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July 29, 2011

This week's picks

Failure to fix nitrogen by non-reproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates
This paper, by my former PhD student Ryoko Oono and Carolyn Anderson, formerly an undergrad in our lab and now a grad student at UC Davis, was published on-line months ago, so I've already discussed it.

Sib mating without inbreeding in the longhorn crazy ant
"Workers developed through normal sexual reproduction between queens and males. However, queens were produced clonally and, thus, were genetically identical to their mothers. In contrast, males never inherited maternal alleles and were genetically identical to their fathers. The outcome of this system is that genetic inbreeding is impossible because queen and male genomes remain completely separate." -- crazy indeed, but this is essentially how we make hybrid corn.

Sexual imprinting on ecologically divergent traits leads to sexual isolation in sticklebacks "imprinting is essential for sexual isolation between species; isolation was reduced when females were raised without fathers"

July 27, 2011

Would IEEE really sponsor a fake scientific conference?

The email was typical fake-scientific-conference-in-China spam: "we courteously invite you to deliver a Plenary Speech" as a "leading authority" in a field where I have no expertise. I've gotten several of these from "BIT Life Sciences."

This time, though, IEEE, a (formerly?) respectable engineering organization, was listed as a sponsor. I assumed the scam was using IEEE's name without permission, but the "6th International Conference on Bioinformatics and Biomedical Engineering " is actually listed on the IEEE web site. Apparently, IEEE has been involved in many fake conferences, which have, for example, accepted papers that are computer-generated garbage. Sad.

Not all conferences in China are fake -- I went to one a few years ago that was excellent, and am scheduled to speak at another -- and fake conferences are presumably held in other countries as well. China does seem to be afflicted with more than its share, though. Maybe it's harder to sue there, or something.

UPDATE -- someone left a comment with links to a blog suggesting that IEEE sponsors many fake conferences. Unfortunately, I had to delete the comment, because it linked to a blog attributing my concerns to "The University of Minnesota." The views presented here are my own, and not official positions of the university.

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 22, 2011

This week's picks

Cryptic female preference for genetically unrelated males is mediated by ovarian fluid in the guppy

Self-Recognition in Social Amoebae Is Mediated by Allelic Pairs of Tiger genes

Religion, fertility and genes: a dual inheritance model

Visual mimicry of host nestlings by cuckoos

Fitness costs of disrupting circadian rhythms in malaria parasites

Dinosaur Body Temperatures Determined from Isotopic (13C-18O) Ordering in Fossil Biominerals

July 15, 2011

Evolution of human cooperation

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

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

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

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

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

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.

Cotton plants have natural chemical defenses against insects, including gossypol. The researchers found that rs and rr mutants tend to absorb more of the gossypol they eat. As expected, gossypol slowed their growth, which would tend to reduce fitness.

The rs insects were more susceptible to gossypol than ss insects, so they would tend to stay rare in a high-gossypol refuge. They also looked at rr insects, although once these arose, the crop is doomed. Those with two copies of the same r gene were more susceptible to gossypol than ss insects were, but one strain with two different r genes was fairly resistant to gossypol.

Effects of gossypol on growth were fairly small -- about 5% for ss to 30% for rr. Would higher gossypol levels be better?

It's important to remember that the purpose of the refuge is to saturate the local mating market with ss insects. Higher gossypol levels would help keep rs mutants rare, but we don't want gossypol high enough to also reduce ss populations. For example, if we reduced ss populations in the refuge by 50%, we would need a refuge twice as large.

July 5, 2011

Another fake conference?

My latest invitation to speak at a fake "scientific conference" in China is for the "1st Annual Symposium of Antimicrobial Research."

This one is hosted by Xiaodan Mei, from BIT Life Sciences. I guess they still haven't been able to trick any well-known scientists into forming a puppet "organizing committee."

July 4, 2011

Carnival of evolution

Future evolutionary biologist William has an interesting summary of recent evolution blogs at Lessons of Evolution.

July 2, 2011

The "boy pill", assortative mating, and human evolution

There's a debate underway about whether we should oppose sex-selective abortion because it's abortion or because it's sex-selective. Matthew Yglesias argues for the latter. What if scientists developed a "boy pill" that would make a man produce only Y-chromosome sperm? He suggests that:

if we found out that use of the "boy" pill was extremely widespread, this might still legitimately worry us for three kinds of reasons. One is that widespread use of the boy pill would express the inegalitarian idea that men are more valuable than women. A second is that widespread use of the boy pill would reflect the existence of ongoing inequities in society that make it the case that a male child is more valuable than a female child. The third is that there are plausible reasons to believe that even a relatively small gender gap in the population could have problematic macro-scale consequences for society.
I'm not sure about his first and second points. Yes, the lower the status of women, the more likely parents might be to want a son rather than a daughter, even if they personally deplored discrimination against women. But would a male-biased sex ratio contribute to lower status for women, or perhaps alleviate it? If there were twice as many men as women, would women have more opportunities to choose partners who would support their aspirations?

A male-biased sex ratio could certainly cause "problematic macro-scale consequences for society", but would those consequences be all negative? Population growth can have negative macro-scale consequences, but every country except China has decided that those consequences are not negative enough to justify the "mutual coercion, mutually agreed upon" that Garrett Hardin thought necessary to limit population growth.

Making the hypothetical "boy pill" freely available would hardly qualify as coercion, but a male-biased sex ratio would tend to slow population growth. Could the net benefits of slower population growth (mostly positive) outweigh the net costs of a male-biased sex ratio (probably negative)?

Things get more interesting when we ask who it is that would prefer sons to daughters. In the US, men strongly prefer sons, by 49 to 22%, while women value sons and daughters equally. Conservatives prefer sons, 41 to 25%, while liberals value both equally. If this tendency applies worldwide, then widespread availability of the hypothetical "boy pill" would lead to male-biased sex ratios mainly in more-conservative countries and subcultures where men dominate decision making.

Would a shortage of females slow the population growth of conservatives? That's far from clear. If conservatism were highly heritable, either genetically or culturally, and if conservatives didn't marry outside of their subculture (i.e., if mating were highly assortative), then conservative societies with male-biased sex ratios would tend to grow more slowly. To the extent that conservatism (or a preference for sons) has a genetic basis, those genes would become less common than if the "boy pill" were not available.

Similarly, a "girl pill" could perhaps slow the population growth of any society with a strong preference for girls, assuming both assortative mating and lifelong monogamy.

Sex selection is just one example of the choices that parents may be able to make within the next few decades. Would it matter whether parental choices for the skin pigmentation of their offspring were motivated by their own prejudices, societal prejudices that they personally abhor, or the relative risks of skin cancer versus vitamin-D deficiency at their latitude?

July 1, 2011

This week's picks

How an Organism Dies Affects the Fitness of Its Neighbors

Gametogenesis Eliminates Age-Induced Cellular Damage and Resets Life Span in Yeast

The impact of seasonal and year-round transmission regimes on the evolution of influenza A virus

Adaptation to climate change: contrasting patterns of thermal-reaction-norm evolution in Pacific versus Atlantic silversides

Risk of collective failure provides an escape from the tragedy of the commons

The Luoping biota: exceptional preservation, and new evidence on the Triassic recovery from end-Permian mass extinction