, which benefit their legume hosts by providing them with nitrogen, to the antibiotic-resistant bacterial persisters that cause disease? In this new paper, Will Ratcliff showed that...

Continue reading "Sleep as a survival strategy" »

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.
Thumbnail image for Bacteroids.jpg

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 28, 2010

How "mostly harmless" bacteria manipulate the immune system

"It may be better to keep alive the goose that lays the golden eggs than to kill it. But this argument depends on the assumption that, if you do not kill the golden goose, no one else will either: that is, it assumes that the host is infected by a single clone of symbionts." -- Maynard Smith 1989 Nature 341:284-285.

This week, I'll discuss a paper recently published in Science: Has the Microbiota Played a Critical Role in the Evolution of the Adaptive Immune System?, by Yun Kyung Lee and Sarkis K. Mazmanian. They argue that gut bacteria produce "signals that are recognized by host receptors to mediate beneficial outcomes for both microbes and humans."

Well, how nice! What sort of outcomes would be beneficial for a gut microbe? Reproducing a lot in the gut and spreading to lots of new hosts would be good. How to do this? Diarrhea seems promising. That might sicken or even kill the human, but does that matter to the microbes? Paul Ewald has pointed out that pathogens whose spread depends on host mobility may evolve lower virulence, so people with the flu feel well enough to go to work and spread it. Pathogens that spread via sewage to drinking water, though, may spread more readily if they cause more severe diarrhea. But we also need to consider conflicts of interest among gut bacteria, not just conflicts of interest with the host. For example, species X might trigger diarrhea before species Y has had time to reproduce much. If so, then species Y might benefit from suppressing, or at least delaying diarrhea.

More generally, the diversity of bacteria in the gut creates a "tragedy of the commons", where bacterial strains that pursue their own interests would rapidly out-compete hypothetical strains that sacrificed their own interests for the "greater good", either of the host or of the entire gut bacterial community.

Or so I would predict. But what about those mutually beneficial "signals?"

Continue reading "How "mostly harmless" bacteria manipulate the immune system" »

November 3, 2010

Is it really bet-hedging?

Before the ink is even dry on our Current Biology paper on bet-hedging in rhizobia (actually, before it's even printed), Xue-Xian Zhang and Paul B Rainey have critiqued it in Genome Biology. They summarize Will Ratcliff's results, then ask "whether it is an evolutionary response to fluctuating selection shaped by natural selection." Experimental evolution, an approach Rainey and colleagues have used successfully, would be a good way to answer this question.

But is it really even bet-hedging? To qualify as bet-hedging, you need to sacrifice arithmetic-average fitness to gain greater geometric-average fitness. That would obviously depend on the environment, but it seems reasonable to assume that having half your progeny go dormant would sacrifice fitness when food is abundant, while increasing the chances of having at least one surviving progeny under starvation.

Zhang and Rainey seem to think there's an additional requirement to qualify as bet-hedging, namely, "switching rates to suit prevailing conditions." I disagree. Isn't a 50:50 mix of stocks and bonds (rather than 100% stocks, which have higher average return but are riskier) considered bet-hedging, even if you never change that ratio? But I do agree that it's important to know whether the ratio of dormant to growing cells changes in response to conditions, which I would call phenotypic plasticity. We are working on that.

October 15, 2010

Bet-hedging in symbiotic rhizobia from alfalfa nodules

This week's paper is another recent one from my lab "Individual-level bet hedging in the bacterium Sinorhizobium meliloti", now on-line at Current Biology. Will Ratcliff did a guest post earlier, discussing a paper on the experimental evolution of bet hedging. This latest paper reports Will's own experiments.

S. meliloti is best known for its symbiosis with alfalfa. After infecting via root hairs, it reproduces inside developing root nodules.AlfalfaNodules2.jpg
Alfalfa nodules in our lab; copyright Inga Spence, used by permission.

When the nodules senesce, reproductive rhizobia escape into the soil, leaving the nonreproductive "workers" (bacteroids), which had been providing the plant with nitrogen, behind. A nodule may release millions of rhizobia -- we're not sure how many, actually -- each of which may have accumulated resources there, including high-energy PHB. So a single rhizobial cell that infects a root hair may end up with millions of well-endowed descendants, a few months later. But then what?

Continue reading "Bet-hedging in symbiotic rhizobia from alfalfa nodules" »

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.

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.

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?" »

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" »

December 1, 2009

Better ant fungus farming through chemistry

Leaf-cutter ants feed the leaves to fungi and eat the fungi. Another fungus can parasitize their crop. A few years ago, it was reported that bacteria living on the ants' bodies make antifungal compounds that kill the parasite.

I wondered about this: wouldn't a bacterium that invests resources in antifungal production grow more slowly than a mutant that avoids this costly investment? In the long run, this might hurt ants and bacteria alike, but natural selection has no foresight. So why haven't bacterial "cheaters" that don't make antifungals displaced "altruists" that do? When yeasts (single-cell fungi) were found on the same ants, I suggested that antifungal production might benefit individual bacteria in their war with the yeasts, with activity against the parasitic fungus as a side effect. (Similarly, bacteria that make antibiotics that protect plant roots from fungi have their own selfish reasons.)

Consistent with this hypothesis, it turns out that the antifungal chemicals made by the bacteria aren't active only against the parasitic fungi, and may even harm the fungal crop. But the bacteria presumably benefit the ants more than they harm them, because the ants have specialized structures and secretions whose main function seems to be to support the bacteria. At least, this is true of some fungus-growing ant species. Other species have apparently abandoned use of these bacteria. Instead, they control harmful fungi with antibiotics they make themselves, in special glands. This is an example of a species abandoning one symbiosis (ant/bacteria) when it's no longer beneficial, while retaining a beneficial symbiosis (ant/fungus).
Black lines shows fungus-growing ant lineages that rely on antibiotics they make themselves, rather than those made by symbiotic bacteria, to control parasitic fungi that attack their fungal crop.
Source: Hermógenes Fernández-Marín, Jess K. Zimmerman, David R. Nash, Jacobus J. Boomsma and William T. Wcislo (2009) Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants. Proceedings of the Royal Society B 276:2263-2269.

November 25, 2009

Not so fast!

I always enjoy Olivia Judson's columns in the New York Times, but today's post on evolution "failing" left out an important point. She referred to a paper published last year from Richard Lenski's long-term evolution experiment, showing that a bacterial population took 31,000 generations to evolve the ability to use citrate. Furthermore, although she didn't mention this, this trait has only evolved, so far, in one of their twelve replicate populations. If evolution is too slow to keep up with the changes we humans are making in the environment, then species that might evolve and survive if changes were slower will instead go extinct.

I agree that this is a significant problem, but I wouldn't assume that it would take polar bears, for example, 31,000 generations to evolve adaptations to warmer temperatures. The bacteria that Lenski's group studies don't have sex. So if one cell has a mutation that would allow it to use citrate, but only in combination with a second mutation found in another cell, they don't have any way to combine the two mutations in one citrate-using individual. If cells with only one mutation or the other have no advantage over cells with neither, then lineages with the first mutation will usually die out before acquiring the second mutation. A lineage could die out, for example, because the next mutation is gets is one of the many lethal ones, rather than one of the few beneficial ones.

Bacterial populations can sometimes evolve rapidly (with significant changes in only a few days) because their generation times are so short and because their large population sizes include many mutants. Evolution requiring a series of steps isn't a problem so long as each step is an improvement. But when a mutation is neutral or negative, except in the context of a second mutation, sexual species can evolve faster. Not necessarily fast enough to save the polar bears, though.

November 23, 2009

Are ants' fungus gardens a source or sink for nitrogen?

This week's paper, Symbiotic Nitrogen Fixation in the Fungus Gardens of Leaf-Cutter Ants, has already been discussed by Ed Yong, whose blog is among my favorites, and by the always-interesting Susan Milius of Science News. When she interviewed me, I endorsed the main conclusions of the article but expressed skepticism on one point.

The paper clearly shows that the fungus "gardens" cultivated by leaf-cutter ants contain bacteria that extract nitrogen from the air. The part I wondered about was their statement that:

Continue reading "Are ants' fungus gardens a source or sink for nitrogen?" »

November 11, 2009

Experimental evolution of bet hedging

Will headshot.jpg
Guest blogger: Will Ratcliff

This week's paper, "Experimental evolution of bet hedging" by Hubertus Beaumont, Jenna Gallie, Christian Kost, Gayle Ferguson and Paul Rainey, published in Nature, shows that a trait that initially evolves for non bet hedging purposes can be maintained in the population through bet hedging.

The theory of bet hedging was first mathematically developed by Daniel Bernoulli (yes, the Bernoulli we all learned about in high school physics) in 1738. Because the basic idea is so simple - uncertain future conditions make conservative strategies beneficial - it is likely that folk wisdom advising bet hedging long predates Bernoulli's maths. The phrase "Don't put all your eggs in one basket" is one example of a widespread but anachronistic reminder to spread risk. Before we dive into this week's paper, I want to briefly cover the theory of bet hedging.

Like investing in the stock market, evolution is a multiplicative process, not an additive one. Steve Stearns (2000) illustrates this well....

Continue reading "Experimental evolution of bet hedging" »

November 5, 2009

Experimental evolution meets genomics

Richard Lenski and colleagues have been monitoring evolution of the bacterium Escherichia coli in his laboratory for 40,000 generations. Their latest paper, "Genome evolution and adaptation in a long-term experiment with Escherichia coli" was recently published in Nature.

One nice thing about E. coli is that they can freeze samples of their evolving populations every few thousand generations, for later analysis. So they were able to compare the fitness of different generations by competing each against a thawed ancestor. They also found the complete DNA sequence for many of these strains....

Continue reading "Experimental evolution meets genomics" »

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?" »

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 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?" »

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 23, 2009

Staying ahead in the evolutionary arms race with viruses

This week's paper uses molecular methods to reveal new details of the evolutionary arms race between primates, including humans, and viruses. "Protein kinase R reveals an evolutionary model for defeating viral mimicry" was published in Nature by Nels Elde and colleagues in Seattle.

Protein kinase R (PKR) is an important defense against viruses in many species, from humans to yeast. When it detects a virus inside a cell, it activates eIF2-alpha, which shuts down protein production in that cell. With protein production blocked, the virus can't replicate and spread to other cells. Viruses, however, have evolved counter-measures. These include molecules that resemble eIF2-alpha. These molecular mimics interact with PKR and prevent its normal defensive activity.

Viral epidemics can be a major cause of death, so we expect populations to evolve PKR resistant to the eIF2-alpha-mimics produced by viruses. Can we find evidence of such evolution in primates?

Continue reading "Staying ahead in the evolutionary arms race with viruses" »

January 19, 2009

Safe-crackers have vaults in their cells

This is the most amazing thing I've seen in awhile. Vaults are abundant in our cells and bigger than ribosomes and apparently I'm not the only biologist who had never heard of them. They seem to be important in defense against bacteria, but nobody understands them in detail yet, apparently.

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.

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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.

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November 7, 2008

Can an NPR gene explain gregarious and solitary behavior?

This week's issue of Science has a special section on the genetics of behavior. In humans, at least, conflicting results seem to be common. According to the overview paper, one study found that people who were abused as children have a two-thirds chance of depression as adults, if and only if they also have a particular version of a serotonin transporter gene; an analysis of several studies on this gene rejected this conclusion, however. Other combinations of genes affecting testosterone and the rate at which certain brain chemicals break down may increase criminal activity, but maybe not. One company is already offering genetic testing of potential mates for a gene possibly linked to divorce. How soon will we see "in-vitro tourism", to countries that offer genetic modification of behavior-linked genes in human germ-line cells? Clinics that currently offer untested or dangerous "cancer cures" might not wait for answers to the many scientific, technical, and ethical questions that such services would raise. But genetic effects on behavior are complex and hard to predict, even in the simplest cases, as seen in this week's paper.

"npr-1 regulates foraging and dispersal strategies in Caenorhabditis elegans" was just published in Current Biology by Andrea Gloria-Soria and Ricardo Azevedo.
C. elegans is a tiny worm, barely visible without magnification. Two alleles of the npr gene produce two different versions of the NPR signal-receptor protein, differing in a single amino acid. (Despite the connection to signals, the NPR gene actually has as much to do with National Public Radio as the famous "sonic hedgehog" gene has to do with hedgehogs.)

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October 10, 2008

Experimental evolution of predation and sexual attractiveness

Fossils and DNA-sequence comparisons among species are like fingerprints and other clues found at crime scenes. We can often draw reliable conclusions about past events (evolutionary or criminal) from such physical evidence, but some people prefer eyewitness accounts. So evolutionary biologists are increasingly doing experiments that let us see evolution in action. Evolution is a change over generations, so the short generation times of microbes make them especially useful for experimental evolution.

Two recent examples, both published in Proceedings of the Royal Society, are "Experimental evolution of a microbial predator's ability to find prey", by Kristina Hillesland, Greg Velicer, and Richard Lenski, and "Experimental evolution of a sexually selected display in yeast", by David Rogers and Duncan Grieg.

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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.

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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.

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June 11, 2008

Explaining the evolutionary persistence of persisters

This week's paper is "Nongenetic individuality in the host-phage interaction"?, published in PLoS Biology by Silvan Pearl and others. This is one of many recent papers on bacterial "persisters" a topic we are also starting to explore in my own lab.

Update: In 2010, we published a paper (discussed here) showing that the bacterial symbionts of alfalfa can form a much greater percentage of persister-like cells than most bacteria. When a starving cell divides, the mother cell keeps most of the resources and then goes dormant. We see this as an example of microbial bet-hedging.

When a large population of bacteria (in an infected person, for example) is exposed to antibiotics, a few of the bacteria may survive. One explanation, which is often true, is that these survivors have genes that make them resistant to the antibiotic. For the purposes of this discussion, it doesn't matter whether they have mutated versions of genes also found in the susceptible bacteria, or an extra gene acquired by horizontal gene transfer from another bacterial cell. Either way, those without the gene (or with the nonmutated version) mostly get killed by the antibiotic. Therefore, subsequent bacterial generations are founded mainly by these surviving resistant mutants. Therefore, the frequency of the resistance gene increases over generations: a classic example of evolution.

Sometimes, however, testing the "evolved"? population for antibiotic resistance shows the same results as in the previous unevolved generation: most of the bacteria die, but a few survive. If there's no change in gene frequency over generations, then the population hasn't evolved. But then why did any of the bacteria survive?

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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.

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May 3, 2008

Sharing diseases with relatives and neighbors

Not enough people voted on the Reader’s Choice, so this week’s paper is “Phylogeny and geography predict pathogen community similarity in wild primates and humans? by Jonathan Davies and Amy Pedersen, published in Proceedings of the Royal Society.

Many humans diseases, from flu to AIDS, come from other species. Similarly, diseases from dogs are an increasing threat to lions, while cat diseases kill sea otters. Are there general rules that predict how likely two species are to share diseases?

To find out, the authors analyzed several large data sets on diseases of humans and 117 other species of primate (apes, monkeys, etc.). They hypothesized that species are more likely to share diseases if they live near each other and/or if they are more closely related, that is if they share a more recent common ancestor. This is similar to how we define relatedness in humans: brothers and sisters have more recent common ancestors (parents) than cousins do (grandparents). Fortunately, the family tree for primates is relatively uncontroversial, at least among scientists.

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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?

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March 9, 2008

Tricky parasites winning the evolutionary arms race

Two papers this week describe recently discovered sophisticated adapatations of two different parasites: Gall insects can avoid and alter indirect plant defenses, published in New Phytologist by John Tooker and colleagues, and Parasite-induced fruit mimicry in a tropical canopy ant, published in American Naturalist by Steve Yanoviak and colleagues (if you're in a hurry, skip to the end for amazing photos).

Various plants recruit "bodyguards" when attacked by insects. For example, when caterpillars start munching on corn (maize) plants, the plants (including uninjured leaves) release gaseous chemicals called terpenoids. These terpenoids attract parasitic wasps, which lay their eggs into the caterpillars. This eventually kills the caterpillars, which presumably benefits the plant. But what if the caterpillars could prevent the plant from signaling to the wasps? As far as I know, caterpillars haven’t evolved this trick (yet), but there are apparently some insects – the Hessian fly, Mayetiola destructor (say) – that do not trigger signaling when they feed on wheat plants. There are at least two possible explanations…

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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?

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February 11, 2008

Ancient temperatures inferred from DNA

"Where was you hid to see all that?" he cried. "It seems to me that you knows a great deal more than you should."? - The Complete Sherlock Holmes
"Our DNA is a coded description of the worlds in which our ancestors survived. And isn't it an arresting thought? We are digital archives of the African Pliocene, even of Devonian seas; walking repositories of wisdom out of the old days. You could spend a lifetime reading in this ancient library and die unsated by the wonder of it."? -- Richard Dawkins, Unweaving the Rainbow

Like many of the characters baffled by Sherlock Holmes, I am repeatedly amazed by the detailed inferences my fellow scientists are able to draw about events in the distant past. This week's paper:
Palaeotemperature trend for Precambrian life inferred from resurrected proteins
is a good example. Eric Gaucher and colleagues at the University of Florida and DNA2.0 Inc. used protein sequences from a variety of modern bacteria species to infer the protein sequences of their distant and more recent ancestors...

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December 7, 2007

The ghost of infections past, present, and future

Summary: A 39-year record of host-parasite interaction, recovered from sediment layers in a pond, is consistent with rapid coevolution.
Link: Host-parasite /`Red Queen/' dynamics archived in pond sediment

As I've discussed previously, archival samples often prove useful for answering questions that weren't being asked when the samples were collected. But what if nobody collected and preserved the samples you need for your research? Maybe you can find a "natural archive" that has what you need.

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November 16, 2007

Communication doesn't automatically prevent cheating

There are enough examples of ‘‘cheating’’ in bacteria ... that mindless obedience to such [quorum-sensing] chemical signals cannot be assumed. Mindlessness can be assumed, but not obedience. -- Denison et al. (2003) Ecology 84:838-845
Millions of cooperating cells can do things far beyond the ability of an individual cell. This is most obvious in multicellular organisms, whose cells cooperate because they are all genetically identical, or nearly so. Genetically diverse populations of cells could often benefit from cooperating, but do they? For example, the mixed bacteria populations associated with plant roots might benefit from keeping the plant healthy, so that it can continue to feed them with its root exudates. But for this to happen, they need some method of coordinating their plant-benefiting activities. Furthermore, cells whose genes lead to this form of cooperation must, on average, survive and reproduce more than "cheaters" who don't invest in cooperative activities. Otherwise, cooperative traits will disappear.

Quorum sensing, an exchange of chemical signals among bacteria, can solve the coordination problem. But this week's paper Cooperation and conflict in quorum-sensing bacterial populations shows that quorum sensing doesn't automatically solve the problem of cheaters. The paper is by Stephen Diggle, Ashleigh Griffin, Genevieve Campbell, and Stuart West and published in Nature.

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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 31, 2007

Whose genes are these, anyway?

Most of the genome of Wolbachia, a bacterial parasite of fruit flies, has been incorporated into the genome of the fruit-fly itself. Discussion at Not Exactly Rocket Science. Bacteria tend to pass genes around, or (more accurately, perhaps) bacterial genes tend to move themselves around (usually to other bacteria), but this is amazing.

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 12, 2007

Rhizobia, pesticides, and peer review

I have some comments on a recent paper that's only tangentially related to evolution. Actually, it's more relevant to science fair projects, the topic of my last post.

One type of science fair project my fellow judges and I are really sick of is "The effect of X on plants", where X is mouthwash, vinegar, cola, etc. The obvious question, which we always ask, is "how often are plants in the field exposed to high concentrations of mouthwash?" Unfortunately, whoever reviewed this paper in Proceedings of the National Academy of Science, claiming that "Pesticides reduce symbiotic efficiency of nitrogen-fixing rhizobia and host plants" apparently failed to ask this question.

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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 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 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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