Open access next week
Just Royal Society publications, unfortunately, but now's your chance to get three papers I published with Toby Kiers over the years:
...or some of those other Royal Society papers you've been craving.
Just Royal Society publications, unfortunately, but now's your chance to get three papers I published with Toby Kiers over the years:
...or some of those other Royal Society papers you've been craving.
That's the title of a review article just published online by Science.
The US National Science Foundation, which is funding some of the authors and previously funded my research on evolution of symbiotic cooperation, is highlighting the article on their website.
Past and ongoing evolution have important implications for health, agriculture, and conservation of biodiversity, but communication among scientists applying evolutionary biology to different practical problems has been limited. That started to change in 2010, when a bunch of us (including most authors of today's paper) met on Heron Island, Australia, at the Applied Evolution Summit. Scott Carroll (UC Davis and Institute for Contemporary Evolution) had a lead role in both the meeting and the review article.
Evolutionary changes occur over generations, so crop pests and disease-causing pathogens with short generation times can evolve quickly, undermining our control measures. Species with longer generation times, including humans and some endangered species, evolve too slowly to keep pace with changes in their environments. For example, food preferences that evolved when meat and sugar were scarce may lead to unhealthy diet choices today.
Our paper discusses various ways to slow harmful evolution. Refuges not exposed to selection (e.g., by insecticides or fishing with nets) may slow evolution of insecticide-resistant pests or evolution of smaller fish. This approach partly depends on insect pests or fish from the refuges mating with individuals from outside. Refuges might be less effective for populations that reproduce asexually, such as bacteria or cancer cells.
To protect valued species that are evolving too slowly, we may be able to modify the environment to better match their inherited traits. Taxing unhealthy food might help, assuming we're sure which foods are unhealthy. For wild species, moving them to environments to which they're better adapted may work. Obsession with native species may blind us to the fact that their native range is now warmer than it was when they evolved. Unless we can reverse climate change, saving those species may require moving them (or allowing them to migrate) further from the equator or to a higher elevation.
Despite the authors' shared interests in evolution and in practical problems, applying insights from one field to another can be difficult. But I hope that this review will be helpful, both to practitioners and to students of evolution that have not yet narrowed their career options.
Both talks are part of symposia with other interesting speakers.
August 18: Student Organic Seed Symposium, NY Finger Lakes Region
October 28: minisymposium (with Emma Marris, author of "Rambunctious Garden: Saving Nature in a Post-Wild World") on "Saving Nature and Improving Agriculture: Where does Nature's Wisdom Lie?" Washington State University, Pullman
Wow! I can't decide whether I'm more impressed by:
* the guy in the pickup truck who saw us carrying the cutout photo of young Darwin and asked "Is that [W.D.] Hamilton?"
* the evolution-themed parody of John Lennon's "Revolution", composed and performed by a dean who, like God, may have "an inordinate fondness for Beatles".
* the wildly popular herpetology petting zoo (I should have taken a photo), or
* the "Hall of Biodiversity" (a wide range of interesting materials from campus natural-history collections, showing butterfly mimicry, comparing mammoth with mastodon teeth, using C4 photosynthesis as an example of parallel evolution, etc.) set up in the student center next to the auditorium where I gave my talk on "Darwinian Agriculture: Evolutionary Tradeoffs as Opportunities" and the lobby area (shown) where they sold Darwin-Day tee shirts and served cake.
But the cake I made for Darwin's 200th birthday was better.
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.
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.
I don't think my talk at Ringberg Castle next week is open to the public, but these departmental seminars probably are:
Sept. 27, Kellogg Biological Station, Michigan
Oct. 4, St. Thomas University, Minnesota
Oct. 11, Oberlin College, Ohio
Oct. 30, Horticulture Department, University of Minnesota
Nov. 21, Iowa State University
Talk titles are mostly something like:
"Darwinian agriculture: evolutionary tradeoffs as opportunities"
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.
"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.
All five of my Darwinian Agriculture lectures at the International Rice Research Institute are now available on YouTube.
Here are some interesting papers published this week.
Multiple Instances of Ancient Balancing Selection Shared Between Humans and Chimpanzees " In addition to the major histocompatibility complex, we identified 125 regions in which the same haplotypes are segregating in the two species [neither version has displaced the other in either species in 6 million years], all but two of which are noncoding [i.e., they probably control other genes rather than coding for a protein]." The most likely explanation for such prolonged co-existence is that individuals with less-common alleles may be resistant to pathogens that have evolved to attack those with more-common alleles.
Accelerated gene evolution through replication-transcription conflicts" "We propose that bacteria, and potentially other organisms, promote faster evolution of specific genes through orientation-dependent encounters between DNA replication and transcription."
I'm off to the International Rice Research Institute to give a series of five lectures on Darwinian Agriculture. Here are some papers that look interesting this week.
Adaptive Evolution of Multiple Traits Through Multiple Mutations at a Single Gene
Hind Wings in Basal Birds and the Evolution of Leg Feathers
Lifespan of neurons is uncoupled from organismal lifespan
Naturally occurring allele diversity allows potato cultivation in northern latitudes"
Water-controlled wealth of nations
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.
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.
In case you missed the news coverage by Carl Zimmer in the New York Times, Jeff Akst in The Scientist, and Ed Yong on Nature's news site, among others, our paper on experimental evolution of multicellularity has just been published in Proceedings of the National Academy of Sciences. It's open access, so you can read all the details yourself.
In nature, multicellularity has only evolved
a few about 25 times, and it took billions of years. But Mike Travisano (a fellow faculty member in Ecology Evolution and Behavior) and postdoc Will Ratcliff (who earned a PhD with me recently) came up with a simple and repeatable way to speed the process enough to study under lab conditions: selection for rapid settling in liquid media, starting with unicellular yeast. They kindly invited Mark Borrello and me to participate in this exciting project, which also depended on hard work by undergrads Kristin Jacobsen, Mitch Hoverman, and Amanda Muehlbauer and funding from the National Science Foundation. We have also had some support for preliminary genetic analysis (in progress) from the College of Biological Sciences at the University of Minnesota.
The best collection of links related to this work is at the Microbial Population Biology (Micropop) website, which brings together people and projects from the laboratories of Mike Travisano, Tony Dean, and me. I particularly recommend the videos showing reproduction of snowflake-like multicellular yeast via smaller multicellular propagules -- think of plants reproducing from fragments, rather than seeds -- and genetic stability of the multicellular trait, shown by regrowth of multicellular clusters from enzymatically isolated single cells.
I gave some background for this work in an earlier post, when Elizabeth Pennisi wrote about it for Science.
Update: two scientists criticize some of our claims, and Will Ratcliff responds, on Carl Zimmer's blog, here.
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).
Keeping publication lists on web pages up to date is a task that often gets neglected. Now Google has made it easy. Search Google Scholar for "Ford Denison" and you should get this page, which took me about three minutes to set up. The list of publications is updated automatically, supposedly, and it also plots citations over years and provides links to abstracts and sometimes to PDFs.
If you're a published scientist, information on how to set up your own page is here.
Update: links to our open-access Proceedings of the National Academy of Sciences paper on experimental evolution of multicellularity, including PDF and great videos, can be found at the Microbial Population Biology (Micropop) website.
The Nov. 18 issue of Science has a news feature by Elizabeth Pennisi on recent research using experimental evolution, including some work on the evolution of multicellularity, led by Mike Travisano and Will Ratcliff, in which I've been involved.
Two interesting experimental evolution projects are underway in Canada. In Montreal, Graham Bell has been evolving algae that get their energy from a simple organic molecule, acetate, instead of from light. At first, the algae could barely survive without light, but after five years (still a fraction of the time that Richard Lenski has been evolving E. coli) he has hundreds of independent lines that have evolved a variety of ways to grow on acetate in the dark.
In Toronto, Aneil Agrawal is subjecting the sex life of rotifers to experimental evolution. Like aphids, Daphnia, and some other species, rotifers normally reproduce asexually, resorting to sex only under stress. Populations consisting of females, producing other females asexually, grow twice as fast as populations that are half male. (In my forthcoming book, Darwinian Agriculture, I discuss how reindeer herders increase production by harvesting mostly male calves for meat, so that most adults are females producing more calves, rather than males fighting over females.) But sexual reproduction shuffles genomes in ways that may be beneficial under different conditions. Agrawal and his postdoc Lutz Becks found that the balance between sexual and asexual reproduction evolved in response to environmental conditions. In stable environments, sex eventually disappeared. Once you've evolved the perfect genotype for some particular stable environment, why scramble that genotype through sex?
Unicellular life apparently had the earth to itself for over a billion years before even simple multicellular life evolved. So you might think that this major evolutionary transition requires some complicated series of genetic changes that would only happen rarely. Alternatively, maybe the first simple multicellular organisms weren't that different, genetically, from their unicellular ancestors -- they just couldn't out-compete their unicellular parents until conditions were right.
Individual cells would have greater access to nutrients in their environment than cells in the middle of a cluster, but what advantages might clusters have, under what conditions?
Major journals often ask scientists to limit interactions with the press before their work is published. I agree with this policy, which prevents the public disillusionment with science that can happen when a scientist makes claims (like cold fusion) that don't stand up to subsequent peer review. But presentations at scientific meetings (where the audience can critique exaggerated claims) are allowed. Members of the press can attend those meetings, report on what they hear, and ask other scientists for their reactions.
That's what happened this week, when Will Ratcliff (my recent PhD student, now doing a postdoc with Mike Travisano, Mark Borrello and me) talked about experimental evolution of multicellularity in yeast, at the Evolution meetings. His PhD was recent enough that he was eligible for and won the (William) Hamilton Prize for "Best Student Presentation." Our interactions with the press are constrained, for now, by the journal that's considering our paper on this work, but I look forward to blogging about it once it's published.
Meanwhile, see my earlier posts on Will's theoretical work on the evolution of aging, commentary on multiple roles for antibiotics in interactions among bacteria, and the discovery of a new form of bet-hedging in bacteria. This work was made possible by support from the US National Science Foundation.
I'm back at work. With Darwinian Agriculture book "in production" at Princeton University Press, maybe I'll have more time to blog, assuming no relapse into septicemia. I'm also looking forward to spending a little time in the lab; it seems like all I've been doing lately is writing and revising. It's been a productive year, though, with the publications below and more in the works. Thanks to the US National Science Foundation for funding the research upon which these publications were based.
Denison, R.F., E.T. Kiers. 2011. Life histories of symbiotic rhizobia and mycorrhizal fungi. Current Biology (in press).
Ratcliff,W.C., R.F. Denison. 2011. Alternative actions for antibiotics. Science 332:547-548.
Oono, R., C.G. Anderson, R.F. Denison. 2011. Failure to fix nitrogen (N2) by nonreproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates. Proceedings of the Royal Society B (on-line 1/2011).
Kiers, E.T., R.F. Denison, A. Kawakita, E.A. Herre. 2011. The biological reality of host sanctions and partner fidelity. Proc. National Academy of Sciences (on-line 1/2011).
Ratcliff, W.C., R.F. Denison. 2011. Bacterial persistence and bet hedging in Sinorhizobium meliloti. Communicative and Integrative Biology 4:1-3.
Denison, R.F. 2011. Past evolutionary tradeoffs represent opportunities for crop genetic improvement and increased human lifespan. Evolutionary Applications 4:216-214.
Hendry,A.P., M.T. Kinnison, M. Heino, T. Day, T.B. Smith, G. Fitt, C.T. Bergstrom, J. Oakeshott, P.S. Jørgensen, M.P. Zalucki, G. Gilchrist, S. Southerton, A. Sih, S. Strauss, R.F. Denison, S.P. Carroll. 2011. Evolutionary principles and their practical application. Evolutionary Applications 4:159-183.
Thrall,P.H., J.G. Oakeshott, G. Fitt, S. Southerton, J.J. Burdon, A. Sheppard, R.J. Russell, M. Zalucki, M. Heino, R.F. Denison. 2011. Evolution in agriculture: the application of evolutionary approaches to the management of biotic interactions in agro-ecosystems. Evolutionary Applications 4:200-215.
Science has kindly allowed us to link to a PDF of our recent Perspective, but only from one web page. So I've linked to it from last week's post.
"Do you expect me to talk?"Sometimes, there are more than two possibilities.
"No, Mr. Bond, I expect you to die!"
Many bacteria make antibiotics which, in high doses, kill other bacteria. But microbiologists have noticed that, at lower doses, antibiotics may change gene expression or alter behavior, without killing. So, they suggest, maybe antibiotics are mainly "tools of communication," rather than weapons.
Maybe, but those are not the only possibilities. Will Ratliff and I have just published a short Perspective in Science suggesting that two other possibilities are more likely. A PDF is freely available here, courtesy of the journal.
If communication (or "signaling") implies mutual benefit, what about nonlethal effects of antibiotics that benefit receiver or sender, but not both? For example, a bacterium that detects an antibiotic may hide in a biofilm to escape from the antibiotic, just as a zebra that smells lions hides in a herd to escape predators. If hiding in the biofilm benefits the bacterium that detected the antibiotic, but not the bacterium that made it, we would call the antibiotic a "cue."
Or, suppose a bacterium making antibiotics benefits by scaring competitors into dispersing (or hiding in biofilms)? This could benefit the producer, by reducing competition, but harm the receiver. We would call that "manipulation."
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.
This week's paper, Bacterial persistence and bet hedging in Sinorhizobium meliloti, was just published in Communicative and Integrative Biology. It's a brief but important follow-up to a paper in Current Biology, which I've already discussed.
Bacterial persisters are a serious medical problem. An infection that appears to have been cured by antibiotics sometimes "springs back to life." Evolutionary biologists have focused on cases where the renewed infection is caused by an antibiotic-resistant mutant, a classic example of evolution by human-imposed selection. Sometimes, however, the resurgent bacteria are still susceptible to the original antibiotic, yet bounce back after one or more treatments. What gives?
Many antibiotics only kill bacteria that are actively growing. So, if a few cells go dormant, these persisters may survive until the antibiotic breaks down, even if they aren't otherwise resistant.
Will Ratcliff recently reported that Sinorhizobium meliloti bacteria, best known as the nitrogen-fixing, root-nodule symbiont of alfalfa, can also make dormant cells. When S. meliloti cells divide, under starvation conditions, the elder daughter inherits most of the accumulated wealth (energy-rich polyhydroxybutyrate or PHB) and the younger daughter goes off to seek her fortune. You can see this unequal allocation of PHB in the Nile-red-stained image of a dividing cell, below right.
This apparent bet-hedging strategy is much more organized and more common than the random, one-in-a-thousand process that seems typical of human pathogens. A rhizobial population that starts with the usual normal distribution of PHB (above left) divides, initially, into one with roughly equal numbers of persisters and growers (above center).
Our original paper showed that about 70% of the high-PHB S. meliloti persisters are still alive after 528 days without food. So the well-known ability of rhizobia to survive in soil for months or years between legume hosts may not depend on their ability to out-compete other soil bacteria for limited food supplies.
But how relevant is this work with rhizobia, which benefit their legume hosts by providing them with nitrogen, to the antibiotic-resistant bacterial persisters that cause disease? In this new paper, Will Ratcliff showed that...
There must be some mistake here. Professor Smith, of PhD comics has out-performed me by a factor of 3 (papers in Science or Nature) to 17 (PhDs graduated), by every criterion except the H-index of citation impact, where I hold a slight lead, 23 to 19. In other words, 23 of my papers have been cited 23 or more times, so far. And my lead seems to be increasing.
I don't think my H-index is unusually high, so maybe Smith's is unusually low. Perhaps, if he treated his students better, they'd write better papers together?
Also, where's his Erdos number, the degrees-of-separation formula that inspired this XKCD cartoon? Mine is 5, via T.R. Sinclair, R.H. Rand, H.D. Block, and P.C. Rosenbloom. The first two links are via papers in nonmathematical journals, though. I'd be more interested in my W.D. Hamilton number, anyway. Incidentally, Hamilton's H-index is only 15, so maybe it's not such a reliable measure of scientific impact after all. Other approaches to citation analysis have been developed, including "eigenfactors."
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.
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.
In one of my first posts, I surveyed the scientific literature and found that there are thousands of scientific papers published on evolution every year, strong evidence against the long-running claims of evolution-denialists that scientists are rejecting evolution. But would it be rude to compare a single evolutionary biology lab's research productivity for one year to "intelligent design's" total for five years?
Denison lab: 4 papers published in 2010, all with original data.
They claim: 0 in 2010 (as of today), 2 in 2009, 0 in 2008, 0 in 2007, 2 in 2006...
... so 4 papers in 5 years (<1/yr), 0 with original data.
Their pathetic publication record confirms the criticism their list was intended to refute, namely, that intelligent design advocates don't publish much because they "don't have scientific data." Here's our list:
4) Ratcliff, W.C., R.F. Denison. 2010. Individual-level bet hedging in the bacterium Sinorhizobium meliloti. Current Biology 20:1740-1744.
Perhaps because the duration of starvation is often unpredictable, these bacteria "hedge their bets" by dividing into one starvation-resistant "persister" and one more-active "grower." See this blog post.
3) Oono,R., R.F. Denison. 2010. Comparing symbiotic efficiency between swollen versus nonswollen rhizobial bacteroids. Plant Physiol. 154:1541-1548.
Rhizobia provide nitrogen more efficiently (more N per CO2 respired) in hosts that make the nitrogen-fixing bacteroid form swell up and lose the ability to reproduce, relative to the same rhizobial strains in hosts where bacteroids aren't swollen. See this blog post.
2) Denison, R.F., J.M. Fedders, B.L. Harter. 2010. Individual fitness versus whole-crop photosynthesis: solar tracking tradeoffs in alfalfa. Evolutionary Applications 3:466-472. By disrupting solar tracking and measuring effects on photosynthesis, we showed that the overall effects of tracking on photosynthesis can be negative. So why do they do it? See this blog post.
1) Oono,R., I. Schmitt, J.I. Sprent, and R.F. Denison. 2010. Multiple evolutionary origins of legume traits leading to extreme rhizobial differentiation. New Phytologist 187:508-520. Legumes have evolved the ability to impose bacteroid swelling (shown above to increase nitrogen-fixation efficiency) repeatedly. See this blog post.
Our small lab should outperform all of "intelligent design" again in 2011, as the following have been already published or accepted:
Denison, R.F. 2011. Past evolutionary tradeoffs represent opportunities for crop genetic improvement and increased human lifespan. Evolutionary Applications (already on-line). See this post.
Kiers, E.T., R.F. Denison, A. Kawakita, E.A. Herre. 2011. The biological reality of host sanctions and partner fidelity. 2011. Proc. National Academy of Sciences (already on-line). Four of us, each studying a different mutualism, critique this paper, one of many that draws incorrect conclusions from modeling that ignores the tragedy-of-the-commons created by multiple symbionts per host, as I've discussed previously. Here's their response.
Oono, R., C.G. Anderson, R.F. Denison. 2011. Failure to fix nitrogen (N2) by nonreproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates. Proc. Roy. Soc. B (already on-line). Inside the root nodules of some legume species, rhizobial bacteroids (the differentiated form of these bacteria, which convert atmospheric nitrogen into a form the plant can use) have lost the ability to reproduce. If these plants just cut off resources to nonreproductive bacteroids that fixed too little nitrogen, that would have no direct effect on future generations of rhizobia. But Ryoko Oono and Carolyn Anderson showed that pea and alfalfa, two examples of such legumes, can reduce the reproduction of the bacteroids' still-reproductive clonemates in the same nodule, perhaps by cutting off resources to an entire nodule when it doesn't fix nitrogen.
Ratcliff,W.C., R.F. Denison. 2011. Bacterial persistence and bet hedging in Sinorhizobium meliloti. Communicative and Integrative Biology (abstract already on-line). This is a follow-up to Will Ratcliff's recent paper showing that starving rhizobial bacteria bet-hedge by splitting into one high-resource "persister" (which can survive long-term starvation) and one low-resource but more-active "grower." New data in this paper show that the persister cells are resistant to an antibiotic that kills growing cells, and that they have lower rates of protein synthesis, at least for the green-fluorescent protein.
Hendry, A.P., M.T. Kinnison, M. Heino, T. Day, T.B. Smith, G. Fitt, C.T. Bergstrom, J. Oakeshott, P.S. Jørgensen, M.P. Zalucki, G. Gilchrist, S. Southerton, A. Sih, S. Strauss, R.F.Denison, and S.P. Carroll. 2011. Evolutionary principles and their practical application. Evolutionary Applications (in press). What can evolutionary biology contribute to conservation biology, agriculture, and medicine? This synthesis paper from the Applied Evolution Summit, held on Heron Island in January finds some useful generalizations.
My research has been and is supported by the National Science Foundation, but the opinions expressed here are my own.
Princeton University Press sent the third review of the draft for my book, "Darwinian agriculture: where does Nature's wisdom lie?" and needed my responses to all three reviews, so that's kept me too busy to blog this week. Sorry about that. Two of three reviews were enthusiastic, so I'm guessing the book will actually be published.
Next week, I'll be in Paris, talking to plant breeders interested in "organic and low-input" farming. I'm going to talk about evolutionary tradeoffs and associated opportunities, including our ideas for improving symbiotic nitrogen fixation and Jacob Weiner's ideas for crops that cooperate to suppress weeds. Someone emailed me saying the meeting (EUCARPIA) had more people wanting to attend than they could accommodate.
Mike Travisano, Will Ratcliff, Mark Borrello, and I got an NSF grant for experimental evolution of multicellularity. We already have some cool results, which I'll write about as soon as our first paper is published.
Before the ink is even dry on our Current Biology paper on bet-hedging in rhizobia (actually, before it's even printed), Xue-Xian Zhang and Paul B Rainey have critiqued it in Genome Biology. They summarize Will Ratcliff's results, then ask "whether it is an evolutionary response to fluctuating selection shaped by natural selection." Experimental evolution, an approach Rainey and colleagues have used successfully, would be a good way to answer this question.
But is it really even bet-hedging? To qualify as bet-hedging, you need to sacrifice arithmetic-average fitness to gain greater geometric-average fitness. That would obviously depend on the environment, but it seems reasonable to assume that having half your progeny go dormant would sacrifice fitness when food is abundant, while increasing the chances of having at least one surviving progeny under starvation.
Zhang and Rainey seem to think there's an additional requirement to qualify as bet-hedging, namely, "switching rates to suit prevailing conditions." I disagree. Isn't a 50:50 mix of stocks and bonds (rather than 100% stocks, which have higher average return but are riskier) considered bet-hedging, even if you never change that ratio? But I do agree that it's important to know whether the ratio of dormant to growing cells changes in response to conditions, which I would call phenotypic plasticity. We are working on that.
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.
This week's paper is another recent one from my lab "Individual-level bet hedging in the bacterium Sinorhizobium meliloti", now on-line at Current Biology. Will Ratcliff did a guest post earlier, discussing a paper on the experimental evolution of bet hedging. This latest paper reports Will's own experiments.
S. meliloti is best known for its symbiosis with alfalfa. After infecting via root hairs, it reproduces inside developing root nodules.
Alfalfa nodules in our lab; copyright Inga Spence, used by permission.
When the nodules senesce, reproductive rhizobia escape into the soil, leaving the nonreproductive "workers" (bacteroids), which had been providing the plant with nitrogen, behind. A nodule may release millions of rhizobia -- we're not sure how many, actually -- each of which may have accumulated resources there, including high-energy PHB. So a single rhizobial cell that infects a root hair may end up with millions of well-endowed descendants, a few months later. But then what?
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?
Denison, R.F. 2010. Past evolutionary tradeoffs represent opportunities for crop genetic improvement and increased human lifespan. Evolutionary Applications (on-line).
Ratcliff, W.C., R.F. Denison. 2010. Individual-level bet hedging in the bacterium Sinorhizobium meliloti. Current Biology (on-line).
Oono,R., R.F. Denison. 2010. Comparing symbiotic efficiency between swollen versus nonswollen rhizobial bacteroids. Plant Physiol. (on-line).
Denison, R.F., J.M. Fedders, B.L. Harter. 2010. Individual fitness versus whole-crop photosynthesis: solar tracking tradeoffs in alfalfa. Evolutionary Applications 3:466-472.
Oono,R., I. Schmitt, J.I. Sprent, and R.F. Denison. 2010. Multiple evolutionary origins of legume traits leading to extreme rhizobial differentiation. New Phytologist 187:508-520.
I'm trying to get caught up after a week at Glacier National Park, but plan to blog about some of these. We will be submitting another couple of papers soon, but I doubt that they'll be out this year.
Princeton University Press is waiting for a third review of my book, "Darwinian agriculture: where does nature's wisdom lie?" Of the first two, one was enthusiastic and detailed, the other sketchy and negative.
Research in my lab is supported by National Science Foundation grants NSF/DEB-0918897 and NSF/IOS-0918986.
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.
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?
Amazon.uk 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.
Amazon.com doesn't have my book listed yet, but they are selling a crop physiology book with a chapter I wrote on Darwinian Agriculture.
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.
Our ancestors who delayed reproduction when environmental cues predicted famine were more likely to survive to reproduce after the big die-off. Delaying reproduction therefore increased relative representation in the smaller post-famine gene pool.
Biological responses inherited from those ancestors are still triggered by cues that predicted past famines, such as eating less or eating "famine foods." These responses can therefore extend lifespan, with a decrease in potential fertility as a side-effect. But most of us don't want to achieve our maximum possible family size anyway.
"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.
"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."
Ratcliff, Travisano, Hawthorne, and Denison. Can you spot the model?
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