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September 16, 2013

Meeting size matters

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I usually enjoy smaller meetings (20 to 40 people) more than larger ones (hundreds to thousands). Big meetings often schedule sessions on related topics at the same time, so the person who could point out a fatal flaw in the speaker's argument may be in another room. They usually allow only 2-3 minutes for questions, after which people may disappear into the crowd. At small meetings, in contrast, the whole group typically eats together, so there's plenty of time to pursue arguments.

That was certainly the case at last week's meeting on connections among evolutionary biology, anthropology, and economics. Peter Turchin has some discussion and pictures on his blog. With fewer people, small meetings can be held in more-interesting settings than the typical big-city convention center. Last week's meeting, for example, was held at Ringberg Castle, in the Bavarian Alps. Note that Peter's castle photo is almost identical to one I took, at right -- we must have been prowling the same battlement. In the dinner photo, the bald head at lower right is mine.

The Applied Evolution Summit was another great small meeting, held on an island in the Great Barrier Reef, bringing together people applying evolutionary biology to medicine, agriculture, and conservation.
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Location aside, grad students would really benefit from hearing the vigorous and usually constructive discussions at smaller meetings. Unfortunately, if everyone brought grad students, the meetings wouldn't be small anymore. Fortunately, there are lots of stimulating discussions at big meetings as well. It's just that they don't necessarily happen in the lecture halls. Poster presentations sometimes generate better discussions than oral talks, but it's also important to include grad students in meals where interesting arguments are likely.

April 5, 2013

Tradeoff-free longevity?

I have argued that understanding evolutionary tradeoffs is key to improving agriculture and increasing longevity.

For example, in 2009 I discussed a paper showing that food deprivation extends lifespan of C. elegans nematode worms by delaying their reproduction. I've seen other papers claiming to extend lifespan without reducing reproduction, but those papers have ignored possible effects on timing of reproduction. In a growing population, reproducing later reduces fitness, because your offspring are added to a larger gene pool. On the other hand, if the population is decreasing...

But a recent paper in PNAS reports that chemicals called ascorides (thought to be used as a crowding cue) increase the lifespan of C. elegans, without an apparent reproductive cost. Treated animals produced at least as many offspring as controls, at all ages. I don't understand this result. If there's no tradeoff, why haven't they evolved to turn on this response all the time, even without the crowding cue?

In humans, though, "Exceptional longevity is associated with decreased reproduction." That was the conclusion of a 2011 paper. They found that Ashkenazi Jewish centenarians (average age ~100 years) averaged 2.0 children, while a control group (parents of their children's spouses and friends, who died in their 70's) averaged 2.5 children. The centenarians also reproduced later in life (28-32 vs. 26-30). So, is it worth having 0.5 fewer children, to live 30 more years? Natural selection apparently doesn't think so.

February 1, 2013

Wrinkled fingers, spandrels, and an adaptationist approach to applied evolutionary biology

I was asked to talk to a local TV reporter about the winkled-finger study. Didn't happen, but it got me to read the paper and think about writing about it here. But Ryan Gregory has already done a much better job than I would have. He used this paper as an example of the widespread tendency to assume that, if some trait serves a useful function today, that must be why it evolved.

To test such hypotheses, he suggests that we (among other things):

"3) Explicitly address the necessary assumptions about ancestral traits, habitat, selective coefficients, and population size.

4) Use the comparative method within a phylogenetic context. Identify other species that have the trait and those that lack it. Has the trait evolved independently under similar conditions? Is it found in species that would not be expected to exhibit it if it evolves adaptively for a particular function?

5) Consider and rule out non-adaptive explanations (developmental constraints, pleiotropy, etc.) as much as possible."

This seems reasonable, if our goal is to figure out why some trait evolved. But, as an applied evolutionary biologist, I am less interested in why solar tracking evolved or how legumes first came to impose sanctions on rhizobial "cheaters" than in figuring out whether it would be possible and useful to enhance (or perhaps eliminate!) these traits in crops.

But many of Gregory's points still apply. Consider Ryoko Oono's recent work in my lab. We knew that some legume species make their symbiotic rhizobia swell up, as the rhizobia differentiate into nitrogen-fixing bacteroids. She found that a given strain of rhizobia fixes nitrogen more efficiently (more N, relative to its respiration cost) in a host where its bacteroids are swollen. She repeated this with another rhizobial species in another pair of hosts.

But can we generalize, from only one strain each of two rhizobial species? Is this enough evidence to justify trying to breed this trait into soybean? Probably not, but there's only one other reported example of a rhizobial species that swells in some hosts and not in others. Despite considerable effort, she couldn't get that strain to nodulate one of its reported hosts.

So Dr. Oono took a phylogenetic approach, analogous to that advocated by Gregory. Based on ancestral state reconstruction, she concluded that legume traits that make make bacteroids swell have evolved at least five times. These independent evolutionary transitions suggest that imposing bacteroid swelling (or doing something else that consistently has swelling as a side effect) might be broadly useful to legumes, at least under past conditions.

September 26, 2012

Diversity of Opinions on Diversity

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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.

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.

March 7, 2012

Is diet soda bad for us? An evolutionary perspective.

A recent paper reports that "Diet Soft Drink Consumption is Associated with an Increased Risk of Vascular Events in the Northern Manhattan Study." The correlation persisted even after they corrected for "age, sex, race/ethnicity, education, smoking, physical activity, alcohol consumption, BMI, daily calories, consumption of protein, carbohydrates, total fat, saturated fat, and sodium... and this persisted after controlling further for the metabolic syndrome, peripheral vascular disease, diabetes, cardiac disease, hypertension, and hypercholesterolemia."

Previous studies have found correlations between diet soft drink consumption and other health problems. What's going on? A specific artificial sweetener could have some specific negative effect. But could the sweet taste itself cause health problems? An evolutionary perspective suggests that it could.

Continue reading "Is diet soda bad for us? An evolutionary perspective." »

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 Berfrois.com, 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"

December 24, 2011

BRCA linked to reproduction-versus-longevity tradeoff

This is amazing. BRCA mutations have been linked to increased risk of breast cancer and ovarian cancer. Yet these mutations are not that rare. Hasn't natural selection been doing its job? Or is there some benefit that balances the risk?

The authors of "Effects of BRCA1 and BRCA2 mutations on female fertility," recently published in Proceedings of the Royal Society, hypothesized that women with a BRCA mutation might have more children, even if they don't live as long, on average.

Today, enough couples use birth control that the number of children born depends on preferences for family size, not just innate fertility. So the authors compared women (with and without the mutation) born before 1930. They used the Utah Population Database, which has data on births, deaths, and family relations for large numbers of Utah residents. Most of those women are no longer alive, however, so how can we know whether they had the BRCA mutation or not?

The authors used a variation on ancestral state reconstruction. When two women had the same BRCA mutation -- apparently there are various versions -- the authors assumed that their most-recent common ancestor had that mutation also. They also identified a number of controls -- women who presumably did not have a BRCA mutation, because none of their descendants did -- from the same time period.

So, was there any difference in fertility between women with versus without a BRCA mutation?

Continue reading "BRCA linked to reproduction-versus-longevity tradeoff" »

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.

LITERATURE CITED

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.


LITERATURE CITED

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.


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" »

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.
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January 21, 2011

Modeling reproduction/longevity tradeoffs and phenotypic plasticity in fluctuating environments

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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 28, 2010

How "mostly harmless" bacteria manipulate the immune system

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

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

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

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

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

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

October 19, 2010

Applied Evolution Summit video (Heron Island)

Many evolutionary biologists do field work in exciting locations, like the Galapagos. I mostly work in the lab these days -- when I'm not at the computer writing or revising papers -- but I often get invited to speak at meetings in interesting places. For example, I'll be talking about Darwinian agriculture in Paris in December, at the EUCARPIA meeting on plant breeding for organic farming.

But it's hard to beat Heron Island, Australia, where I spoke at the Applied Evolution Summit in January. The scientific output from our discussions will be coming out in Evolutionary Applications, but if you like sea turtles, birds, and coral reefs with your science...

Here's a beautiful video about the meeting.

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Casuarina, a tree that hosts nitrogen-fixing bacteria not closely related to those that form symbioses with legumes, frames a sea turtle laying eggs, on Heron Island. Photo by R. Ford Denison.

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.
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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 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 17, 2010

Directed evolution versus intelligent design of enzymes

"How have all those exquisite adaptations of one part of the organisation to another part, and to the conditions of life, and of one distinct organic being to another being, been perfected? We see these beautiful co-adaptations most plainly in the woodpecker and missletoe; and only a little less plainly in the humblest parasite which clings to the hairs of a quadruped or feathers of a bird; in the structure of the beetle which dives through the water; in the plumed seed which is wafted by the gentlest breeze; in short, we see beautiful adaptations everywhere and in every part of the organic world." -- Charles Darwin
Evolution denialists often claim that these adaptations must have come from an Intelligent Designer, who has apparently been too busy lately (protecting pedophile priests, maybe, or working to block gay marriage?) to come up with any new designs. They claim that natural selection (nonrandom proliferation of random variants) isn't up to the job.

But intelligent human designers are increasingly relying on processes similar to natural selection. The latest issue of Science discusses two examples of the use of selection-like processes for developing useful enzymes. One paper explicitly calls their approach "directed evolution." The other doesn't use the term, but what would you call generating billions of randomly varying designs in a computer and selecting those that meet certain criteria? Sounds like selection to me. In neither case did the researchers rely only on natural-selection-like processes. Instead, they used some combination of intelligent design and selection from among random variants. But nonrandom selection from among random variants was a key contributors in each case, solving problems beyond the reach of human reason or intuition.

November 5, 2009

Experimental evolution meets genomics

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

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

Continue reading "Experimental evolution meets genomics" »

July 6, 2009

Throwing the longevity switch

If you could choose a longer, healthier life, but only by having fewer kids, would you? What if you could eventually have the same number of kids, but only by having sex more often, and with no possibility of becoming a parent as a teen-ager?

Is this really possible? Based on the paper we published last week, we are pretty sure it is, although we don't yet know how much of an increase in lifespan is achievable, nor how much it will "cost" in reduced fertility.

A key assumption is that there are tradeoffs between longevity and reproduction, especially early reproduction. There is plenty of evidence for this antagonistic pleiotropy hypothesis: some gene variants that increase longevity nonetheless stay rare, because individuals with those variants have fewer kids. There are many possible reasons for this tradeoff. Calories used for reproduction aren't available for maintaining our bodies. Blood pressure and insulin levels optimal for reproduction are unlikely to be exactly optimal for longevity. Other risks associated with reproduction include sexually transmitted diseases and direct risks of childbirth. When there is a conflict between reproduction and longevity, natural selection will often favor reproduction.

There are, however, two ways we may be able to choose differently, increasing longevity at the expense of (potential, but maybe not actual) reproduction. First, once germ-line gene therapy is perfected and available (initially, perhaps, only in one or two "outlaw states"), maybe we could reverse some of the effects of past natural selection. We might be able to produce genetically engineered kids who would reach puberty later and with low enough intrinsic fertility that occasional unprotected sex would rarely lead to pregnancy, but who would still be healthy at age 100.

Second, what about people already born? Is there some biological "switch" we can throw, that tilts the longevity-vs.-reproduction tradeoff more towards longevity? Or has past natural selection welded the switch in the "reproduce now" position?

We think the switch is free to move, depending on environmental cues that affected our ancestors' survival and reproduction. Our paper shows that the switch position that maximizes Darwinian fitness depends on whether the overall population is increasing or decreasing. If population is decreasing, then individuals that live longer and reproduce later can contribute a larger fraction to their species' (shrunken) gene pool than those that reproduce earlier, on average, even if a few of them die before they get a chance to reproduce, and even if their lifetime reproduction is less than they might have achieved earlier.

Therefore, even though gene variants that always sacrifice early reproduction to increase longevity may not have persisted in the gene pool, variants that delay reproduction (thereby increasing longevity) only when populations were decreasing are likely to be with us, in each of our DNA molecules, today.

If this is true, all we need to do to increase our longevity is to give our bodies (false) cues that, over our evolutionary history, usually predicted population declines. To the extent that population declines were caused by food shortage, eating less may work, as it does in most species tested. Eating "famine foods" (leaves rather than meat, maybe) may also trigger physiological responses that reduce fertility but extend lifespan. On the other hand, if population declines were usually caused by cold winters, is there some reasonably comfortable way to trigger similar responses?

Delaying reproduction can only increase fitness if it increases the chances of surviving the famine or cold winter and reproducing later. So stresses that often predicted the death of the stressed individual (those associated with violent conflict, perhaps) won't necessarily delay reproduction or increase longevity. But there are lots of examples of mild stress increasing longevity. These stresses presumably trigger health-and-longevity-promoting mechanisms, but we may be the first to explain why such beneficial mechanisms aren't turned on all the time: they tend to reduce fertility.

Now, here's a question for you: would increasing human longevity be a good thing? I've seen this issue discussed in various places, but rather superficially. Assume that this option was made available to everyone, given that the cost could be quite low: inexpensive drugs or lifestyle changes that might even save money. Death rates would go down, in the short run, but so would birth rates, especially in countries where birth control is now rare. Death from old age is a fairly small component of overall population trends in these countries (relative to birth rate and infant mortality), so their rate of population increase might actually slow. But, if people expected to live longer, would they have more children (despite lower intrinsic fertility) or fewer, and at what age? Assuming some increase in population, we might need to grow more food -- a significant challenge -- but how would the overall impact of two healthy 90-year-olds who are still working (perhaps as doctors or nurses) and driving compare to that of one 90-year old who doesn't drive but needs expensive medical care? If professors keep working into their 90's, will that slow the spread of good new ideas, or only of stupid ideas that younger faculty may not know were debunked long ago? Would a longer-lived population produce too many bloggers?

June 25, 2009

The bitter fountain of youth

"When stress predicts a shrinking gene pool, trading early reproduction for longevity can increase fitness, even with lower fecundity." That's the title of a paper that Will Ratcliff, Mike Travisano, Peter Hawthorne and I just published in PloS-One. This was a spin-off from Ratcliff's work on the timing of reproduction in bacteria, but our main conclusions should apply broadly to plants and animals, with important implications for human health. Our entire paper is available on-line, but here is some additional background and explanation.

Earlier, I blogged about our research at UC Davis showing that tomatoes grown using organic methods have higher concentrations of a specific chemical (Mitchell, et al. 2007). Plants make this chemical to defend themselves against insects, which may be why there was more of it in tomatoes not protected by artificial pesticides. Surprisingly, this chemical actually seems to benefit human health. At the time, I thought this might just be coincidence, and wrote that "some of the natural insecticides plants make... are likely to be harmful to humans, rather than beneficial."

Now, I'm not so sure. It turns out that many toxins, including natural insecticides, can have health benefits in low doses, a phenomenon known as hormesis (Mattson & Cheng. 2006). Other forms of mild stress, such as dietary restriction (calorie restriction, intermittent fasting) or high temperature, have also been shown to increase longevity.

How can stress be beneficial? Some stresses trigger various protection mechanisms, such as antioxidants or heat-shock proteins, which may increase lifespan, even relative to individuals not exposed to stress. But why aren't these protective mechanisms turned on all the time, rather than only under stress? Don't individuals with longer lifespans leave more descendants than those with shorter lifespans? Not necessarily.

What if some mechanisms that increase lifespan also delay sexual maturity or decrease the rate of reproduction? For example, what if the blood pressure that maximizes lifespan is lower than that which maximizes reproduction? Then a gene for lower blood pressure would not necessarily increase in frequency over generations. A trade-off between early reproduction and longevity (and later reproduction) was central to the "antagonistic pleiotropy" hypothesis of Williams (1957). Our paper builds on this widely accepted hypothesis.

Given trade-offs between early and late reproduction, when will natural selection favor genes that potentially increase longevity but delay reproduction? Sometimes, resources not used for reproduction can be invested in growth, increasing reproduction in future years. Also, more experienced individuals may care for their offspring better. But what if delaying reproduction doesn't increase either the number of offspring or their survival?

We showed that delaying reproduction can still increase Darwinian fitness, that is, proportional representation in the gene pool, provided that overall population size is decreasing. Hamilton (1966) pointed out that an offspring added to a smaller population represents a larger fraction of the total gene pool. Therefore, if total population is increasing, offspring produced earlier have a larger effect on fitness. But if population size is decreasing, then offspring produced later have a larger effect on fitness. This means that delaying reproduction can sometimes increase fitness, even if delay does not increase the number of offspring.

Most populations will alternate between increasing and decreasing in numbers. If the population is stable or increasing, delaying reproduction can only decrease fitness. This is especially true if there is a high risk of death from causes unrelated to reproduction. But if the size of the gene pool is likely to decrease, delaying reproduction can increase fitness. This is especially true if risks directly or indirectly associated with reproduction are large relative to other risks.

Our mathematical models show that the best strategy is to delay reproduction only when an individual's chance of surviving to reproduce later is high, and only when an individual has reliable information predicting a decrease in overall population size. This is where stress comes in.

Past population declines were often caused by shortages of food, which can affect both the amount and types of food eaten. For example, natural insecticides in plants often have an unpleasant taste. Over most of our evolutionary history, therefore, these plants may have been eaten only when preferred foods, like meat or fruit, were not available. Consumption of these "famine foods" would therefore have been a reasonably good predictor of population decline, so they may trigger physiological changes (lower testosterone, etc.) that increase longevity while tending to delay reproduction.

A remarkable result, seen in both nematode worms and fruit flies, is that food odors can reverse the beneficial effects of dietary restriction on longevity (Libert, et al. 2007). If an individual smells food, others may be eating that food, so population size may be increasing. In that case, delaying reproduction would be a losing strategy, even if reproducing now increases the chance of an early death.

What about humans? Our models assumed that individuals reproduce only once, then die, like salmon or soybeans. However, we expect that some of our results will apply to species, like humans, with more complex life histories. One result for humans that is consistent with our hypothesis is that artificially sweetened soft drinks are just as likely to cause metabolic syndrome (related to diabetes) as sugared soft drinks are (Lutsey, et al. 2008). Like food odors, sweet foods may have been correlated, over much of our evolutionary history, with abundance, and therefore with impending increases in population size. If we want to live longer, maybe we should instead eat foods whose chemical composition or flavor remind our bodies of past famines. The health benefits we get from eating vegetables like kale may be due, in part, to the chemicals that give them their slightly bitter taste.

High levels of toxins, including natural ones, are still presumably harmful. But low doses of plant toxins, perhaps especially those found in traditional famine foods, may often improve health. This assumes that our hypothesis is correct, so you might want to wait for the results of experiments we are planning before making major changes in your diet.

We are also assuming that most people would consider some decrease in potential reproduction to be acceptable. For the many humans that already choose to limit their own reproduction, this need not result in any decrease in actual family size. For example, if people don't expect to marry until after college, the risks of early fertility may outweigh the benefits, even apart from health effects of hormone levels etc. in the teenage years on health later in life. Delaying puberty might, however, result in larger adults, with possible negative implications for automobile fuel economy and other resource issues.

Another popular hypothesis has been that individuals benefit from delaying reproduction in a bad year and waiting until conditions are better. This may increase the number of offspring produced, but we show that it does not increase proportional representation if the entire population also reproduces more in the good year.

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"How is putting our entire kingdom to sleep for 100 years better for my family than losing one daughter, however much we love her?" asked the queen. "In 100 years, our other children would have had countless grandchildren. Meanwhile, those in neighboring kingdoms will multiply. By the time the impenetrable thorn forest you put around our kingdom dies and we awake, our enemies will vastly outnumber us."

"Not necessarily", replied the fairy scientist, "My computer models predict 100 years of wars, famines, and plagues. It's true that your population won't grow, but those of your enemies will shrink. This would have been a winning strategy, even if there were another way to save your daughter's life."

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Ratcliff, Travisano, Hawthorne, and Denison. Can you spot the model?

LITERATURE CITED

Hamilton WD. 1966. The moulding of senescence by natural selection. Journal of Theoretical Biology. 12 : 12-45

Libert S, Zwiener J, Chu X, VanVoorhies W, Roman G, Pletcher SD. 2007. Regulation of Drosophila life span by olfaction and food-derived odors. Science. 315 : 1133-7

Lutsey PL, Steffen LM, Stevens J. 2008. Dietary intake and the development of the metabolic syndrome: The atherosclerosis risk in communities study. Circulation. 117 : 754-61

Mattson MP, Cheng A. 2006. Neurohormetic phytochemicals: Low-dose toxins that induce adaptive neuronal stress responses. Trends in Neurosciences. 29 : 632-9

Mitchell AE, Hong YJ, Koh E, Barrett DM, Bryant DC, et al. 2007. Ten-year comparison of the influence of organic and conventional crop management practices on the content of flavonoids in tomatoes. Journal of Agricultural and Food Chemistry. 55 : 6154-9

Williams GC. 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution. 11 : 398-411