New paper: Understanding mutualism with population genomics

Comparing metrics of diversity (x axis) and geographic differentiation (y axis) for thousands of genes in the Medicago truncatula genome (gray points) reveals that some symbiosis genes (red points) are genome-wide outliers — but they are not all the same kind of outlier (crosses and triangles). Yoder (2016), Figure 1.

Comparing metrics of diversity (x axis) and geographic differentiation (y axis) for thousands of genes in the Medicago truncatula genome (gray points) reveals that some symbiosis genes (red points, crosses, and triangles) are genome-wide outliers — but they are not all the same kind of outlier. Yoder (2016), Figure 1.

My very latest scientific publication is now online at the American Journal of Botany. It’s sort of an odd paper — something of a review, or an opinion piece, discussing how population genomic data can help us understand why mutualisms stay stable [PDF] in spite of the risk of “cheating” by partners, with a “worked example” with data from the Medicago HapMap Project. Here’s some key bits from the abstract:

Different hypothesized models of mutualism stability predict different forms of coevolutionary selection, and emerging high-throughput sequencing methods allow examination of the selective histories of mutualism genes and, thereby, the form of selection acting on those genes. … As an example of the possibilities offered by genomic data, I analyze genes with roles in the symbiosis of Medicago truncatula and nitrogen-fixing rhizobial bacteria, the first classic mutualism in which extensive genomic resources have been developed for both partners. Medicago truncatula symbiosis genes, as a group, differ from the rest of the genome, but they vary in the form of selection indicated by their diversity and differentiation — some show signs of selection expected from roles in sanctioning noncooperative symbionts, while others show evidence of balancing selection expected from coevolution with symbiont signaling factors.

The paper is my contribution to a Special Section on “The Ecology, Genetics, and Coevolution of Intimate Mutualisms”, which I co-edited with Jim Leebens-Mack. You can view the whole Special Section here, and download my paper here [PDF].

Chapter on coevolution in the Encyclopedia of Evolutionary Biology

Grant (1949).

My visualization of key data from Verne Grant’s 1949 paper showing that floral traits are more likely to be important in the taxonomic descriptions of plant species when those species are pollinated by animals — which suggests that those plant-pollinator interactions play a role in the formation of new species.

I got word this morning that the Encyclopedia of Evolutionary Biology, a huge compendium of current knowledge on evolution, systematics, and ecology, is now online. That’s exciting in and of itself, but it’s particularly so because it means you can finally see my contribution, the introduction to the topic of coevolution. Here’s the opening paragraph, of which I’m rather fond:

No organism is an island. Every living thing contends with predators, parasites, and competitors, and most also receive benefits from mutualists (Table 1). These interactions with other species exert natural selection—and predators, parasites, competitors, and mutualists may also experience selection in return. The mutual evolutionary change that results from this reciprocal selection is ‘coevolution’ (Janzen 1980; Thompson 2005).

The rest of the Encyclopedia includes contributions from a tremendous array of other authors, and I’m grateful to subject editor Andrew Forbes for the invitation to contribute. You can browse the whole thing on the publisher’s website, and download a manuscript-format PDF of the final text of my chapter here.

Coming soon: Crowd-funding a Joshua tree genome

Joshua trees at Tikaboo Valley, Nevada (Flickr: jby)

Joshua trees at Tikaboo Valley, Nevada (Flickr: jby)

I’m very excited to announce a new project, with a new model for doing science: The Joshua Tree Genome Project, in which I’m working with a bunch of smart, accomplished folks to sequence the genome of my favourite spiky desert plant. A sequenced Joshua tree genome will provide the framework to understand how coevolution with highly specialized pollinators has shaped the history of Joshua trees, and to use the landscape genomics skills I’ve developed with the Medicago HapMap Project and AdapTree to understand how the trees cope with extreme desert climates — and how to ensure they have a future in a climate-changed world.

Perhaps most excitingly (terrifyingly?) we’re going to raise some of the funds to do the genome sequencing by crowdfunding, using the platform. So please keep an eye on the project site, follow our Twitter feed, and Like our Facebook page to make sure you don’t miss your chance to help understand Joshua trees’ evolutionary past and ensure their future.

Nothing in Biology Makes Sense: Your dinner, or your life?

2010 076 Masai Mara b 24 Photo by ngari.norway.

Over at Nothing in Biology Makes Sense!, I’ve written about a new study that tries to disentangle conflicting sources of natural selection to determine whether big herbivores like antelope, zebras, and ostriches have evolved to run because they’re always running away from predators.

An antelope’s frame is under more demands than evading cheetahs—it also needs to travel long distances to follow food availability with the shifting rainy season. In fact, the North American fossil record suggests that big herbivores on that continent evolved long legs for distance running millions of years before there were predators able to chase after them. And then again, not all predators run their prey down; lions, for instance, prefer to pounce from ambush.

To find out whether gazelles are running for their lives, or running for dinner, go read the whole thing.◼

Nothing in Biology Makes Sense: The vital importance of genetic variation

Black Bean Aphid Aphis fabae. Photo by robbersdog.

Over at Nothing in Biology Makes Sense!, Devin Drown describes an interaction between aphids and a species of wasp who lay their eggs in the aphids so their larvae can eat the aphids alive. A new study tests whether the success of a wasp larva infecting an aphid depends on the specific genetics of the wasp, and of a bacterial symbiont the aphid carries:

The Vorburger group studies a crop pest aphid, Aphis fabae, and its common wasp parasitoid, Lysiphlebus fabarum. The adult parasitoids lay their eggs in unsuspecting aphid hosts. As the parasitoids develop they battle the hosts defenses. Some aphid hosts are also infected with a bacterium symbiont, Hamiltonella defensa, which can provide protection against the parasitoid by releasing bacteriophages that target the parasitoid invader (Vorburger et al 2009; Vorburger and Gouskov 2011). If the wasp parasitoid can evade all the host defenses then eventually it develops inside the still living aphid. Eventually, as the authors describe in grisly detail

“metamorphosis takes place within a cocoon spun inside the host’s dried remains, forming a ‘mummy’ from which the adult wasp emerges” (Rouchet and Vorburger 2012).

To learn how Vorburger et al. evaluated the importance of wasp genetics for successfully mummifying aphids, go read the whole thing.◼

Ecological complexity breeds evolutionary complication

Photo by futureatlas.

ResearchBlogging.orgCross-posted from Nothing in Biology Makes Sense!

It is a truth universally acknowledged in evolutionary biology, that one species interacting with another species, must be having some effect on that other species’ evolution.

Actually, that’s not really true. Biologists generally agree that predators, prey, parasites, and competitors can exert natural selection on the other species they encounter, but we’re still not sure how much those interactions matter over millions of years of evolutionary history.

On the one hand, groups of species that are engaged in tight coevolutionary relationships are also very diverse, which could mean that coevolution causes diversity. But it could be that the other way around: diversity could create coevolutionary specificity, if larger groups of closely-related species are forced into narower interactions to avoid competing with each other.

Part of the problem is that it’s hard to study a species evolving over time without interacting with any other species—how can we identify the effect of coevolution if we can’t see what happens in its absence? If only we could force some critters to evolve with and without other critters, and compare the results after many generations …

Oh, wait. That is totally possible. And the results have just been published.

A team of evolutionary microbiologists has performed exactly the experiment I outlined above. The study’s lead author is Diane Lawrence, a Ph.D. student in the lab of Timothy Barraclough, who is listed as senior author.

For the experiment, the team isolated five bacterial species, of very different lineages, from pools of water at the bases of beech trees—ephemeral pockets of habitat for all sorts of microbes that break down woody debris, dead leaves, and other detritus. They cultured the bacteria on tea made from beech leaves, in vials containing either a single species, or all five species, and let them evolve for eight weeks—several dozens of bacterial generations. In a particularly clever twist on standard experimental evolution methods, they also used nuclear magnetic resonance (NMR) to identify the carbon compounds in sterilized tea that had been “used up” by the bacterial cultures, and compared the compounds in fresh beech tea to determine what the bacteria were eating.

The base of a beech tree. Photo by -nanio-.

And, maybe not surprisingly, the bacterial species’ evolution with company turned out to be quite a bit from their evolution alone. Left alone, most of the species evolved a faster growth rate. This is a common result in experimental evolution, because the process of transferring evolving bacteria to fresh growth medium—”serial transfers” that were performed fifteen times over the course of the experimetn—can create natural selection that favors fast-growing mutants. But, grown all together in the same tube, species that had evolved faster growth rates in the solo experiment evolved slower growth instead.

To find out what had evolved in the multi-species tubes, the team tested the growth of the bacterial species on beech tea that had been used to grow one of the other species, then sterilized. The original, ancestral strains of bacteria generally had negative effects on each others’ growth—they lived on similar compounds in the beech tea, and so their used tea wasn’t very nourishing for the other species. The same thing occurred with the strains that had evolved alone, only stronger, which makes sense in light of the increased growth rates, which would’ve depleted the growth medium faster.

But the interactions among the strains of the different bacterial species that had evolved together was strikingly different. Many of them actually made the tea more nutritious for other species in the evolved community. That is, some of the bacteria had evolved the capacity to eat the waste products of another species that was evolving with them. Using the NMR method to track changes in the presence of different carbon compounds in the tea before and after use provided confirmation that the co-evolved species were using, and producing, complementary sets of resources.

In short, the evolving community didn’t simply become more diverse—it evolved new kinds of mutually beneficial relationships between species that began as competitors.

Beech leaves—yum? Photo by Colin-47.

That evolutionary shift toward mutual benefit had a significant impact on the bacterial community as a whole, too. Lawrence et al. assembled new communities of bacteria extracted from the end-point of the group evolution experiment, and compared their carbon dioxide production, a proxy for overall metabolic activity, to that of a community assembled from bacteria extracted from the end point of the solo-evolution experiments. The community of co-evolved bacteria produced significantly more carbon dioxide, suggesting they were collectively able to make more use out of the growth medium.

So that’s a pretty nifty set of results, I have to say. But I’m also left wondering what it tells us more generally. In both Lawrence et al.‘s paper, and in accompanying commentary by Martin Tucotte, Michael Corrin, and Marc Johnson, there’s a fair bit of emphasis on the unpredictability of the result. Lawrence et al. write, in their Discussion section,

The way in which species adapted to new conditions in the laboratory when in monoculture—the setting assumed for many evolutionary theories and experiments—provided little information on the outcome of evolution in the diverse community.

And, as Corrin et al. note,

These results imply that predictions constructed from single-species experiments might be of limited use given that most species interact with many others in nature.

So … evolution went differently under different conditions? That isn’t exactly a shocking revelation. The fact that this is one of the study’s major conclusions is a symptom of how little experimental work has actually tested the effects of multiple species on evolution. One experiment I’ve discussed here previously, focused on the joint effects of predators and competitors on microbes that live in pitcher plant pitfalls, similarly emphasized the fact that it wasn’t possible to predict the evolutionary effects of predators and competitors together based solely on their individual effects. Work in this line of inquiry is hanging at the point of establishing that complex conditions lead to complex results.

What I’d really like to know—and I think all the authors of both the paper and the commentary would agree with me on this—is how we can begin to make general predictions about community evolution beyond, “it depends what we put in at the start.” It may be that we’ll need a lot more studies like this current one before we can start to identify common processes, and more interesting trends.◼


Turcotte, M., Corrin, M., & Johnson, M. (2012). Adaptive evolution in ecological communities. PLoS Biology, 10 (5) DOI: 10.1371/journal.pbio.1001332

Lawrence, D., Fiegna, F., Behrends, V., Bundy, J., Phillimore, A., Bell, T., & Barraclough, T. (2012). Species interactions alter evolutionary responses to a novel environment. PLoS Biology, 10 (5) DOI: 10.1371/journal.pbio.1001330

Notes from the field: What’s Chris doing to that Joshua tree?

Joshua tree, diverged. Photo by jby.

Cross-posted from Nothing in Biology Makes Sense!

ResearchBlogging.orgMy postdoctoral research is shaping up more and more to be hardcore bioinformatics; apart from some time spent trying to get a dozen species of peanut plants to grow in the greenhouse as part of a somewhat long-shot project I’m working on with an undergraduate research associate, I mostly spend my workday staring at my laptop, writing code. It’s work I enjoy, but it doesn’t often give me an excuse to interact directly with the study organism, much less get outdoors. So, when Chris Smith dropped the hint that he could use an extra pair of hands for fieldwork in the Nevada desert this spring, I didn’t need a lot of persuasion.

Chris is continuing a program of research he started back when he was a postdoc at the University of Idaho, and which I contributed to as part of my doctoral dissertation work. The central question of that research is, can interactions between two species help to create new biological diversity? And the specific species we’ve been looking at all these years are Joshua trees and the moths that pollinate them.

Joshua trees, the spiky icon of the Mojave desert, are exclusively pollinated by yucca moths, which lay their eggs in Joshua tree flowers, and whose larvae eat developing Joshua tree seeds. It’s a very simple, interdependent interaction—the trees only reproduce with the assistance of the moths, and the moths can’t raise larvae without Joshua tree flowers. So it’s particularly interesting that there are two species of these highly specialized moths, and they are found on Joshua trees that look … different. Some Joshua trees are tall and tree-ish, and some Joshua trees are shorter and bushy. Maybe more importantly for the moths, their flowers look different, too.

Joshua trees, diverged. Photo by jby.

Here’s a photo of two of those different-looking Joshua tree types, side by side in Tikaboo Valley, Nevada. Tikaboo Valley has the distinction of being the one spot where we’ve found both of the tree types, and both of the pollinator moth species, living side by side. That makes Tikaboo Valley the perfect (well, only) place to figure out whether there’s an evolutionary consequence to the divergence of Joshua tree and its association with two different pollinators. Do Joshua trees make more fruit, or fruit with more surviving seeds, when they’re pollinated their “native” moths?

So, over several years of work at Tikaboo Valley, we’ve been edging towards answering that question. We’ve found evidence that, given access to both tree types, the two moth species spend more time on their “native” tree type, and have more surviving offspring when they lay eggs in “native” flowers. But to determine whether plant-pollinator matching matters to Joshua trees, we’d really like to find out what happens when each moth species is forced to use each type of tree, and that’s what Chris has been working on for the last several field seasons.

Installing a Joshua tree chastity device. Photo by jby.

The method for the experiment, developed after some false starts, goes like this:

  • Find Joshua trees with flowers that haven’t opened yet—untouched by pollinating moths;
  • Make sure said flowers are far enough off the ground to be out of reach of the open-range cattle that graze all over Tikaboo Valley;
  • Catalog the tree, measuring how tall it grew before it started branching (a good indicator of which type of tree it is), and its total height, and take a nice photo of it with an ID number placed nearby, for handy future reference;
  • Seal up the not-yet-open bunch of flowers inside fine-mesh netting, to keep moths out—and also, as we’ll see below, to keep moths in;
  • Cover the netted flowers in chicken wire, to keep out all the desert critters that like to eat Joshua tree flowers, even if said flowers are served with a side of netting;
  • While the flowers get closer to opening, go collect some yucca moths, which you do by cutting down clusters of open Joshua tree flowers, dumping them into a bag or a cloth butterfly net, and sorting through the flowers looking for fleeing moths, which can be guided into plastic sample vials—these moths don’t usually like to fly; and finally
  • Open caged flowers, and insert moths.

By introducing moths of each species into flowers on each variety of Joshua tree, we’ll be able to see whether trees with the “wrong” moth species are less likely to make fruit than trees with the “right” moth species; and directly verify that moths introduced into the “wrong” tree type have fewer surviving larvae than moths introduced into the “right” tree type.

Camp Tikaboo, 2012 edition. Photo by jby.

But, being desert plants, Joshua trees aren’t prone to making much fruit even under ideal conditions. After a dry winter (like this last one), it can be hard to find any flowering trees at all. So to obtain a respectable sample size takes a lot of folks—this year, I was one of ten people on the field crew camped in the middle of the valley: a cluster of tents grouped around a rented recreational vehicle, which served as a kitchen/gathering area/lab.

Chris’s lab tech, Ramona Flatz, kept the whole show organized, dividing us into teams to scout for trees with flowers, teams to follow up on scouting reports and install experimental net/cage setups, and teams to go collect moths to put in the cages. This planning was, naturally, conducted in a tent containing a table with laminated maps of the valley, and this tent was called, naturally, the “war tent.”

In the “war tent,” making plans. Photo by jby.

What results we’ll get remain to be seen; this is the second year with a substantial number of experimental trees, and we won’t know whether all that work has borne fruit until Chris returns in a few weeks to see whether any of the experimental trees have, er, borne fruit. As far as I’m concerned, it was wonderful to return to an old familiar field site, in the middle of the desert, and spend a few days hiking around and harassing yucca moths instead of anwering e-mail. But if the experiment works, the results should be mighty interesting.

Below, I’ve embedded a slideshow of all the photos I took over a few days at Tikaboo Valley—including a special moth-themed production number coordinated by Ramona.◼


Godsoe, W., Yoder, J., Smith, C., & Pellmyr, O. (2008). Coevolution and divergence in the Joshua tree/yucca moth pollination mutualism The American Naturalist, 171 (6), 816-823 DOI: 10.1086/587757

Smith, C. I., C. S. Drummond, W. K. W. Godsoe, J. B. Yoder, & O. Pellmyr (2009). Host specificity and reproductive success of yucca moths (Tegeticula spp. Lepidoptera: Prodoxidae) mirror patterns of gene flow between host plant varieties of the Joshua tree (Yucca brevifolia: Agavaceae) Molecular Ecology, 18 (24), 5218-5229 DOI: 10.1111/j.1365-294X.2009.04428.x

Yoder, J., & Nuismer, S. (2010). When does coevolution promote diversification? The American Naturalist, 176 (6), 802-817 DOI: 10.1086/657048

Nothing in Biology Makes Sense: You are coevolving in another dimension …

Photo by Thomas Hawk.

This week at Nothing in Biology Makes Sense!, Devin Drown walks us through a cool new theoretical model that shows how hosts and prey species can evade parasites and predators in an ongoing coevolutionary struggle—if they each coevolve in multiple dimensions.

Instead of treating a coevolutionary interaction between two species as the interaction of only two traits, the authors investigate the nature of an interaction among a suite of traits in each species. It’s not hard to think of a host having a fortress of defenses against attack from a parasite with an arsenal loaded with many weapons.

Full disclosure: Scott Nuismer, one of the coauthors on the new model, has collaborated with me and with Devin. For more detail, go read the whole thing. ◼

In flour beetles, coevolution mixes things up

A red flour beetle. Photo via Wikimedia Commons.

Cross-posted from Nothing in Biology Makes Sense.

ResearchBlogging.orgWhen evolutionary biologists think about sex, we often think of parasites, too. That’s not because we’re paranoid about sexually transmitted infections—though I’d like to think that biologists are more rigorous users of safer sex practices than the general population. It’s because coevolution with parasites is thought to be a major evolutionary reason for sexual reproduction.

This is the Red Queen hypothesis, named for the character in Lewis Carroll’s Through the Looking Glass who declares that “it takes all the running you can do to keep in the same place.” Parasite populations are constantly evolving new ways to infest and infect their hosts, the thinking goes. This means that a host individual who mixes her genes with another member of her species is more likely to give birth to offspring that carry new combinations of anti-parasite genes.

But although sex is the, er, sexiest prediction of the Red Queen, it’s not the whole story. What matters to the Red Queen is mixing up genetic material—and there’s more to that than the act of making the beast with two genomes. For instance, in the course of meiosis, the process by which sex cells are formed, chromosomes carrying different alleles for the same genes can “cross over,” breaking up and re-assembling new combinations of those genes. Recombination like this can re-mix the genes of species that reproduce mostly without sex; and the Red Queen implies that coevolution should favor higher rates of recombination even in sexual species.

That’s the case for the red flour beetle, the subject of a study just released online by the open-access journal BMC Evolutionary Biology. In an coevolutionary experiment that pits this worldwide household pest against deadly parasites, the authors show that parasites prompt higher rates of recombination in the beetles, just as the Red Queen predicts.

The red flour beetle, Tribolium castanaeum, is named for its predilection for stored grain products. This food preference makes the tiny beetles particularly easy to raise in the lab, where they’ve been useful enough as a study organism to rate a genome project, which was completed in 2008.

Another red flour beetle. Photo via Icelandic Institute of Natural History.

Tribolium castanaeum reproduces strictly sexually. But, like any other biological trait or process, the beetle’s rate of recombination can vary, and evolve. And, as I’ve explained above, the Red Queen suggests that selection by parasites should favor higher rates of recombination. So the authors of the new study set experimental populations of the beetle to evolve either in parasite-free habitats, or under attack by Nosema whitei, a protozoan that infects and kills flour beetle larvae.

The team started experimental populations of beetles (fed on organic flour, natch) in each of the two treatments with eight different genetic lines, maintaining them at a constant population by collecting 500 beetles at the end of each generation to start the next generation. To make the coevolution treatment coevolutionary, the authors also transferred spores of the parasite produced in the previous generation to infect each new generation of beetles.

After 11 generations of coevolution, the authors sampled male beetles from four of the experimental populations in each treatment, and mated them with females from the same genetic line. By collecting the genotypes of the sampled males for a small number of strategically chosen genes, and comparing them to the genotypes of the males’ offspring, it was then possible to identify recombination events—offspring who had combinations of alleles at different genes that weren’t seen in their fathers.

And, indeed, the frequency of recombination—the proportion of offspring whose genetics showed signs of recombination events when compared to their fathers—was greater in the experimental lines that coevolved with Nosema whitei.

That’s a fairly remarkable result for a simple, relatively short selection experiment, and to my knowledge it’s the first of its kind to deal with recombination, as opposed to sex. There are a few study systems in which natural populations show signs of coping with parasites by having more sex, including C.J.’s favorite mollusks, and there is one good experimental example in which the worm Caenorhabditis elegans evolved to reproduce sexually when confronted with bacterial parasites. But this study marks a new bit of empirical support for the Red Queen: coevolution acting to boost the gene-mixing benefits of sex. ◼


Kerstes, N., Berenos, C., Schmid-Hempel, P., & Wegner, K. (2012). Antagonistic experimental coevolution with a parasite increases host recombination frequency BMC Evolutionary Biology, 12 (1) DOI: 10.1186/1471-2148-12-18

Morran, L., Schmidt, O., Gelarden, I., Parrish, R., & Lively, C. (2011). Running with the Red Queen: Host-parasite coevolution selects for biparental sex. Science, 333 (6039), 216-218 DOI: 10.1126/science.1206360

Nothing in Biology Makes Sense: Making sense of ubiquitous plant defenses

A giraffe, dodging thorns like a pro. Photo by Colin Beale, via Nothing in Biology Makes Sense.

We have a second post at the collaborative blog Nothing in Biology Makes Sense! this week, in which ecologist Colin Beale (guest posting from Safari Ecology) tackles the question of why so many African savannah plants grow thorns:

At one level the answer is obvious—there are an awful lot of animals that like to eat bushes and trees in the savanna. Any tree that wants to avoid this would probably be well advised to grow thorns or have some other type of defence mechanism to protect itself. But then again, perhaps the answer isn’t so obvious: all those animals that like to eat bushes seem to be eating the bushes perfectly happily despite the thorns. So why bother having thorns in the first place?

To find out why, and see more of Colin’s great photos, go read the whole thing. ◼