Principle interviewee: Erica Bree Rosenblum

This post was chosen as an Editor's Selection for ResearchBlogging.orgSince her office is just down the hall from mine, I couldn’t very well write about Erica Bree Rosenblum’s latest scientific paper without talking to her about it in person. Rosenblum and her coauthor Luke Harmon weave together the stories of three lizard species’ evolutionary responses to the gypsum dunes of White Sands, New Mexico. As Rosenblum told me in our interview, the study both consummates work she began as a doctoral student and suggests new avenues of study at a striking and beautiful field site.

Erica Bree Rosenblum at White Sands, where she has studied lizards’ adaptation to the dramatic gypsum dunes since graduate school. Photo courtesy Erica Bree Rosenblum.

(I’ve edited the transcribed interview for clarity and length, and paraphrased the questions I asked in person to minimize my interruptions. Rosenblum previewed, corrected, and approved the text of her answers and my questions as they appear below.)

Jeremy B. Yoder: Tell me about the new study and its context.

Erica Bree Rosenblum: Some of the things that are compelling about White Sands that motivated us to write the “Same Same but Different” [$a] are that there are a number of different species that colonized this recent formation. … At first blush, this system looks all “same same.” You look at the main trait that has allowed these animals to survive there, which is becoming light in color, and many diurnal animals at White Sands are white, unless they have some other strategy for avoiding predation. … So a lot of my work over the last several years has been focused on the “same same” aspect of convergent evolution and on the one trait that appears to be the key trait for colonizing, which is light color.

The motivation of this paper was that there is an enormous “but different” side to the story, because there are three lizard species there, and they exhibit some really compelling differences in their degree of adaptation and their progress toward speciation. And also if you start looking at other traits besides color, if you take a multidimensional perspective on adaptation, then there are a lot of really striking differences across species.

JBY: Body size and limb length?

EBR: Body size and limb length and also the genetic basis of color and how structured the populations are across the ecotone. [The transition zone between white sand dunes and dark soil – JBY] So the motivation for this study was to look at what are the essential factors for ecological speciation and then what are the promoting factors for ecological speciation and how might the three species differ.

JBY: How did you start studying the White Sands lizards in the first place?

EBR: I was co-advised in graduate school by two eminent evolutionary biologists who have opposite perspectives on how you find study systems. My first year in graduate school, my one advisor, Craig Moritz, said to pick the theory you are interested in first and then find the system that will let you address that theory. My other advisor, David Wake, said to pick something that you love aesthetically, and then learn more about that. So I had these competing influences, in that sense, when I was trying to form my dissertation project.

Rosenblum and her collaborator Luke Harmon pursue Sceloporus magister, a close evolutionary relative of one species that has colonized White Sands. Photo courtesy Erica Bree Rosenblum.

I had just come back from a bunch of years abroad, and I knew I didn’t want to do research overseas. I also knew that I wanted to do my own thing and just “plug into” a system that had already been established. So I had an idea for wanting to do a study about ecotones—to study divergence with gene flow—in herps. [Lizards and snakes – JBY]

I had talked with different people and taken a map of the U.S. and circled every place that had really sharp transition zones that had to do with interesting problems in herpetology. So I had considered other field sites—in some of the lava flows in California that have strong transition zones, coastal-to-inland [transitions], these cool legless lizards in California—there’s a bunch of strong ecotonal transitions in western U.S. reptiles.

So I circled a bunch of places on the map and I was driving around catching animals and thinking about what I wanted to do. And when I got to White Sands, the Dave Wake part of me was drawn to it aesthetically. … It just seemed like such a striking example of adaptation with such clear possibilities. I knew I wanted to study something simple enough to wrap my head around, and White Sands has a striking, small, depauperate community, so you can actually study everything. And with a few exceptions, no one had done any biological research at White Sands since the forties, when the White Sands species were described.

JBY: What question would you like to have answered five years from now?

EBR: One of the big things I’d like to know is about the dimensionality of selection in the wild. We have a tendency to think about whatever trait seems most accessible to us, but when environments change, organisms are confronted with a lot of adaptive problems to solve at once.

… Number one is understanding the genetic architecture of adaptation and speciation. We know a lot about genotype to phenotype connections in natural populations, but we don’t know a lot about genotype-to-phenotype-to-speciation connections. I’m really interested in traits that might function as “magic traits,” that make speciation easier. I’m interested in whether [for White Sands lizards] color serves as a magic trait and can “high-tail” populations towards speciation.

The other thing I’m interested in is the genetic architecture of multidimensional adaptation. If you have lots of traits that are changing in a new environment, and it is happening very quickly over time, are the genes that underlie those adaptive traits all clustered in the genome? Is there a “signature” of multidimensional adaptation at the genetic level?

And then the third thing is about the predictability of evolution in general. I think it would be really fun to do a more systematic study of the entire fauna at White Sands and understand not just three lizard replicates but all the other species that are white, from invertebrates to mammals, to understand how predictable those adaptive changes are.

Different shades of Sceloporus undulatus, one of the three lizard species adapted to life at White Sands. Photo courtesy Simone Des Roches.

JBY: What about ten years from now?

EBR: The challenge of working at White Sands is that it’s a compelling empirical system to test some classic population genetics ideas, but it’s very hard to develop general conclusions from one system with three replicates. It’s nice to have the three lizard replicates, but it’s still only one system in one place. I’ve tried to visit all the other gypsum sand dune systems in the world. There are others—in Texas, in Mexico … they have unique faunas in other ways, but none of them seem to have blanched species. So when you study natural systems, finding compelling evolutionary replicates can be difficult.

JBY: And when we go looking for study systems we often find the ones with the strongest signals first.

EBR: That’s right … Another example where we’re running into a problem is that … in two of the three species the gene that controls color is the same gene, but has different dominance patterns [PDF]. In one species the mutation that leads to white color is recessive and in the other it’s dominant. And there’s a longstanding debate from Haldane, of how dominance should influence adaptation, but it’s just an N of two. So we could get any pattern. We’re doing follow-up studies to see if the predictions would be upheld in terms of how dominance affects the rate at which adaptive alleles are fixed, and visibility to selection. But whichever way the story goes, it’s either the way you expect it or the way you don’t expect it, but it’s just two replicates. So that is one challenge of studying things in nature.

JBY: Let’s conclude with an outrageous, blog-oriented question: Is White Sands the new Galapagos Islands?

EBR: Yes. [Laughs]

JBY: That’s what I hoped you’d say.

EBR: There are things that are compelling about white sands not only for learning about evolution but also for teaching about evolution. One of the new grants I have is for integrating research and outreach there, because it’s such a compelling place to say, “this is how adaptation happens.” You can see it with your eye, and it’s exactly what you expect. We just finished helping build a new evolution museum at the visitor center at white sands. … So I think that it has cool potential for helping public education around evolution, and it’s not as expensive to go there as it is to go to the Galapagos!


Rosenblum, E., Rompler, H., Schoneberg, T., & Hoekstra, H. (2009). Molecular and functional basis of phenotypic convergence in white lizards at White Sands. Proc. Nat. Acad. Sci. USA, 107 (5), 2113-7 DOI: 10.1073/pnas.0911042107

Rosenblum, E., & Harmon, L. (2010). “Same same but different”: Replicated ecological speciation at White Sands. Evolution DOI: 10.1111/j.1558-5646.2010.01190.x


Gardening ants grow their own treetop nests

This post was chosen as an Editor's Selection for ResearchBlogging.orgIf you were to combine ants’ dispersal of seeds and plant protection interactions, and maybe squint a little, you might see something like epiphitic ant gardens. Ant gardens form when tree-nesting ants collect the seeds of some epiphytes—plants evolved to grow in the branches of trees—and the collected seeds sprout. The nests provide congenial conditions for the plants, since gardening ants frequently use dung as a building material. The roots running through the nest help stabilize its structure and suck out moisture to control interior conditions.

Ants cultivate “gardens” of epiphytes like Anthurium gracile to provide nesting space. Photo by gjofili.

This adds up to a mutually beneficial relationship between ant and epiphyte [$a]. A number of tropical epiphytes grow almost exclusively in ant gardens, and the inclusion of plants in the structure of their nests apparently helps gardening ant species to establish nests wherever food is most abundant.

Association with ant gardens has evolved independently in a number of epiphytic species, from arums like Anthurium gracile (pictured to the right) to orchids and philodendrons. When distantly-related species begin to perform the same ecological role, they often evolve convergent traits that facilitate the common role. Almost all ant-dispersed plants attach fatty bodies called elaisomes to their seeds to reward the ants that pick them up. Almost all ant-protected plants grow domatia in which the ants can nest, and nectaries to reward them with sugary sap. But plants that grow in ant gardens don’t seem to have a common trait that prompts ants to collect their seeds. Can it be that every ant-garden plant species has a unique way to be an ant-garden plant?

That’s what studies of ant-garden plants, including a new one just published in PLoS ONE, suggest. Plants associated with ant-gardens don’t have elaisomes on their seeds. Many produce fleshy fruit, but ants will collect their seeds even if no shred of fruit flesh clings to them. In some cases, ants will even collect seeds from the dung of fruit-eating birds and mammals.

This leaves the possibility that ant-garden plants produce some ant-attracting chemical in their seeds. In the new paper, Elsa Youngsteadt and her coauthors set out to identify chemical compounds that might be the common attractant used by nine different ant-garden plants from seven different plant families. Youngsteadt et al. isolated seven different compounds found in the seeds of ant-garden plants but not in closely related species that do not grow in ant gardens. (The absence of the seven compounds from the non-ant-garden relatives is established, rather amusingly, with a blank data table.)

The authors then painted crude extractions of all soluble organic compounds from two ant-garden plants onto seeds from species that gardening ants do not cultivate, and found that the ants were indeed more likely to collect them. (As a control, the ants were also offered seeds coated in the pure solvents used to extract attractive compounds. They didn’t like those.) However, analysis of the extracts failed to find a compound or set of compounds present in all three species.

It’s possible that Youngstead et al. simply failed to isolate the compound or compounds that all three ant-garden plants use to prompt ants to collect their seeds. But it’s not that far-fetched to think that these distantly-related plants might each use different attractive compounds to interact with ants in the same way. Natural selection may often arrive at different solutions when shaping different species for the same ecological role. It might also be that ant-garden relationships were established not by plants evolving a way to prompt ants to pick up their seeds, but by ants evolving to recognize seeds of plants that work well in gardens.


Davidson, D. (1988). Ecological studies of neotropical ant gardens. Ecology, 69 (4), 1138-52 DOI: 10.2307/1941268

Youngsteadt, E., Guerra Bustios, P., & Schal, C. (2010). Divergent chemical cues elicit seed collecting by ants in an obligate multi-species mutualism in lowland Amazonia. PLoS ONE, 5 (12) DOI: 10.1371/journal.pone.0015822


Mutualist matchmaking made simple

This post was chosen as an Editor's Selection for ResearchBlogging.orgBack in September, I wrote about a new economic model of mutualism that proposed mutualists could keep their partner species from cheating—exploiting the benefits of a mutualistic relationship without returning the favor—without explicitly punishing them, so long as failure to play nice led to a reduction in mutualistic benefit [$a]. Now the same research group has published an elaboration of the economic approach to mutualism in the January issue of The American Naturalist, which suggests that mutualists can recruit better partners by manipulating the cost of entering into partnership [$a].

The bobtail squid, whose mutualism with luminescent bacteria is an example for the new model. Photo by megpi.

As a concrete example for their model, the authors refer to the mutualism between bobtail squid and a species of bioluminescent bacteria, which colonize the squid’s light organ and makes it glow. Short of some kind of complicated squid-bacterium signaling system, how does a squid ensure that its light organ is only colonized by bacterial strains that will pay it back and generate light?

They charge a cover.

More specifically, while the squid’s light organ supplies food for colonizing bacteria, it is also full of toxic reactive oxygen compounds. In order to take advantage of the food supply, a bacterium has to clear out these toxins—and conveniently, the bacterial enzyme that generates light consumes oxygen and removes the toxins in the course of the light reaction. So the only bacterial strains that colonize the squid’s light organ are those that can pay the cost of eating up the oxygen-based toxins and still make a “profit” on the food supply provided by the squid, generating light in the process.

The trick in setting up this screening is to find the right balance of cover charge and reward for prospective mutualists. The cover charge paid by high-quality partners has to be high enough that low-quality partners won’t accept it, and the reward offered for paying that high cost must be sufficiently good to make it worthwhile.

The authors suggest that this model should also apply not just to other mutualisms in which a host takes on microbial partners, such as plants’ partnerships with nitrogen-fixing bacteria, or animals’ interactions with the bacteria living in their guts—but also to interactions like obligate pollination mutualism or ants’ protection interactions with some plants.

Yuccas and ant-protected plants have to screen mutualists, too—and may impose their own cover charges. Photos by jby and Alistair Rae.

In the case of obligate pollination mutualism, like the one between yuccas and yucca moths, the cover charge is the effort involved in pollination—to guarantee a supply of yucca seeds for their larvae to eat, yucca moths must deliver plenty of pollen and do relatively little damage to the flower as they lay their eggs in it. There do exist yucca moth species who don’t pollinate, but lay their eggs on yucca flowers after they’ve been pollinated and are starting to develop into fruit. The new model would predict that the lower effort of this strategy is reflected in a lower payoff, maybe a lower rate of survival for the eggs of these “bogus” yucca moths.

In the case of ant-protected plants, the cover charge is the effort involved in defending a host plant from other ant colonies that would like to occupy it. As it happens, parts of an ant-plant that are better protected grow to provide better food and shelter for the ants occupying them, which gives a competitive advantage to a colony of effective defenders trying to fight off a colony of less-effective defenders.

Both of these scenarios, and similar ones in other interactions, suggest ways to test for self-screening mechanisms like the one described in this new model. The model suggests that active screening using signaling between interacting species should be rare in nature, and that a simple cost/benefit structure usually underlies the process of establishing associations between partners. I’ll be very interested to see whether new experimental or observational data further supports the self-screening hypothesis.


Archetti, M., Úbeda, F., Fudenberg, D., Green, J., Pierce, N., & Yu, D. (2011). Let the right one In: A microeconomic approach to partner choice in mutualisms. The American Naturalist, 177 (1), 75-85 DOI: 10.1086/657622

Weyl, E., Frederickson, M., Yu, D., & Pierce, N. (2010). Economic contract theory tests models of mutualism. Proc. Nat. Acad. Sci. USA, 107 (36), 15712-6 DOI: 10.1073/pnas.1005294107


Under the mistletoe, coevolution is about s and m

This post was chosen as an Editor's Selection for ResearchBlogging.orgPlants and plant products, from sprigs of holly to pine boughs, have been traditional winter holiday decorations since before Christmas became Christmas. Nowadays, if we don’t resort to plastic imitations, we deck our halls with garlands from a nursery and a tree from a farm. But seasonal decorations have natural histories apart from mantelpieces and door frames—ecological roles and, yes, coevolutionary interactions with other species.

Mistletoe. Photo by Ken-ichi.

One good example is mistletoe, whose white berries contrast nicely with holly’s red ones, and whose traditional association with kissing is probably responsible for more holiday party awkwardness than anything short of rum-spiked eggnog. Mistletoes are parasites, rooting in the branches of trees and shrubs to make a living at the expense of those hosts.

This sort of intimate interaction might be expected to result in coevolutionary natural selection between mistletoe and its hosts, potentially creating very specific pairings in which individual mistletoe species are only able to infect one or a few host plants with particular immune responses and defense chemistry. Yet mistletoe is dispersed by birds, which like to eat mistletoe berries, or can carry mistletoe seeds in their feathers—so seeds from a single plant might end up on a wide range of hosts. This means the specificity of mistletoe’s host associations is determined in a tug-of-war between selection from individual hosts and gene flow created by wide-ranging seed dispersal.

In population genetics models, we usually use s to represent selection, and m to represent gene flow, or migration. If s from an individual host species or the local climate is stronger than m, it creates local adaptation to those conditions. But even relatively small m from populations experiencing different conditions can wipe out that local adaptation. So in the case of mistletoe, does s win out, or does m?

One approach to answer this question would be to experimentally infect a range of host plants with a particular mistletoe, and compare their success. But with long-lived host plants, this method would be slow and expensive. Conveniently, local adaptation of mistletoe to individual host species should mean that mistletoe collected from different hosts is more genetically differentiated than mistletoe samples from the same host. And that’s quite a bit easier to test.

A 2002 study [PDF] of one North American mistletoe species found exactly this pattern. Coauthors Cheryl Jerome and Bruce Ford sampled dwarf mistletoe, Arceuthobium americanum from several host trees—Jack pine, ponderosa pine, Jeffrey pine, and two subspecies of lodgepole pine—growing across North America. They found that almost a third of the genetic variation they found in A. americanum was distributed among hosts—that is, it could differentiate dwarf mistletoes collected on one host from dwarf mistletoes collected from another.

A lodgepole pine branch supporting dwarf mistletoe in the Uinta Mountains, Utah. Photo by Fool-On-The-Hill.

Within these “host races,” geographic distance did have an isolating effect, but the effect was not as strong as that attributable to host differences. When Jerome and Ford examined the population genetics of the three principal A. americanum host trees—Jack pine and the two lodgepole pine subspecies—they found less differentiation than in mistletoe from the same populations [$a]. That suggests that, although coevolution with the trees strongly shapes mistletoe’s genetics, mistletoe infection is only one of many selective pressures acting on the host trees.

Although this approach is frequently used to test for coevolution, it isn’t entirely conclusive. The observed pattern of genetic differentiation in dwarf mistletoe on different host species could also arise if the A. americanum host races have climactic requirements that closely mirror the distribution of their respective hosts, or if birds carrying mistletoe seeds tend not to move the seeds between host species. Other indirect approaches exist to test these alternatives, but (so far as I can find) they haven’t been applied to dwarf mistletoe.


Jerome, C., & Ford, B. (2002). The discovery of three genetic races of the dwarf mistletoe Arceuthobium americanum (Viscaceae) provides insight into the evolution of parasitic angiosperms. Molecular Ecology, 11 (3), 387-405 DOI: 10.1046/j.0962-1083.2002.01463.x

Jerome, C., & Ford, B. (2002). Comparative population structure and genetic diversity of Arceuthobium americanum (Viscaceae) and its Pinus host species: insight into host-parasite evolution in parasitic angiosperms. Molecular Ecology, 11 (3), 407-20 DOI: 10.1046/j.0962-1083.2002.01462.x


Not all species interactions are (co)evolved equal

Biologists have long thought that coevolutionary interactions between species help to generate greater biological diversity. This idea goes all the way back to The Origin of Species, in which Darwin proposed that natural selection generated by competition for resources helped cause species to diverge over time:

Natural selection, also, leads to divergence of character; for more living beings can be supported on the same area the more they diverge in structure, habits, and constitution, of which we see proof by looking at the inhabitants of any small spot or at naturalised productions.
—Darwin (1859), page 128.

In the twentieth century, this idea was extended into suggestions that coevolution between plants and herbivores or flowers and pollinators helped to generate the tremendous diversity of flowering plants we see today. In general, biologists have found that strong coevolutionary interactions are indeed associated with greater diversity.

Yet although there is a well-established association between coevolution and evolutionary diversification, correlation isn’t causation. Furthermore, every species may coevolve with many others, and diversification that seems to be driven by one type of interaction might actually be better explained by another. It has even been suggested that coevolution rarely causes speciation at all.

Species interact in a lot of different ways, as antagonists, competitors, and mutualists. Do all these interactions shape diversity the same way? (Flickr: jby)

One step toward determining how often coevolution promotes diversification would be to identify what kinds of coevolutionary interaction are more likely to generate diversity. This is precisely the goal of a paper I’ve just published with Scott Nuismer in this month’s issue of The American Naturalist. In it, we present a single mathematical model that compares a wide range of species interactions to see how they shape diversification, and that model shows that coevolution doesn’t always promote diversity [PDF].

Continue reading


Between two host plants: The middle road doesn’t work for hybrid butterflies

This post was chosen as an Editor's Selection for ResearchBlogging.orgNew species form when separate populations of related organisms are no longer able to interbreed. Reproductive isolation can arise if two populations evolve different mating behaviors, or lifestyles so different that individuals from different populations don’t even encounter each other—but it need not mean that matings between the two populations never occur. In fact, speciation can arise in the face of quite a lot of interbreeding, so long as the hybrids produced by interbreeding are less fit than “purebred” individuals.

Edith’s checkerspot in Mount Diablo State Park, California. Photo by davidhoffman08.

This is what seems to be occurring in populations of Edith’s checkerspot, a small butterfly native to Western North America. Checkerspot populations in California use a wide variety of different host plants, and a recent study has shown that the offspring of parents from different host plants are maladapted in the wild.

In the Sierra Nevada mountains, logging has created a new kind of habitat for Edith’s checkerspot [PDF]—patches of cleared forest where the butterfly’s locally preferred host plant, Pedicularis semibarbata, is rare or nonexistent, but an alternative host plant, Collinsia torreyi, is plentiful. In the transition between clearings and less-disturbed forest, the two plants may often grow side by side.

A tale of two host plants: Pedicularis semibarbata and Collinsia torreyi. Photos by Wayfinder_73.

Examination of checkerspot populations that have access to only one of the two host plants suggests that each plant is best used in rather different ways. For instance, Pedicularis-using checkerspot females lay lots of eggs on a few plants, while Collinsia-using females lay a few eggs on each of a large number of plants. Once they hatch, larvae from Pedicularis populations feed on leaves closer to the ground than larvae from Collinsia populations, which makes sense since Pedicularis grows lower in general.

If these differences have a genetic basis, then hybrid checkerspots might exhibit intermediate behaviors, which might not work so well on either host plant. To test for this “hybrid inviability,” the new study’s authors crossed checkerspots from populations encountering only one host plant or the other, and then tested the hybrids’ performance in the field—and what they found confirms those predictions.

The Goldilocks principle—intermediate is better–doesn’t apply to hybrid checkerspots. Hybrid caterpillars foraged on leaves at an intermediate height on both host plants, and grew more slowly than purebred caterpillars. Hybrid females laid an intermediate number of eggs on both host plants, and laid them at an intermediate height. This left their offspring in a poor position for foraging after they hatched—and indeed, they grew more slowly than larvae hatched from eggs that were laid at the “traditional” heights on the host plants.

So it looks as though natural selection for better performance on Collinsia has led to the evolution of checkerspots that are at a disadvantage using Pedicularis (and vice versa). This even to the point that hybrids, which feed and oviposit in ways that are only somewhat different from the optimum, pay performance costs.

What’s interesting, though, is that this hasn’t led to greater genetic differentiation of checkerspot populations using different host plants; as assessed using randomly-selected genetic markers, there is an isolation-by-distance effect, but no effect of host plant use. (The authors cite a previous study using about 400 AFLP loci [PDF].) That suggests that only a few genes are responsible for the observed adaptive differences, and that natural hybridization between checkerspot populations using different hosts may be mixing together the rest of the genome.


McBride, C., & Singer, M. (2010). Field studies reveal strong postmating isolation between ecologically divergent butterfly populations. PLoS Biology, 8 (10) DOI: 10.1371/journal.pbio.1000529

Singer, M.C., & Wee, B. (2005). Spatial pattern in checkerspot butterfly-host plant association at local, metapopulation and regional scales. Annales Zoologici Fennici, 42, 347-61


What keeps mutualists honest—cake, or death?

This post was chosen as an Editor's Selection for ResearchBlogging.orgSomewhat like cooperation between members of the same species, mutually beneficial interactions between different species should be prone to fall apart when one species evolves a way to cheat the other. Biologists who study mutualism (myself included) have long believed that the solution to cheating is to punish cheaters—but a new model suggests that the benefits gained from playing nice might be enough to deter cheating [PDF].

I knew I had to write about this one when I saw that the authors use their model to propose a new explanation for the dynamics of my own favorite mutualism, between yuccas and yucca moths. (And, yes, it’s also an excuse to reference Eddie Izzard. I’m only human.)

Cake: definitely preferable to death. Photo by 3liz4.

The new analysis by Weyl et al. applies an economic modeling framework to species interactions in which one species provides some benefit to another, and then itself receives a benefit that at least partially derives from the help initially provided. To take one example the authors cite, many ant species colonize acacia plants, which grow structures in which the ants can nest (or domatia), and often produce nectar or other food rewards for the ants. The ant colony defends the plant from insect herbivores, with the consequence that the plant can devote more energy to growth, including new domatia and new leaves to fuel nectar production via photosynthesis.

In many such interactions, it’s been thought that each species can only keep the other from cheating—taking the benefits of the relationship without returning the favor—by actively punishing such behavior. Weyl et al. argue that instead of punishment, cheaters might be deterred if their refusal to play their role results in reduced payback from the other partner.

In the ant-acacia example, ant-tended plants kill off branches that lose a lot of leaves to herbivores, which can happen if the ants cheat by slacking off on their protection duties. But this isn’t punishment as such, say Weyl et al. Plants that aren’t protected by ants also kill off damaged branches, to conserve resources. Instead, because ant domatia tend to be located on the youngest, most herbivore-vulnerable shoots of ant-tended plants, lazy ants harm themselves by allowing herbivores to trigger a response that the plant would make whether or not it hosted ants.

An ant domatium on a “whistling thorn” acacia tree. Photo by Alistair Rae.

It sounds a bit passive-aggressive on the plant’s part, doesn’t it? But let’s look at the example that caught my attention: yuccas and yucca moths. Yucca moths are the sole pollinators of yuccas, and lay their eggs in pollinated yucca flowers; as a pollinated flower develops into a fruit, the eggs hatch, and the new-born larvae eat some of the seeds inside. Moths have good incentive to cheat on yuccas by laying lots of eggs in a single flower or not providing much pollen, but yuccas abort flowers that receive too many moth eggs, or not enough pollen [PDF]. Those of us who study yuccas have tended to interpret this as punishment, since killing off a pollinated flower also kills off any seeds a yucca might have produced via that flower.

However, as Weyl et al. note, yuccas abort flowers in response to damage to the floral ovules [PDF] (the tissue that will become seeds when pollinated), not to the presence of moth eggs per se. Moths generally damage the ovules a bit when laying eggs inside the flowers; but damage without eggs has the same effect. If floral abortion were punishment, say Weyl et al., it would occur as a result of moth eggs alone, not damage to the ovules in general.

In other words, the mutualists analyzed by this new paper are kept honest not by the threat of punishment (death) but the possibility that cheating will result in reduced rewards (less cake). It’s a clever inversion of perspective, and I’ll be very interested to see whether new empirical studies can back it up.


Marr, D., & Pellmyr, O. (2003). Effect of pollinator-inflicted ovule damage on floral abscission in the yucca-yucca moth mutualism: the role of mechanical and chemical factors. Oecologia, 136 (2), 236-43 DOI: 10.1007/s00442-003-1279-3

Pellmyr, O., & Huth, C. (1994). Evolutionary stability of mutualism between yuccas and yucca moths. Nature, 372 (6503), 257-60 DOI: 10.1038/372257a0

Weyl, E., Frederickson, M., Yu, D., & Pierce, N. (2010). Economic contract theory tests models of mutualism. Proc. Nat. Acad. Sci. USA, 107 (36), 15712-6 DOI: 10.1073/pnas.1005294107


New cooperation theory has major Mommy issues

This post was chosen as an Editor's Selection for ResearchBlogging.orgThe cover article for last week’s issue of Nature promised to be the last word in a long-running scientific argument over the evolution of cooperation—but it really just rejiggers the terms of the debate. Instead of solving the problem of how cooperative behavior can evolve, the new paper presents a model of maternal enslavement [$a]. These are not, it turns out, quite the same thing.

Group selection versus kin selection

Let’s start with some background. Unselfish, cooperative behavior has long been a puzzle in evolutionary biology, because natural selection should never favor individuals who make significant sacrifices for the benefit of others. Sure, an unselfish individual might expect those she helps to reciprocate later; but a population of the unselfish would be easily overrun by those who don’t reciprocate.

There have historically been two answers to the problem of the selfish out-competing the unselfish. The first case is basically an extension of logic we all learned in kindergarten: cooperative groups can do things that uncooperative groups can’t. Like, for instance, start a neighborhood garden.

Under this model, neighborhoods of cooperative, garden-making people are nicer places to live, and their inhabitants can collectively out-compete other neighborhoods that can’t get it together to start a community garden. In evolutionary terms, this is group selection—even if individuals sacrifice to build the garden, the group as a whole benefits. Unfortunately, this breaks down if the new garden attracts selfish people to move to the neighborhood, buy up all the cheap real estate, and open Urban Outfitters franchises.

There’s another possibility, though. What if unselfish behavior isn’t always truly unselfish? For instance, if you help your relatives, you’re actually helping some of your own genes. You share half your genes with your siblings, a quarter of your genes with half-siblings, an eighth of your genes with first cousins, and so on. This means that Michael Bluth might be on to something.

Evolutionarily speaking, it doesn’t matter if Michael spends all his time helping his feckless family, as long those efforts help someone in the family (G.O.B., most likely) reproduce and perpetuate some of the genes that Michael shares with him or her. This idea was advanced by W.D. Hamilton in two 1964 papers, one mathematical [PDF], and one more focused on real-world examples [PDF]; we now know it as kin selection. It doesn’t hold up so well for maintaining the kind of complex society humans have today, where we interact with lots of completely unrelated people—but it might have got the ball rolling toward the wheel, war, New York and so forth by selecting for cooperative behaviors within small tribes back at the dawn of history.

The group selection versus kin selection debate has gone back and forth for decades, and the new paper is a shot across the bow of kin selection. The authors, Martin Nowak, Corina Tarnita, and E.O. Wilson, aim to do two things: first, prove that kin selection is wrong; and second, describe an alternative explanation. For the first, they argue that kin selection only applies in narrow circumstances, that those circumstances never show up in nature, and that empirical studies just don’t support the model. Johnny Humphreys makes some reasonable objections to these arguments, and so do several folks interviewed by Carl Zimmer, and I’ll refer you there rather than try to improve on them.* I’m more interested in the second part: the alternative explanation.

Enslaved by Mom

No individual fitness for you—you’re cogs in the Superorganism. Photo by jby.

Nowak et al. propose to explain the evolution of unselfishness as it applies to eusociality—organisms like ants or bees or naked mole rats, in which colonies of (closely related) individuals defer most or all of their opportunities to reproduce, in order to support one or a few individuals that reproduce a lot. As Johnny points out in his critique, it’s not clear that eusociality is the same thing as unselfishness at all, even though it’s historically cited as an example of unselfishness [$a]. The new model that Nowak et al. develop actually makes the difference between eusociality and unselfishness even clearer. Under their model, it’s not that worker ants give up reproductive opportunities to help their mother, the Queen, reproduce—it’s that the Queen takes away their reproductive opportunities.

The key insight of the new model is that, in evolving from a non-social insect to a eusocial one, the natural selection that matters affects not the individuals evolving into workers, but the individual who would be Queen. Consider an insect similar to the probable ancestor of ants: females build nests, provision them with food, and lay eggs inside. Nowak et al. propose that a female who evolved the ability to lay “worker” eggs—females that grow up not to found their own nest, but to help in their mother’s—would have greater fitness than females without such helpful offspring.

Aside from the probability of evolving “worker” eggs (which is not a small issue, I think), this shift in perspective from the fitness of the worker to the fitness of the Queen makes all sorts of sense to me. I’ve often wondered why myrmecologists don’t treat ant colonies as single organisms, rather than collections of cooperating individuals.

But this approach also seems to sidestep the key question biologists hope to answer with kin selection and group selection models—these models aim to explain how individuals can come together to cooperate, but Nowak et al. have built a model that looks more like enslavement. I can’t learn anything about how unselfish behavior can spontaneously evolve in a population by looking at a population that has had unselfishness imposed upon it. To indulge in one last especially geeky pop culture reference, it’d be like trying to learn about market economics by studying The Borg.

Nowak, Tarnita, and Wilson might have come up with a very good model for the evolution of eusociality; but if so, it means that eusociality is a bad model for the evolution of cooperation as we usually conceive it.

* I will, however, note that Nowak et al. do something I’ve never seen in a scholarly paper before—in dismissing empirical studies of kin selection, they defer substantive discussion to the Supplementary Information. There are, in fact, 43 pages of SI for this 6-page paper, including two major mathematical models and the discussion of empirical kin selection studies. This is a problem, but one that is beyond the scope of this already-long post.


Axelrod, R., & Hamilton, W. (1981). The evolution of cooperation. Science, 211 (4489), 1390-1396 DOI: 10.1126/science.7466396

Hamilton, W.D. (1964). The genetical evolution of social behaviour. I. Journal of Theoretical Biology, 7 (1), 1-16 DOI: 10.1016/0022-5193(64)90038-4

Hamilton, W.D. (1964). The genetical evolution of social behaviour. II. Journal of Theoretical Biology, 7 (1), 17-52 DOI: 10.1016/0022-5193(64)90039-6

Nowak, M., Tarnita, C., & Wilson, E. (2010). The evolution of eusociality. Nature, 466 (7310), 1057-62 DOI: 10.1038/nature09205


Before they were yucca moths

This post was chosen as an Editor's Selection for ResearchBlogging.orgYuccas and yucca moths have one of the most peculiar pollination relationships known to science. The moths are the only pollinators of yuccas, carrying pollen from flower to flower in specialized mouthparts and actively tamping it into the tip of the pistil. Before she pollinates, though, each moth lays eggs in the flower—the developing yucca seeds will be the only thing her offspring eat. How does such a specialized, co-adapted interaction evolve in the first place? My coauthors and I attempted to answer this question in a paper just published in the Biological Journal of the Linnean Society, by reconstructing the ecology of yucca moths before they were yucca moths [PDF].

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The “Big Four,” part II: Mutation

This post is the second in a special series about four fundamental forces in evolution: natural selection, mutation, genetic drift, and migration.

This post was chosen as an Editor's Selection for ResearchBlogging.orgIn order for populations to change over time, to descend with modification, as Darwin originally put it, something has to create the modifications. That something is mutation.

A mutation of large effect? Photo by Cayusa.

A mutation is any change to an individual’s genetic code, whether caused by an external factor like radiation, or an error in the DNA copying that takes place every time an individual cell divides. However, not all mutations are created equal.

First and foremost, for a mutation to have any future existence beyond the individual in which it occurs, it must be in a cell that will go towards forming the next generation, a germline cell. In sexually reproducing species, this means sperm or egg cells, or the progenitor cells in the testes or ovaries that form them. Second, for a mutation to be “visible” to natural selection, it must have some effect on fitness, the number of offspring an individual carrying the mutation is likely to have. The genetic code determines how and when individual cells make proteins, and proteins determine phenotypes, the visible characteristics of living things. However, many changes to the genetic code don’t affect their carriers’ fitness. Mutations might be more or less neutral because

  • They occur in regions of the genome that don’t code for proteins or control protein production—so-called “junk” DNA.
  • They are synonymous substitutions, which occur in a protein-coding region of DNA, but don’t alter the protein produced.
  • They alter a protein, but not in a way that changes its function [PDF].
  • They alter a protein’s function and an individual’s phenotype, but in a way that doesn’t affect how many offspring that individual has.

Neutral mutations are actually quite important for biological studies—DNA fingerprinting and population genetics studies rely on them. Their frequencies evolve at random, reflecting the history of the populations that carry them rather than the effects of natural selection.

Favorable new mutations sweep the population

TOP: DNA sequences from a population are variable (blue) before a new mutation (red dot) arises; after it “sweeps,” every individual carries the allele as well as identical sequence nearby (red). BOTTOM: a figure from Linnen et al. (2009), demonstrates this pattern in deer mice. Images from Pritchard et al. (2010), fig. 3 and Linnen et al. (2009), fig. 4.

The variation introduced by neutral mutations—or, rather its absence—can help identify regions of the genome where selection is active. When a new gene arises by mutation, and it is strongly favored by selection, it can quickly spread through a population. In species that remix their genomes through sexual selection, the region of the genome containing a useful new gene can recombine into many different genetic backgrounds—but the closer a region of DNA is to the favored mutation, the less likely it is to recombine and separate from it. Thus, a region of the genome rather larger than the gene favored by selection is carried along until everyone in the population has the same DNA sequence.

When a new mutation takes over a population in this manner, it’s called a selective sweep, and the pattern it produces has been used to identify genes recently favored by selection in many different species, including humans. For instance, Linnen et al. documented reduced genetic variation in the neighborhood of gene variant responsible for light-colored fur in deer mice to demonstrate that it spread rapidly through the population after the mice colonized a region with light-colored sand.

Fuel for the engine of natural selection

Selective sweeps highlight how natural selection acts in opposition to mutation: mutation introduces new variation into populations, and natural selection causes the most fit variants to spread—potentially until the whole population carries the same trait. At the same time, selection requires variation in order to operate. If everyone is identical, then everyone has the same expected number of offspring, and the next generation will look just like the current one.

Because of this, natural selection can only operate as rapidly as mutation can introduce new variation from which to select. We know of specific cases in which selection seems to have “stalled” for lack of heritable variation. For instance, the fly Drosophila birchii lives in rainforest habitats along the northeast coast of Australia. Fly populations from the driest locations in this range have greater tolerance for dry conditions, but they also have virtually no heritable variation for drought tolerance [PDF]—and the authors suggest that this could limit the flies’ ability to evolve in response to climate change.

In other cases, though, biologists have found that mutation seems to provide new variation at least as fast as selection can remove it, leading to sustained, long-term evolution of experimental populations [PDF]. One important factor that may determine the outcome of this mutation-selection balancing act is actually the size of the population—more individuals means more opportunities for mutations to occur.

So the rate at which new mutations accumulate in a population depends on many factors, not the least of which are how you choose to measure that rate, and the fitness effects of the counted mutations. (Does a mutation “count” as soon as it occurs in a cell’s nucleus, or only when it has passed on to the next generation, or only when it has spread to everyone in a population?) Ultimately, populations evolve through a constant tension between the effects of mutation, natural selection, and the subject of next week’s Big Four force: genetic drift.


Barton, N., & Keightley, P. (2002). Understanding quantitative genetic variation. Nature Reviews Genetics, 3 (1), 11-21 DOI: 10.1038/nrg700

Drake J.W., Charlesworth B., Charlesworth D., & Crow J.F. (1998). Rates of spontaneous mutation. Genetics, 148 (4), 1667-86 PMID: 9560386

García-Dorado, A., Ávila, V., Sánchez-Molano, E., Manrique, A., & López-Fanjul, C. (2007). The build up of mutation-selection-drift balance in laboratory Drosophila populations. Evolution, 61 (3), 653-65 DOI: 10.1111/j.1558-5646.2007.00052.x

Hoffmann, A., Hallas R.J., Dean J.A., & Schiffer M. (2003). Low potential for climatic stress adaptation in a rainforest Drosophila species. Science, 301 (5629), 100-2 DOI: 10.1126/science.1084296

Keightly, PD. (2003). Mutational variation and long-term selection response. Pages 227-48 in Plant Breeding Reviews, Volume 24, part I. J. Janick, ed. John Wiley & Sons. Google Books.

Linnen, C., Kingsley, E., Jensen, J., & Hoekstra, H. (2009). On the origin and spread of an adaptive allele in deer mice. Science, 325 (5944), 1095-8 DOI: 10.1126/science.1175826

Pritchard, J., Pickrell, J., & Coop, G. (2010). The genetics of human adaptation: Hard sweeps, soft sweeps, and polygenic adaptation. Current Biology, 20 (4) DOI: 10.1016/j.cub.2009.11.055

Tokuriki, N., & Tawfik, D. (2009). Protein dynamism and evolvability. Science, 324 (5924), 203-7 DOI: 10.1126/science.1169375