July 19, 2013

Weed evolution in the New York Times

Carl Zimmer, author of several evolution-themed books and an interesting blog, published an article on weed evolution in Tuesday's New York Times. He used one of my favorite examples of rapid evolution of complex traits (flooding tolerance and crop mimicry in Echinochloa barnyardgrass/watergrass in <1000 years) to make the point that evolution of herbicide resistance (a much-simpler trait) in only a few years shouldn't have been a surprise.
(Left) Under selection pressure imposed by farmers with hoes, Echinochloa watergrass evolved to resemble rice more than it resembles its own recent ancestor, barnyardgrass (Barrett, 1983). I discussed this example near the end of this lecture at the International Rice Research Institute.

Glyphosate-resistant weeds are becoming increasingly common, just before the expiration of Monsanto's patent on Roundup-Ready soybeans. What does the US Constitution say about patents?

"The Congress shall have Power To...promote the Progress of Science and useful Arts, by securing for limited Times to Authors and Inventors the exclusive Right to their respective Writings and Discoveries...."
If the original intent was to give inventors short-term monopolies, in exchange for long-term benefits to society, should the duration of patent protection be shorter for inventions whose useful life is likely to be limited by evolution? For example, 17 years with a really good resistance-management plan, 5 years with no resistance-management plan.... Of course, the Patent Office might need to hire an evolutionary biologist or two.

I agree with the statement from David Mortensen that adding another resistance gene to glyphosate-resistant crops, and spraying with both herbicides, will be only "a short-lived solution," although it might last long enough to be worth patenting. If they had put two different herbicide-resistant genes into soybean from the start, and if evolution of resistance requires two or more independent mutations -- this isn't always true -- and if farmers growing that herbicide-resistant crop were somehow required to use both herbicides (so that mutants resistant to just one of the herbicides wouldn't have increased in frequency), evolution of resistance might have taken much longer.

Zimnmer quoted me and mentioned my book on Darwinian Agriculture, depleting Amazon's stock, though they still have a few copies left. You could try your favorite independent bookstore or library.

May 31, 2013

This week's picks

Functional Extinction of Birds Drives Rapid Evolutionary Changes in Seed Size "areas deprived of large avian frugivores for several decades present smaller seeds than nondefaunated forests, with negative consequences for palm regeneration"

Molecular evolution of peptidergic signaling systems in bilaterians "phylogenetic reconstruction tools... show that a large fraction of human PSs [peptide-based signaling systems] were already present in the last common ancestor of flies, mollusks, urchins, and mammals"

Honey constituents up-regulate detoxification and immunity genes in the western honey bee Apis mellifera "apicultural use of honey substitutes, including high-fructose corn syrup, may thus compromise the ability of honey bees to cope with pesticides and pathogens and contribute to colony losses"

Palaeontological evidence for an Oligocene divergence between Old World monkeys and apes" "the oldest known fossil 'ape', represented by a partial mandible... the oldest stem member of the Old World monkey clade, represented by a lower third molar... recovered from a precisely dated 25.2-Myr-old stratum in... the East African Rift in Tanzania."

Experimental evidence that evolutionarily diverse assemblages result in higher productivity "Species produced more biomass than predicted from their monocultures when they were in plots with distantly related species and produced the amount of biomass predicted from monoculture when sown with close relatives."

April 17, 2013

High-school student undermines our "famine-food longevity" hypothesis, maybe

Back in 2009, I suggested that, to the extent that organic foods provide greater health benefits, this might be due to tradeoffs with reproduction. See my original post for a more-detailed explanation. Since then, I've seen at least one paper on a diet that increases both longevity and reproduction in some species, but there were no data on the timing of reproduction, which is key to our hypothesis.

This week, however, high school student Ria Chhabra and colleagues published a paper in PLoS One reporting both greater longevity and increased egg-laying at all ages, in fruit flies fed various organic foods. It's not inconceivable that some conventionally-grown produce could be so poor, nutritionally, that it would reduce both lifespan and reproduction. But their data seem inconsistent with our hypothesis that organic-vs-conventional differences were mainly differences in toxins (synthetic in conventional, natural in organic) and that natural toxins mainly acted as environmental cues, switching physiology towards longevity at the expense of reproduction.

I'd like to see this experiment repeated by a different lab, however, before drawing firm conclusions. There are a couple of strange things in their data. First, as noted in the paper, survival curves for Drosophila are usually sigmoidal, whereas theirs are more linear. Also, their peak egg-laying rate was reportedly at an age of 1 day. Other studies I've seen show essentially no egg-laying that early, with peaks at day 5 or so. See this paper or this open-access one.

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 8, 2013

Cooperation, inducible defense, cancer, and more

Here are some papers that look interesting this week.

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

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

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

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

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

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

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

January 25, 2013

What's for dinner?

This week's picks all have something to do with food.

Tree climbing and human evolution "aspects of the hominin ankle associated with bipedalism remain compatible with vertical climbing [to collect fruit or honey]"

Earliest evidence for cheese making in the sixth millennium bc in northern Europe" "compelling evidence for the vessels having being used to separate fat-rich milk curds from the lactose-containing whey... in the manufacture of reduced-lactose milk products among lactose-intolerant prehistoric farming communities"

Anatomical enablers and the evolution of C4 photosynthesis in grasses
"when environmental changes promoted C4 evolution, suitable anatomy was present only in members of the PACMAD clade [which doesn't include rice] explaining the clustering of C4 origins in this lineage"

Macropredatory ichthyosaur from the Middle Triassic and the origin of modern trophic networks "recovery from Earth's most severe extinction event at the Permian-Triassic boundary... may have occurred faster [in oceans than on land]"

Sustainable bioenergy production from marginal lands in the US Midwest" "successional herbaceous vegetation, once well established, has a direct GHG emissions mitigation capacity that rivals that of purpose-grown crops "

Extracellular transmission of a DNA mycovirus and its use as a natural fungicide
"Our findings may prompt a reconsideration of the generalization that mycoviruses lack an extracellular phase in their life cycles and stimulate the search for other DNA mycoviruses with potential use as natural fungicides. "

January 11, 2013

Predictability, multiple fitness peaks, fungus-growing ants, pesticide resistance...

Predictability of evolution depends nonmonotonically on population size
"evolutionary predictability based on an experimentally measured eight-locus fitness landscape for the filamentous fungus Aspergillus niger.... entropies display an initial decrease and a subsequent increase with population size N"

Multiple Fitness Peaks on the Adaptive Landscape Drive Adaptive Radiation in the Wild "We measured the adaptive landscape in a nascent adaptive radiation of Cyprinodon pupfishes endemic to San Salvador Island, Bahamas, and found multiple coexisting high-fitness regions driven by increased competition at high densities"

Laccase detoxification mediates the nutritional alliance between leaf-cutting ants and fungus-garden symbionts "laccase activity is highest where new leaf material enters the fungus garden [in ant feces], but where fungal mycelium is too sparse"

A link between host plant adaptation and pesticide resistance in the polyphagous spider mite Tetranychus urticae "selection for the ability to mount a broad response to the diverse defense chemistry of plants predisposes the evolution of pesticide resistance in generalists"

See my Darwinian Agriculture Blog for links to videos of two of my talks.

September 26, 2012

Diversity of Opinions on Diversity

Cedar Creek plots weeded to maintain low diversity have low plant cover, explaining their low productivity. But why does that space stay open?

Part two of the mostly positive review by Jeremy Cherfas, on the Agricultural Biodiversity blog, argues that my Darwinian Agriculture book understates the benefits of mixing varieties (e.g., with different disease-resistance genes) within a field.

I added a comment there, noting that I had included a comparison of this strategy to an alternative way of deploying the same amount of genetic diversity. But his overall point remains valid. I think I over-reacted to what I see as a tendency to think about crop diversity mainly at fine spatial scales, while ignoring diversity at larger spatial scales and over time.

While I'm on the subject of plant diversity, I talked to Dave Tilman about the suggestion in the book that the low plant cover (see above) in his low-diversity treatments could be an artifact from their weeding protocol. He apparently has data showing that seedlings of the one "resident" species in his monoculture plots do poorly, relative to seedlings of other species. I've seen the same mechanism as an explanation for high tree-species diversity in the tropics -- species X doesn't do well near species X, perhaps due to disease.

The fact remains, however, that photons hitting soil, rather than leaves, drive water loss without contributing to photosynthesis. So it's not surprising that low-cover plots have low productivity. Crop monocultures, however, usually achieve full cover, limiting the relevance of this work to agriculture.

If I get to do a second edition, I will try to correct these flaws. Meanwhile, I see thoughtful negative comments as positive, consistent with my goal of stimulating more-insightful discussion.

September 25, 2012

Blogs discussing Darwinian Agriculture

The bloggers and commentators at Agricultural Biodiversity set the standard for insightful discussion of many agricultural issues, so I was hoping they would review my book. Jeremy Cherfas has just posted the first half of a two-part review.

Tyler Cowen also mentions my book, briefly, in the web version of his op-ed on world hunger in the New York Times, posted on his blog, Marginal Revolution.

Cherfas's review and Cowen's mention are both positive. Both are reasonable summaries. Both somewhat over-state my doubts about biotechnology's potential, however. Yes, many of the approaches suggested or tried by biotechnologists have already been tested and rejected by natural selection. But some tradeoffs rejected by natural selection may be acceptable to us. Less-bitter cucumbers may attract rabbits, but we can build fences.

Eventually, we may learn how to design and implement improvements so radically different from anything that exists now that they have never been tested by natural selection. Radical innovations may carry unknown risks, however.

September 24, 2012

Comments on Forbes article on biomimicry

Steven Kotler, at Forbes, recently posted a story titled "Move Over Genetic-Engineering; Biomimicry Seems The Better Bet For Solving Global Hunger."

The Forbes site said I could comment using my Google identity, if they could just have access to my contact list. No thanks. I"m amazed it's even legal to ask, if it is.

So I'll comment here. Biomimicry is a major theme of my recently published book, Darwinian Agriculture -- but biomimicry of what?

The adaptations of individual plants, animals, and microbes have been improved (by the criterion of Darwinian fitness in past environments) through millions of years of competitive testing against alternatives. But larger-scale patterns we see in nature, such as the total number of species in a forest, or how trees are arranged, haven't been tested competitively. Trees compete against trees, but forests don't compete against forests.

If we copy individual adaptations of trees, we are copying the winners of many past rounds of competition. A forest may have persisted for thousands of years, so it's probably not too dysfunctional. But it hasn't been tested through repeated competition, so there's likely to be plenty of room for improvement.

I would have expected a writer at Forbes -- do they still call themselves "a capitalist tool?" -- to understand how competition is key to improvement, but apparently not.

Now, what about the specific examples in the Forbes post? Spiders compete against spiders and sharks compete against sharks, so it's not surprising that spider silk and shark skin are awesome.

But his "favorite" example is that wildlife corridors that mimic electric circuits work better. I'm not sure what point Kotler is trying to make here -- did he not notice that this is biomimicry in the opposite direction? Although caribou have competed against caribou, curved and straight wildlife migration corridors haven't competed against each other. (OK, maybe they have competed for caribou and their manure, sort of, but the winning corridors don't produce "offspring" with the same degree of curvature.) So this case calls for intelligent design by humans, not mimicry of large-scale patterns seen in nature.

And then there's the endophyte example. Some fungi that live inside plants can provide major benefits to those plants. We will be reading and discussing journal articles about this in a couple weeks, in our graduate seminar.

If there were only one fungus per plant, fungi that benefit their hosts would thereby benefit themselves. But mixed infections seems to be common. With mixed infection, a fungus that invests resources to benefit the host is like someone who pays taxes when nobody else does. Admirable, perhaps, but not likely to be very successful. It's a variation on the classic "tragedy of the commons."

One benefit often provided by endophytes is chemical defense against a plant's enemies. This case isn't too hard to understand. Maybe the various fungi make toxic chemicals to attack each other, since they're competing for the same plant resources, and those same toxins also protect against insects that might otherwise eat the plant.

But how and why do endophytes improve drought tolerance? Unlike mycorrhizal fungi, which extend out into the soil, most endophytes are entirely inside the plant. So it's not as if they can pull more water out of the soil. Sure, they can produce chemicals that mimic plant hormones, thereby manipulating the plant to make more (or fewer) roots or to open (or close) the stomata through which water evaporates from leaves.

But it's hard for me to believe that:
1) a fungus infecting a plant is a better judge of how many roots a plant needs than the plant is
2) that the fungus would put the plant's interests ahead of its own.

It's a mystery. But that's what science does: solve mysteries. Stay tuned.

August 27, 2012

Another route to drought-tolerant crops?

My book, Darwinian Agriculture, argues that the quickest route to crop genetic improvement is to identify tradeoffs that were rejected by past natural selection, but which we are willing to accept. Tradeoffs between individual-plant competitiveness and the collective performance of the whole crop are particularly promising. "MAT kinase", the Scientist Gardener suggests that this is the key to Monsanto's DroughtGard corn:

"From what I've heard, the yield gain of this variety under drought occurs because it slows its growth specifically under drought stress such that existing soil moisture is saved for the critical period surrounding flowering, resulting in less kernel abortion, higher harvest index and greater yield. This is certainly ironic given the expectations of many field physiologists and breeders. It also occurs to me that this is consistent with the thesis of Denison's Darwinian Agriculture - that evolution has already maxed out our crops' ability to deal with most stresses and environments, and that the greatest potential for improvement exist in traits that only work in an ecosystem (such as a farm field), where plants aren't in competition with their neighbors. "

This drought-tolerance-via-slower-growth would be quite interesting, if true, and similar to an idea I discuss in the book in the context of drought-tolerant Drysdale wheat.

In a recent post, I had suggested an alternative idea, that the bacterial gene they transferred to corn might result in a phenotype so radically different that natural selection had never had a chance to test it, in corn or its wild ancestors. I like The Scientific Gardener's hypothesis better. The problem with radically new phenotypes, of course, is that it's very hard to predict all of their effects and side effects.

August 10, 2012

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

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

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

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

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

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

August 9, 2012

Darwinian agriculture and Darwinian medicine: beyond resistance management

DarwinianMedicine.jpg Thumbnail image for BookCover.gif

Evolution happens. Careless use of antibiotics selects for antibiotic-resistant pathogens, careless use of insecticides (including crops that make their own insecticides) selects for pesticide-resistant insect pests, and careless use of herbicides selects for herbicide-resistant weeds.

Many people seem to assume that this well-known problem, evolution of resistance, is all there is to "Darwinian medicine" or "Darwinian agriculture." But check the tables of contents of the books above. You'll only find one chapter on the "arms race" between pathogens and their hosts and one chapter (titled "Stop Evolution Now!") that focuses on slowing the evolution of resistance to pesticides and other pest-control measures.

Both books (Nesse and Williams, 1994, Denison, 2012) and the earlier review articles on which they were based (Williams and Nesse, 1991, Denison, et al., 2003) devote much more space to the implications of past evolution.

"If evolution by natural selection can shape sophisticated mechanisms such as the eye, heart, and brain, why hasn't it shaped ways to prevent nearsightedness, heart attacks, and Alzheimer's disease?"

Similarly, biotechnology allows us to increase the expression of crop genes that enhance drought tolerance, but

"mutations that increase gene expression happen all the time, and natural selection maintains those that are beneficial to the plant. So why does corn normally have lower expression of this gene than was obtained by genetic engineering?"

We don't have definite answers to these questions. Both books present hypotheses with various amounts of supporting data, but additional research is needed. With aging populations and rising food prices, maybe there will even be some money available to fund that research.

Should evolutionary biologists working on fundamental problems and/or wild species consider adding applied work to their research portfolios? If so, you or your students might get some useful ideas from Nesse and Williams or from my book, just published by Princeton University Press.

Literature Cited

Denison RF. 2012. Darwinian agriculture: How understanding evolution can improve agriculture. Princeton: Princeton University Press.

Denison RF, Kiers ET, West SA. 2003. Darwinian agriculture: when can humans find solutions beyond the reach of natural selection? Quarterly Review of Biology 78: 145-168.

Nesse RM, and Williams GW. 1994. Why we get sick: The new science of Darwinian medicine. New York: Vintage Books.

Williams GW, Nesse RM. 1991. The dawn of Darwinian medicine. Quarterly Review of Biology 66: 1-22.

July 9, 2012

Sold out!

Thumbnail image for BookCover.gif
The Princeton University Press table has sold all the copies of my Darwinian Agriculture book they brought to the Evolution meetings. They didn't have that many, but apparently it's out-selling their other books here. You can still order from them or your local independent bookstore.

June 28, 2012

Evolutionary tradeoffs and drought-tolerant crops

The Union of Concerned Scientists recently sent me a link to a report arguing that "Genetic Engineering is not Solving Agriculture's Drought Problem." This is an issue I address in detail in my book on Darwinian Agriculture, which will be available at the upcoming Evolution Meetings in Ottawa and more widely by the end of July.

Briefly, my argument is that mutant plants with greater or less expression of existing genes must have arisen repeatedly over the course of evolution. Some of those mutants were presumably more drought-tolerant than their parents, while others were less drought-tolerant. If there were no disadvantages to a given drought-tolerance gene, then plants with that gene took over. Repeat this process of natural selection for millions of years, and there may be few remaining opportunities for further improvements that are both simple (i.e., achievable by the sort of mutations that arise reasonably often) and tradeoff-free (never having negative effects on fitness, at least in past environments). My book therefore raises doubts about increasing the expression of existing plant genes to improve drought tolerance.

This argument applies to conventional breeding, not just genetic engineering. Another key point is that some tradeoffs rejected by past natural selection may be acceptable in an agricultural context. In fact, accepting acceptable tradeoffs may often be the fastest route to progress.

It's not entirely clear, however, whether my concerns above apply to the particular transgenic crop discussed in the Union of Concerned Scientists report. Monsanto's "DroughtGard" corn (maize) contains a gene derived from bacteria. Does this gene result in a phenotype very different from any seen in the recent evolutionary history of corn? If so, then we can't assume that this approach to drought tolerance has been repeatedly rejected by past natural selection. It may never have been tested by natural selection. Rather than rejecting it on theoretical grounds, therefore, we would need actual field data to determine the advantages or disadvantages of this transgenic variety.

Of course, those data would need to come from independent tests, not run or paid for either by Monsanto or by one of their commercial competitors. Agricultural universities run such tests every year, comparing crop varieties developed by different companies and by public-sector plant breeders. I look forward to seeing how DroughtGard does in such tests.

April 19, 2012

A taste of Darwinian Agriculture

My book on Darwinian Agriculture should be available in June. If you think you might want to read it, Princeton University Press has information, including a PDF of the first chapter.

February 10, 2012

Measuring fitness benefits to rhizobia from symbiosis with legumes

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

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

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

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

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

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

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

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

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


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

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

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

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

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

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

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

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

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

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

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

February 1, 2012

What aspects of nature has natural selection improved?

Much of my forthcoming book, "Darwinian Agriculture", explores possible improvements to agriculture inspired by nature. But what aspects of nature should we copy? A preview of some of my ideas has just been published online by, an web magazine of "Intellectual Jousting in the Republic of Letters."

January 20, 2012

Also this week...

Variation in cognitive functioning as a refined approach to comparing aging across countries "The degree to which demographic aging translates into societal challenges depends to a considerable extent on the age at which mental functioning becomes significantly impaired.... In several countries with older populations, we find better cognitive performance on the part of populations aged 50+ than in countries with chronologically younger populations."

Large-scale, spatially-explicit test of the refuge strategy for delaying [sprayed] insecticide resistance
"refuges delayed resistance and treated cotton fields accelerated resistance"

The evolutionary basis of human social learning "We tested nine hypotheses derived from theoretical models, running a series of experiments..."

Collaborative learning in networks "In contrast to prior work, however, we found that efficient networks outperformed inefficient [slower] networks, even in a problem space with qualitative properties thought to favor inefficient networks."

Historical contingency affects signaling strategies and competitive abilities in evolving populations of simulated robots "populations with the more complex [but less efficient] strategy outperformed the populations with the less complex strategy"

The spread of a transposon insertion in Rec8 is associated with obligate asexuality in Daphnia "this element may be in the process of spreading through the species"

January 4, 2012

Pre-order "Darwinian Agriculture"

Amazon.UK has been listing my book for a while and now says it's #5 in Crop Production and #6 in Biotechnology, based on pre-orders. Order from them and maybe you can help it overtake The Cannabis Grow Bible for third place.

Oops! Biomimicry just leap-frogged past Darwinian Agriculture with a Kindle edition, to take #1 in Biotechnology, somehow bumping Darwinian Agriculture to #10 (just ahead of Little Book of Beer Tips).

You can also order from in the US or direct from Princeton University Press.

August 12, 2011

This week's picks

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

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

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

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

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

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

Bacterial persistence by RNA endonucleases

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

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

August 7, 2011

Nitrogen-fixing cereals?

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

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

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

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

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

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

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

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

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

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

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

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


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

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

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

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

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

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

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

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

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

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

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

July 23, 2011

Beneficial infections?

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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


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

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

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

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

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

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

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

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

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

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

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

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

July 8, 2011

Resistance is futile!

Pathogens and pests evolve resistance to our control measures, from antibiotics and pesticides to crop rotation and pest-resistant crop varieties. Slowing the evolution of resistance is an important practical application of evolutionary biology.

An iconic agricultural example, discussed in my forthcoming book, is the "high-dose/refuge strategy" to slow the resistance of crop-eating insects to the bacterial toxin, Bt, which has been genetically engineered into corn, cotton and other crops. The "high dose" refers to crop Bt levels high enough that only insects with two resistance genes (genotype rr) can survive. Bt-free refuges serve as a source of so many susceptible (ss) insects that any rs mutants that arise will mate with them (producing susceptible ss and rs progeny) rather than with each other (with 25% of their progeny resistant rr).

But rs mutants could arise in the Bt-free refuge, not just in the Bt crop. If, in the refuge, the fitness of rs mutants is as high as that of ss insects (i.e., if there is no cost to Bt resistance), then rs individuals could become common enough that two of them could mate, producing rr progeny that could then devastate the nearby crop. So it would be good if, in the refuge, rs insects had lower fitness than ss insects.

This week's paper shows one way that this goal might be achieved. "Fitness Cost of Resistance to Bt Cotton Linked with Increased Gossypol Content in Pink Bollworm Larvae" was published recently in PLoS One.

Continue reading "Resistance is futile!" »

June 3, 2011

Darwinian agriculture: health benefits of organic vegetables

I'm making final revisions to my book, "Darwinian agriculture: where does nature's wisdom lie?" [they made me change the title, too] and my editor, at Princeton University Press, has asked me to cut two chapters. I agree that doing so will give the book a narrower focus, but I think some people might find them interesting. So here's the first of the missing chapters.

Beneficial toxins, evolutionary tradeoffs, and the health benefits of organic vegetables

"Early births are worth more than late in an increasing population, and vice versa in a decreasing one." -- Hamilton. 1966

What about food quality?

Early in 2011, a majority of the world's population could afford to buy enough food to meet their basic needs for protein and food energy, although this may not always be true in the future. But some diets are better than others. Vegetables appear to be particularly health-promoting.

Some of the income from my brother Tom's family's organic farm (near Corvallis, Oregon) comes from "community supported agriculture" subscriptions, where families pay an annual fee for a weekly food box from his farm. I once asked him whether people save money by buying these subscriptions.

"They save money on their medical bills," he explained. This is because one of his boxes contains more vegetables than most families would otherwise eat. Rather than waste vegetables they've already paid for, they eat them, presumably improving their health.

Why are vegetables so good for us? They provide fiber, vitamins, and antioxidants, all apparently beneficial, but can these explain all of their health benefits?

Continue reading "Darwinian agriculture: health benefits of organic vegetables" »

March 11, 2011

Aging primates, agricultural ants, efficent cooperation, etc.

Lots of interesting papers this week, but I only have time for some brief comments.

I can't believe Obama's response to the earthquake in Japan was to go ahead with a speech on gasoline prices. (BBC cut him off!) Higher prices for nonrenewable resources are an efficient way (relative to rationing, say, or complicated mandates) to encourage us to use them more slowly, so they'll last longer. And although adding more carbon dioxide to the atmosphere may increase photosynthetic efficiency and make our winters here in Minnesota a little less cold, I'm not willing to bet that those benefits will outweigh risks such as rising sea level from melting glaciers. If civilization must be at war with nature, I'm on the side of civilization, but let's not shoot ourselves in the foot. For example, we can stay warm inside insulated houses, while agricultural pests perish in the cold, reducing the need for pesticides later. Cold winters are good! Hmmm... maybe I should turn comments back on; but I'm still deleting all commercial links.

Aging in the Natural World: Comparative Data Reveal Similar Mortality Patterns Across Primates "in neither females nor males did we find evidence of a negative correlation between IMR [initiral mortality risk, at onset of adulthood] and RoA [rate of aging, increase in mortality with age],which would be indicative of a trade-off..."
[I wouldn't have expected a trade-off between those parameters, but what about a tradeoff with reproduction (mentioned only in the definition of adulthood)?]

How within-group behavioural variation and task efficiency enhance fitness in a social group "females of both phenotypes [aggressive versus docile] experience increased fitness when occupying colonies containing unlike individuals"

Experimental peripheral administration of oxytocin elevates a suite of cooperative behaviours in a wild social mammal

Co-Residence Patterns in Hunter-Gatherer Societies Show Unique Human Social Structure

The influence of maternal effects on indirect benefits associated with polyandry

Primate extinction risk and historical patterns of speciation and extinction in relation to body mass

Evolution of cold-tolerant fungal symbionts permits winter fungiculture by leafcutter ants at the northern frontier of a tropical ant-fungus symbiosis

Structural basis for nonribosomal peptide synthesis by an aminoacyl-tRNA synthetase paralog

Global CO2 rise leads to reduced maximum stomatal conductance in Florida vegetation

February 18, 2011

Free downloads of applied evolution papers...

...from the Applied Evolution Summit (Heron Island, 2010) are available, temporarily, from Evolutionary Applications.

I've already discussed part of my paper, "Past evolutionary tradeoffs represent opportunities for crop genetic improvement and increased human lifespan".

I also made minor contributions to two overview papers:
Evolutionary principles and their practical application
and Evolution in agriculture: the application of evolutionary approaches to the management of biotic interactions in agro-ecosystems.

Check out these and other exciting papers and download the ones you want, before they go behind a pay-wall. Some of these would be great for participatory seminars.

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 21, 2011

Modeling reproduction/longevity tradeoffs and phenotypic plasticity in fluctuating environments

A year ago, I was passing through beautiful Brisbane (in the news recently because of disastrous flooding) on my way back from the Applied Evolution Summit on Heron Island. This week, I'll discuss one figure from a paper I wrote for that meeting. An online-early version of "Past evolutionary tradeoffs represent opportunities for crop genetic improvement and increased human lifespan" is up at Evolutionary Applications, which will publish a special issue of papers from the meeting.

Continue reading "Modeling reproduction/longevity tradeoffs and phenotypic plasticity in fluctuating environments" »

December 12, 2010

Conditional cooperation and forest management

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

Continue reading "Conditional cooperation and forest management" »

October 8, 2010

Why do leaves really track the sun?

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

Does increased shading outweigh the photosynthetic benefits of tracking?

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

August 24, 2010

Another way to alarm aphids

A new paper in Current Biology shows that aphids drop off their host plant when breathed on by an animal that's about to eat the plant: Mammalian herbivore breath alerts aphids to flee host plant.

Last week I discussed a paper about transgenic plants that make aphid alarm signals, scaring them away (at least for a generation or two). This latest paper suggests a related approach. Getting crops to release hot, humid "breath" might be hard, but could we make a machine to blast crops with artificial breath, maybe in greenhouses?

August 19, 2010

Evolution-proof pest-resistant crops?

This week's paper is "Alarm pheromone habituation in Myzus persicae has fitness consequences and causes extensive gene expression changes", published in PNAS by Martin de Vos and others.

Aphids suck. This wouldn't be too big a problem for their host plants, except that they sometimes transmit viruses. Some plants repel these pests by giving off gases very similar to the chemical alarm signals aphids release when attacked by predators. Could crops be genetically engineered to do this? Probably, but would it work, or would the aphids evolve to ignore these signals and keep on sucking?

To answer this question, the authors studied aphids on plants genetically engineered to make aphid alarm signal.

Continue reading "Evolution-proof pest-resistant crops?" »

July 23, 2010

Reversing evolution: crops evolving into weeds

Evolutionary Applications will be publishing a special issue on evolution and agriculture. Some of the papers are already available online. One that caught my eye is "Crops gone wild: evolution of weeds and invasives from domesticated ancestors" by Norman Ellstrand and others. (Among Ellstrand's past contributions is work on gene flow from transgenic crops to their wild relatives.)

They looked for cases where long-domesticated crops (>1000 years) evolved into weeds. Of 13 cases, seven involved hybridization, mostly with a wild relative. Many cases involved reversal of evolutionary changes that had occurred during domestication. As I point out in my forthcoming book on Darwinian Agriculture, much of crop genetic improvement has involved reversing effects of past natural selection that are undesirable in agriculture.

For example, nine species re-evolved seed shattering (scattering seeds as soon as they're mature), a trait seen in many weeds and in the wild ancestors of crops, but often lost during domestication. With harvesting by humans, seeds scattered on the ground apparently have worse survival prospects than those that get harvested. Even though the majority of harvested seeds get eaten, some are saved, protected from animals, and carefully planted the next year.

Similarly, three species re-evolved seed dormancy. This trait of wild plants and weeds delays growth of some seeds for a year or more, decreasing the risk that all of a plant's offspring will be killed in a bad year. Dormancy in a crop, however, results in (for example) soybeans coming up in the corn and being killed by herbicides to which corn is resistant.

One trait that was rarely reversed was looking like the crop. A weed that resembles the crop is less likely to be killed by hand weeding. I was familiar with an earlier study by Barrett (1983)showing that the rice-field weed, watergrass, evolved to resemble rice more than its own recent ancestor, barnyard grass, presumably because weeds that look more like rice are less likely to be removed by human weeders (Ehara and Abe 1950).

Continue reading "Reversing evolution: crops evolving into weeds" »

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 7, 2010

E-word in NYT -- a bigger surprise than Roundup-ready weeds?

There have been isolated reports, for years, of various weeds evolving resistance to glyphosate (sold commercially as Roundup etc.), but now glyphosate-resistance is showing up in pigweed, a major problem for farmers in the US and elsewhere. Among alternative ways to kill weeds, other herbicides are mostly more toxic and break down more slowly, whereas mechanical cultivation tends to increase erosion.

On the positive side, maybe more people will buy my book on Darwinian Agriculture, although I'll have to revise it before publication to turn what was a prediction into a fact. Maybe I can get some Neanderthal crackpot with a radio show to accuse me of deliberately spreading Roundup-resistant weeds to increase sales. You can't buy publicity like that! But I'd rather have clean rivers than a best-selling book.

I was impressed that many of the experts discussing the problem in the New York Times referred to "evolution" or "natural selection", although one referred to weeds as "opponents that can adjust" (as if individual plants were trying different ways to survive herbicides) and said that some weeds can "mutate to survive", as if mutation were somehow directed. Plants have evolved so that individuals can adjust to certain changes in their environment (drying soil, for example). But it's populations, not individuals, that evolve. And, in this case, they evolved mainly because herbicide-susceptible individuals did not survive. I assume the author knows this, but some readers could be misled.

Maybe now people will start paying more attention to management practices that slow the evolution of herbicide resistance. Resistance-management programs for insect pests, to slow the evolution of resistance to the Bt toxin, seem to be working reasonably well, but there's nothing similar in place for weeds yet.

One important difference is that the insects plaguing an individual farmer may well come from a distant neighbor, so there's little individual incentive to implement expensive resistance-management programs. An individual farmer's weed problems, on the other hand, are much more dependent on how they were managed on that same farm in the past. So farmers may be more motivated to invent and implement resistance-management strategies for weeds.

One of my favorite weed management strategies is alternating, every few years, between using a field for grazed pasture, where weeds of row crops tend to die out, in rotation with row crops, where pasture weeds tend to die out. That requires farmers with the expertise and willingness to work with both crops and livestock, however. And milk or meat from animals eating mostly grass and clover may be more expensive than the same products produced in a feedlot.

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" »

February 5, 2010

Tradeoff-free drought resistance?

I'm working on the last chapter of my book, Darwinian Agriculture: where does Nature's wisdom lie?, and will be sending it to Princeton University Press soon for their review process. So I'm alert for any information that might make me change my main conclusions.

One theme of the book, and also of my recent talk at the Applied Evolution Summit, is that past natural selection is unlikely to have missed simple, tradeoff-free improvements. So I'm always skeptical when someone speculates that we could double crop yield just by increasing the expression of some newly discovered "drought-resistance gene." My rationale is that mutants with greater expression of any given gene are simple enough to have arisen repeatedly over the course of evolution. (This contrasts with more-complex adaptations, like the ability to form a symbiotic relationship with nitrogen-fixing bacteria, which natural selection may have had fewer opportunities to test.) If past natural selection has repeatedly rejected these "drought-resistant" mutations, then they must have been some negative effects on fitness, at least in past environments.

But could some mutations repeatedly rejected by past natural selection still be beneficial in agriculture? Maybe. Tradeoffs that constrained past natural selection need not always constrain us, as discussed below. But, I suggested at the meeting, we can't just ignore them.

However, someone called my attention to Drysdale wheat, developed in Australia, and reported to have higher yield under drought than older varieties, without any apparent yield penalty under wetter conditions. Is this an example of a tradeoff-free improvement missed by past natural selection?

The answer can be found in a very interesting paper, Breeding for high water use efficiency, published in Journal of Experimental Botany in 2004 by A.G. Condon, R.A. Richards, G.J. Rebetzke and G.D. Farquhar. If you are at all interested in this topic, the entire paper is well worth reading. But here are some key points....

Continue reading "Tradeoff-free drought resistance?" »

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 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?" »

September 2, 2009

Effective communication on preserving crop diversity

This talk by Cary Fowler, on the Global Seed Vault at Svalbard, is worth watching both for the content and as a model for effective public speaking. For that reason, I've categorized it under "careers in science" as well as "agriculture." Note the lack of bullet-point slides!

[Note added 9/11: text slides can make presentations boring, but handouts of text slides help students focus on understanding rather than scribbling notes. So I'm going to cut down on text slides in talks at meetings, but not necessarily in guest lectures to undergraduate classes.]

It's worth noting that even dry, frozen seeds may lose viability in storage. (You could probably still recover DNA, but that's only of practical value for the few traits, if any, whose value can be identified from DNA sequence alone.) So it's good to take seeds out of storage and grow fresh seed periodically. Usually, you want to do this in a way that minimizes natural selection in the seed-increase environment, to avoid losing traits that were useful where the crop was grown originally. For example, you want plants far apart enough that tall plants don't shade shorter neighbors enough to keep them from producing seed. And you don't want plants that were particularly prolific in the seed-increase environment to be over-represented in your next stored sample. Preserving crop diversity is a vastly under-funded activity, although that is true of most areas of agricultural research without immediate links to short-term profit.

Although even a few stored seeds can be multiplied enough in a few years to deal with slowly developing problems, such as climate change, if there's a global wheat epidemic you need at least enough disease-resistant seed on hand that one cycle of seed multiplication will meet farmer needs for the next growing season.

September 1, 2009

This is scary and a couple of other sites are advertising my book before I've even sent a completed version to Princeton University Press. I'm fairly happy with what I've written so far, but I'm not sure I'll finish this month. doesn't have my book listed yet, but they are selling a crop physiology book with a chapter I wrote on Darwinian Agriculture.

August 25, 2009

Vertical farms: a pyramid scheme?

I hate to bash the New York Times twice in one week, but this is such a stupid idea that I hardly know where to start. Some guy thinks we should build multistory skyscraper "farms" in New York City. He claims that:

For every indoor acre farmed, some 10 to 20 outdoor acres of farmland could be allowed to return to their original ecological state (mostly hardwood forest). Abandoned farms do this free of charge, with no human help required.
What about the abandoned farmers? But I'm not really worried about them, because this is not going to happen, at least not on a scale that poses an economic threat to many farmers.

If hydroponics is as wonderful as claimed in this article, do you wonder why most farmers still grow stuff in soil, rather than covering their fields with hydroponic tanks? Hint: it's not because they're stupid.

Growing plants on the roof of a building -- a "green roof" -- poses various challenges, but at least a roof can get the same amount of rain and sunlight as a ground-level garden would, assuming no shading by nearby buildings. With a multilevel "vertical farm", however, water and light must somehow be divided among the levels. OK, if the tower is taller than anything nearby, it can get some sunlight coming in sideways, but consider the geometry...

Continue reading "Vertical farms: a pyramid scheme?" »

July 31, 2009


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

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

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

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

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

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

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

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

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

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

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

July 20, 2009

Join my lab?

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

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

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

July 9, 2009

Has natural selection been asleep at the switch?

"This new forage has great insect resistance", effused a former colleague, "we just need to eliminate the toxins that keep sheep from eating it."

Genetically engineered drought-tolerant crops are introduced with great fanfare, only to disappear when they turn out to have low yield under nondrought conditions.

When natural selection falls short of perfection, it may be because "you can't get there (some desirable adaptation) from here (current genotypes)" without passing through a series of intermediate generations that would have lower fitness. Natural selection favors genotypes best-adapted to current conditions, which are not necessarily steps towards any long-term improvement.

But natural selection often seems to miss even "simple" improvements, that might be achieved by changing as little as one DNA base. Such small changes are often enough to increase or decrease expression of key genes, for example. This sort of evolutionary progress may be blocked by tradeoffs, e.g., between seed production under different conditions (e.g., wet vs. dry), or between the competitiveness of individual plants and their collective seed production.

So what are we to make of two recent papers (in Science and Nature, respectively, discussed in Science News) on extending lifespan, one using calorie restriction and the other using the antibiotic, rapamycin?

Calorie restriction has been shown to increase longevity in model species like nematode worms and mice, but this latest study shows clear benefits in monkeys. The obvious question -- at least, it was obvious to me -- is why has past natural selection given monkeys (and fruitflies, and nematodes, and mice...) appetites that make them eat more than is good for them?

At least, that seemed to be the question, until it was shown that food odors can reverse the beneficial effects of calorie restriction, at least in fruitflies and nematodes. In humans, soft drinks with artificial sweeteners turn out to be just as likely to cause "metabolic syndrome" (related to diabetes) as those with sugar. So apparently our lives can be shortened by a perception of abundance, not just by actually eating too much. What is going on here?

In this case, the evolutionary tradeoff seems to be between current and future reproduction. As discussed in last week's post, delaying reproduction usually decreases fitness (representation in the next generation, relative to others) when population is increasing, but delaying reproduction can increase fitness when population is decreasing. Calorie restriction predicts population decline, triggering physiological responses that delay reproduction and thereby increase longevity. So do bitter-tasting foods, traditionally eaten only during famines. Food odors or sweet tastes have the opposite effect, because they predict population increase.

But what about life extension by rapamycin? One known tradeoff is suppression of the immune system, so we might get longer lives only in a hypothetical germ-free environment. But could the protein target of rapamycin (TOR) also be important to reproduction? Is this yet another example of a longevity-vs.-reproduction tradeoff?

May 30, 2009

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

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

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

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

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

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

May 1, 2009

Sibling rivalry in plants

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

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

Continue reading "Sibling rivalry in plants" »

March 5, 2009

What I should have said to Richard Dawkins

Richard Dawkins gave a pretty good talk here last night. I have often thought that much political and religious speech (Jindal trying to talk folksy, for example) sends the underlying message "We X are kin, distant cousins or something maybe; They are not; give me your vote, your money, or your sons' lives and I will defeat Them." But I hadn't heard the term "fictive kin" used to describe this illusory relationship.

I also got to join a large group of students and faculty for lunch with Dawkins. What I should have said was "I'm writing a book called Darwinian Agriculture, heavily influenced by The Selfish Gene." Instead, I thanked him for calling my attention (when we met several years ago) to a paper about human-imposed group selection in chickens leading to increased egg production. A theme of my book is that humans can sometimes impose strong enough selection for group-level performance to overcome individual selection that undermines group performance (e.g., selecting for wheat that puts more resources into grain and less into tall stems to shade out competitors), whereas nature rarely if ever does that. But I think he just heard "group selection" and tuned me out. It must be tiring touring like that.

December 21, 2008

Spatial structure and the evolution of cooperation between microbes and plants

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

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

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

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

August 28, 2008

Bias in science vs. honest errors

Some comments attached to the previous post discuss cases where scientists made statements or drew conclusions that turned out to be wrong. When should we suspect bias, as opposed to honest errors? Some scientists, of course, may have financial conflicts of interest, such as stock in tobacco or biotech companies. But strong opinions can be a source of bias even without a direct conflict of interest.

Here's an example from my own past research. For ten years, I directed the Long-Term Research on Agricultural Systems project at UC Davis. This huge field experiment included comparisons of organic and conventional farming methods. (LTRAS also compared irrigated and nonirrigated systems, which you might think would generate more interest, given how much of California's limited water supply is used by agriculture. But these comparisons never generated as much controversy, for some reason.)

The simplest way to compare conventional and organic systems would be to have the organic system exactly like the conventional one, only without the synthetic fertilizers and pesticides. But no serious organic farmer would farm that way.

So, for example, we substituted compost and nitrogen-fixing cover crops for fertilizers in the organic system (and in several alternative systems that were not strictly organic). OK, but which cover crops? A scientist biased against organic methods could tilt the balance in favor of the conventional system just be choosing a bad cover crop. A lazy scientist, or one pressed for time or money, could choose a cover crop based on published data (trying to match local conditions) or by asking a nearby organic farmer for a recommendation. Ideally, one would start with such sources but then test various alternatives before making a final decision. At LTRAS, Martha Jimenez tested four cover crop species, each at two seeding rates, and two combinations. Woollypod vetch or a mixture of vetch and peas did best in her one-year experiment, so Dennis Bryant and his crew tested these options over three years before deciding. (Vetch+peas proved to be the least risky, even though vetch-only did slightly better under ideal conditions.) Similarly, we tested Farm Advisor Tom Kearney's suggestion that we should use a different corn cultivar in systems without nitrogen fertilizer. (These tests and other results for the first nine years of this 100-year experiment have been published: see Field Crops Research 86:267; email me if you want a PDF). Without this "tuning", the organic system would have done worse than it did. Similarly, we tried to optimize each of the nine other systems at LTRAS within its particular system-specific constraints. For example, irrigating the nonirrigated system was not an option, but we did choose a wheat cultivar suited to nonirrigated conditions.

Here's where concerns about bias come in. For each system, someone who suspected us of bias could claim that we should have done more to optimize their favorite system. For example, if timing of cultivation is important in all systems, but especially in organic ones, should we always have given the organic systems priority when scheduling, even if that meant neglecting conventional ones in ways no conventional farmer would do? I know that we were committed to finding out which methods are best, rather than trying to prove preconceived ideas. But that doesn't mean we always made perfect decisions. And why should you believe me? After all, my brother Tom Denison is an organic farmer; I could be biased by that or by a graduate education and postdoctoral work in Crop Science that those not familiar with my advisers Tom Sinclair and Bob Loomis might assume was "brainwashing." (It would be more accurate to call their efforts "brain-building.")

If individual scientists or groups of scientists have conscious or unconscious biases, that may influence their conclusions and even their results. Fortunately, two solutions to this problem are built right into the fabric of science today. The first is peer review. Before a paper is published in any reputable scientific journal, it is reviewed by at least two experts with no direct connection to the authors of the paper. (We may know each other, however.) These reviewers look for problems such as unreliable methods, inconsistency between results and conclusions, and inconsistency with previously published results. The latter should not lead to rejection, but reviewers should insist the discrepancy be discussed. Note that most books, web sites, pamphlets, popular magazines, television program, and even certain "junk journals" (low citation impact is a clue) have little or no peer review. As I result, I have usually found reading such sources to be a waste of time. For example, critical details needed to assess the reliability of results are often left out.

Second, and more important, any really important conclusions need to be based on results confirmed by at least two independent groups. This is the best way to detect fraudulent or biased results: do other research groups, who may have different biases, nonetheless get the same results? This is one reason society would benefit from investing more in research. When research money is scarce, studies needed to confirm or refute important results may not get done.

With peer review and independent testing of important results, the biases and errors of individual scientists do not prevent the scientific community from reaching reliable conclusions, sooner or later.

August 21, 2008

Ask the right experts

A book review titled "Redefining 'natural' in agriculture" makes some interesting points. I haven't read the book, which is about organic farming and transgenic crops, although I know both authors slightly from my years as a professor at UC Davis. The review notes that many people have strong opinions about agricultural issues even though they lack relevant expertise. Anthony Trewavas, the author of the review, suggests that even "being a scientist doesn't qualify you to advise on any subject except your specialty."

So what is his own specialty?

Continue reading "Ask the right experts" »

May 25, 2008

Pest control for ants


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

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

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

Continue reading "Pest control for ants" »

April 9, 2008

Welcome, fellow Dr. Tatiana fans!

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

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

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

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

February 18, 2008

Natural enemies complicate reproductive tradeoffs

Semelparous plants and animals are those that reproduce only once, whether after a few months of growth (annual plants, like wheat) or after years (“century plant? or most salmon). Iteroparous species iterate. That is, they reproduce repeatedly. For example, perennial grasses may produce seeds every year for a decade or more.

One reason this difference matters is that perennial crops may have some environmental benefits, relative to annual crops. Plowing, traditionally more common with annual than perennial crops, can greatly increase soil erosion, especially on steep slopes. So there is increasing interest in developing perennial grain crops as an alternative to wheat.

However, perennial plants have lower seed yield than their annual relatives, so we would need to devote more land to agriculture to get the same amount of grain. One reason for the yield difference is that an annual plant can transfer most of the carbon (energy) and nitrogen (needed for protein) from its leaves, stem, and roots into its seeds. It’s going to die anyway, so the next generation gets its accumulated wealth. A perennial plant needs to hold back some carbon and nitrogen for winter survival and spring regrowth. The more resources it puts into this year’s seed production, the less it can carry forward to support reproduction next year.

This week’s paper shows that iteroparous plants face additional costs when they reproduce, namely, ecological costs. “Herbivore-mediated ecological costs of reproduction shape the life history of an iteroparous plant? was written by Tom Miller and colleagues at the University of Nebraska (where I’ll be speaking on Darwinian Agriculture in April) and published in American Naturalist.

Continue reading "Natural enemies complicate reproductive tradeoffs" »

January 21, 2008

Sustainable Darwinian Agriculture and Organic Tomatoes

I will be reviewing another recent journal article today or tomorrow, but meanwhile we seem to have convinced someone that an evolutionary perspective is useful in agriculture. A recent book review mentions a chapter we wrote:

There is also food for thought in some of the chapters, particularly the one by R.F. Denison and E.T. Kiers on sustainable crop nutrition. This perceptive analysis raises questions about the simplistic assumptions that often underlie attempts to improve crop mineral-use efficiency and highlights areas where such attempts are likely to be useful and others where they are not. This reviewer certainly changed his thinking as a result of the ideas put forward.
I doubt that the reviewer, Roger Leigh, remembers a mostly positive review I wrote of a book on long-term field experiments (mostly agricultural) that he edited over ten years ago, when I was directing UC Davis's Long-Term Research on Agricultural Systems (LTRAS) "100-year experiment." Our chapter discussed the implications of "our crops' legacy of preagricultural evolution", a topic we previously addressed in Darwinian Agriculture. For example, past natural selection for individual competitiveness may have favored more investment in roots than is optimal for maximum grain yield. On the other hand, human goals like reducing nitrate loss to groundwater (an environmental problem ignored by natural selection) might call for deeper rooting than would be needed for yield alone. We also discussed evolutionary conflicts in nutritional symbioses (e.g., with nitrogen-fixing rhizobium bacteria or the mycorrhizal fungi that provide many plants with phosphorus), the topic of our current research -- watch for our review in Annual Review of Ecology and Evolution.

Our recent paper comparing organic vs. conventional tomatoes also has an evolutionary twist...

Continue reading "Sustainable Darwinian Agriculture and Organic Tomatoes" »

October 16, 2007

Soybean symbiosis isn't what it used to be

Older soybean varieties benefit more from mixtures of good and bad symbiotic nitrogen-fixing bacteria than modern soybean varieties do. This work has also been
discussed on the Nature website by Heidi Ledford and on the Agricultural Biodiversity Weblog by Jeremy Cherfas.

"variations… profitable to the individuals of a species… will tend to the preservation of such individuals, and will generally be inherited by the offspring. I have called this principle… natural selection, in order to mark its relation to man's power of selection."
-- (Darwin, 1859)
Darwin was rightly impressed by what plant breeders have accomplished. I'm glad that potato breeders have reduced poisonous tomatine concentrations enough that we no longer need to eat absorbent clay with our potatoes, as was necessary with wild potatoes (Johns, 1990 p. 92). But sometimes selecting for a beneficial trait can have negative side effects. This problem applies both to natural selection and to selection by humans. Trade-offs among desirable traits can result from physical linkage between genes, intrinsic constraints (a given amount of sugar can be diluted in a larger strawberry), or random drift in traits not under selection.

This week, Toby Kiers, Mark Hutton, and I are reporting an apparent decrease, over the course of 60 years of soybean breeding, in the ability of plants to benefit from rhizobium bacteria. Our paper “Human selection and the relaxation of legume defences against ineffective rhizobia? is published on-line in Proceedings of the Royal Society.

Continue reading "Soybean symbiosis isn't what it used to be" »

July 28, 2007

Darwinian Agriculture III

Next week I will be meeting with a publisher to talk about the possibility of writing a book on Darwinian Agriculture to be published in 2009, the 150th anniversary of The Origin of Species. (I apologize to one reader who apparently thought it was a done deal.) Here's a short draft of the first chapter, mostly about sustainable agriculture by ants and termites.

Farmers of 50,000 millennia

“We’ve been farming sustainably for three years?, read the email. I was glad to learn that my friend was farming in ways that he hoped could continue indefinitely, but how could he be sure, after only three years?

It might have been a reasonable assumption, if the farming methods he used were similar to those that other farmers have used successfully for a long time. But how similar is similar enough? And what qualifies as “a long time?? As director of “the world’s youngest 100-year experiment?, I often thought about these questions....

Continue reading "Darwinian Agriculture III" »

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.

Continue reading "Rhizobia, pesticides, and peer review" »

June 30, 2007

Tracing the spread of agriculture with stone-age human DNA

This week's paper is "Palaeogenetic evidence supports a dual model of Neolithic spreading into Europe" by M.L. Sampietro and others, published online in Proceedings of the Royal Society. The paper is interesting both for its findings and for its methods.

We know that agriculture spread from the Near East -- do people in Asia call this the Near West? -- to western Europe, starting around 10,000 years ago. But did this mostly involve farmers moving, or the spread of agriculture without major movement of people?

People have tried to figure out past population movements using genetic differences among modern populations, but it would help to have genetic information from people who lived thousands of years ago, as well. This is technically challenging, however...

Continue reading "Tracing the spread of agriculture with stone-age human DNA" »

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.

Continue reading "Individual and kin selection in legume-rhizobium mutualism" »

April 17, 2007

Darwinian agriculture II

Last week, I was at a meeting in the Netherlands on "Darwinian agriculture: the evolutionary ecology of agricultural symbiosis." Topics included: the effects of cows on human evolution, the independent invention of "agriculture" by ants and termites, and some disadvantages of diversity. As promised, here are a few highlights.

Continue reading "Darwinian agriculture II" »

April 6, 2007

Darwinian agriculture I

Next week, I'm speaking at a one-day symposium on "Darwinian Agriculture: the evolutionary ecology of agricultural symbiosis", in Wageningen, The Netherlands. So, instead of reviewing a recent paper, this week I'm going to discuss some of the not-quite-so-recent papers on which my talk will be based. The following week, I plan to summarize some of the talks I hear at the meeting.

I may do the same thing in August, when my grad students and I speak at the much larger Ecological Society of America meetings in San Jose, California. Feel free to comment if you feel cheated of your weekly paper review, and I might reconsider. The Evolution meetings are in Christchurch, New Zealand, this year, but my grant won't stretch that far.

"Darwinian Agriculture: when can humans find solutions beyond the reach of natural selection?" was the title of a paper that Toby Kiers, Stuart West, and I published in 2003. Our answers to the title question suggested how increased understanding of past and ongoing evolution could improve: 1) breeding of crops and livestock, and 2) design of agricultural ecosystems.

Continue reading "Darwinian agriculture I" »

February 20, 2007

Evolutionary trade-offs: how are soybeans like salmon?

Answer: they're both semelparous (reproduce once, then die), so evolutionary trade-offs between number and size of offspring are expected to be similar.

This week's paper is "Evolutionary aspects of the trade-off between seed size and number in crops" (Field Crops Research 100:125-138) by Victor Sadras. You can read the abstract on the web for free. For the full version, you can pay $30 to download, visit your nearest agricultural research library (in the U.S., often at a state university), or email the author at: My discussion is mostly based on a shorter version presented at the Australian Agronomy Conference.

Demand for grain is increasing, to feed growing human and livestock populations and more recently for ethanol production. Unless those trends are reversed, we will either need to expand the land area used for agriculture or increase grain yields per unit area. Grain yield is the product of plants per area, seeds per plant, and weight per seed. Unfortunately, increasing any one of these (by increasing seeding rate, or through plant breeding) tends to decrease the others.

This paper looks at how natural selection (in the wild ancestors of crop plants and in fish) and plant breeding (especially in maize and sunflower) shape trade-offs between seed number per plant and seed size. The similar patterns in plants and fish show that, as predicted by the relevant aspects of evolutionary theory, we are dealing with fundamental constraints that we are unlikely to change.

Continue reading "Evolutionary trade-offs: how are soybeans like salmon?" »