Category Archives: coevolution

Not all species interactions are (co)evolved equal

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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].

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In the depths of a pitcher plant, competitors and predators cancel each other out

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ResearchBlogging.orgSpecies interactions are probably pretty important, in the evolution of life. There are all sorts of studies showing that the fitness and evolutionary history of individual species depends upon interactions with pollinators, symbiotes, food plants, herbivores, parasites, predators, and competitors. Most of these studies focus in on a single interaction—but what living thing interacts with only one other organism? Coevolution, when it happens, happens in a community context.

Adding even a second interaction into the scientific picture can be difficult, but it may also dramatically change the evolutionary outcome, as seen in a new study of evolution in the protozoan communities living in purple pitcher plants. Individually, competitors and predators are significant agents of natural selection—but together, they seem to counterbalance each other [$a].

The purple pitcher plant, Sarracenia purpurea. Photo by petrichor.

Carnivorous pitcher plants grow funnel-shaped leaves that collect water to form a pitfall trap for hapless insects, which provide a source of nitrogen in swampy, nutrient-poor habitats. One species’ pitfall is another’s ideal habitat, however, and pitchers also play host to diverse micro-communities [PDF] of protozoans, bacteria, and even mosquito larvae. By recreating—and experimentally manipulating—these communities in the laboratory, the new study’s author, Casey terHorst, was able to disentangle the individual and combined effects of two different kinds of species interaction within pitcher plant pitfalls.

TerHorst focused on a protozoan species in the genus Colpoda, a widespread single-celled critter found in moist soil and standing water. In pitcher plants, Colpoda makes a living feeding on bacteria that break down insects trapped by the pitfall—and they themselves are prey for the larvae of the mosquito Wyeomyia smithii.

An example of genus Colpoda, the group of ciliates studied (but probably not the same species). Photo by PROYECTO AGUA** /** WATER PROJECT.

To determine the individual and combined effects of competition and predation on Colpoda, terHorst allowed experimental populations of the protozoan to evolve for 20 days (about 60-120 Colpoda generations) with either (1) no competitors or predators, (2) competition from another bacteria-eating protozoan, (3) predation by mosquito larvae, or (4) competition and predation. At the end of the experimental period, he sampled each evolved Colpoda population and measured a number of traits, including the size of Colpoda cells and their speed. Larger Colpoda cells are thought to be better competitors but more vulnerable to predators; faster ones should be better able to evade predation.

Individually, predators and competitors had significant effects on Colpoda evolution. In the presence of mosquito larvae, Colpoda evolved smaller, faster cells than it did alone. Unexpectedly, competitors also caused Colpoda to evolve smaller cells, though not faster ones. TerHorst suggests that this is because competition also favored more rapid reproduction by Colpoda, which meant that individual cells grew less before dividing.

Most interestingly, though, Colpoda evolving in the presence of both predators and competitors looked quite a lot like Colpoda that evolved alone. This is apparently because the mosquito larvae ate both Colpoda and its competitor—the mosquitoes acted to relieve some competitive pressure on Colpoda at the same time they ate fewer Colpoda because they had two prey species to pursue. In fact, the mosquitoes preferred to eat the competitor species, since it tended to hang out in the open while Colpoda hid among the plastic beads lining the base of the artificial habitat.

Thus the indirect effects of the predator offsetting competition, and of the competitor drawing away predation, canceled out the natural selection each imposed on Colpoda individually. Species interactions in a community context, even a simple one like this, are far from straightforward.

References

Buckley, H., Burns, J., Kneitel, J., Walters, E., Munguia, P., & Miller, E. (2004). Small-scale patterns in community structure of Sarracenia purpurea inquilines. Community Ecology, 5 (2), 181-8 DOI: 10.1556/ComEc.5.2004.2.6

terHorst, C. (2010). Evolution in response to direct and indirect ecological effects in pitcher plant inquiline communities. The American Naturalist, 176 (6), 675-85 DOI: 10.1086/657047

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

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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.

References

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

Butterfly, heal thyself! (Or thy kids, anyway.)

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Monarch butterfly, Danaus plexippus. (Flickr: Martin LaBar)

ResearchBlogging.orgUsing specific compounds to cure disease seems like a fairly advanced behavior—it’s necessary to recognize that you’re sick, then know what to take to cure yourself, then go out and find it. You might be surprised to learn, then, that one of the best examples of self-medication behavior in a non-human animal isn’t another primate species, or even another vertebrate. It’s none other than monarch butterflies. Female monarchs infected with a particular parasite prefer to lay eggs on host plants that help their offspring resist the parasite [PDF].

(I first heard about this discovery at this spring’s Evolution meetings, and learned that the article had been published online last week via Bora Zivkovic‘s link to coverage by Scientific American.)

. A monarch caterpillar. (Flickr: Martin LaBar)

Most natural monarch butterfly populations are infected, at varying rates, with the protozoan parasite Ophryocystis elektroscirrha. Monarch larvae become infected when they eat parasite spores laying on the leaves of their food plants; the parasites reproduce inside the growing larvae form more spores while the larvae undergoes metamorphosis. Infected adults emerge from their chrysalises covered in O. elektroscirrha spores, which they spread to their mates and to their own offspring.

Infection reduces monarchs’ lifespans and damages their flight performance [PDF]. This creates a selective tradeoff that prevents the parasites from becoming too damaging—gimpy (or dead) monarchs are less effective at spreading spores [PDF]—but the butterflies are still better off if not infected at all. It’s convenient for monarchs, then, that the plants they prefer to eat can also fight Ophryocystis elektroscirrha.

Monarch caterpillars are well-known to eat milkweeds, which defend themselves by producing organic compounds in a class called cardenolides—literally “heart poisons.” These deter lots of insect herbivores, but monarch caterpillars have evolved physiological mechanisms to store up cardenolides without suffering ill effects, which in turn makes each caterpillar, and its later adult phase, toxic to predators. (Lots of specialist herbivores evolve tolerances to, or even preferences for, their host plants’ defensive chemistry.)

It turns out that cardenolides are also bad for monarchs’ parasites. In an experiment published in 2008, de Roode et al. raised monarch caterpillars on two milkweed species that produced differing amounts of cardenolides, Asclepias curassavica and A. incarnata. They found that infected caterpillars fed the more toxic A. curassavica suffered fewer ill effects of infection [PDF].

This result is remarkable enough on its own. It suggests that the effects of infection by Ophryocystis elektroscirrha might vary in natural monarch populations depending on something separate from the monarch-parasite interaction itself—the toxicity of the locally-available milkweed species. But what if monarchs could choose more toxic milkweed to fight infection?


A female monarch feeds on butterflyweed, Asclepias tuberosa. (Flickr: donsutherland1)

This possibility of self-medication by monarchs is the focus of the latest result in the monarch-parasite system. In the new study, a team of researchers at Emory University and the University of Michigan offered infected and uninfected monarch caterpillars leaf cuttings from both of the milkweed species used in the 2008 experiment. However, infected caterpillars showed no greater preference for the more toxic milkweed.

Caterpillars might not be well-suited to self-medication anyway; they’re not very mobile, and so stuck with the host plant patch in which they hatch. Adult female monarchs, on the other hand, can fly—and seek out a patch of parasite-fighting plants on which to lay their eggs. In a second experiment, the team offered infected and uninfected adult females the opportunity to lay eggs on a single plant of each milkweed species, placed at opposite ends of a flight cage. And, indeed, infected female monarchs looked out for the best interest of their offspring, laying a larger proportion of their eggs on the more toxic plant.

This sort of trans-generational self-medication raises some very interesting questions, particularly, how do infected monarchs know they’re infected? How does local diversity of milkweed species in natural populations alter the coevolution of monarchs with Ophryocystis elektroscirrha? There’s still a lot to learn about this fascinating behavior, which may be happening in backyards across North America.

To conclude, here’s a great video produced by Emory University, in which Principal Investigator Jaap de Roode talks about monarchs in general, and the new discovery in particular.

References

Bradley, C., & Altizer, S. (2005). Parasites hinder monarch butterfly flight: implications for disease spread in migratory hosts. Ecology Letters, 8 (3), 290-300 DOI: 10.1111/j.1461-0248.2005.00722.x

de Roode, J., Pedersen, A., Hunter, M., & Altizer, S. (2008). Host plant species affects virulence in monarch butterfly parasites. Journal of Animal Ecology, 77 (1), 120-6 DOI: 10.1111/j.1365-2656.2007.01305.x

de Roode, J., Yates, A., & Altizer, S. (2008). Virulence-transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. Proceedings of the National Academy of Sciences, 105 (21), 7489-94 DOI: 10.1073/pnas.0710909105

Lefèvre, T., Oliver, L., Hunter, M., & De Roode, J. (2010). Evidence for trans-generational medication in nature. Ecology Letters DOI: 10.1111/j.1461-0248.2010.01537.x

What keeps mutualists honest—cake, or death?

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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.

References

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

Are mutualists monogamists, while antagonists play the field?

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ResearchBlogging.orgTwo of the most diverse groups of living things on Earth are flowering plants and the insects that make their living from flowering plants. Biologists have long thought that the almost incessant, intimate interactions between plants and plant-eating insects might be the evolutionary cause of each group’s spectacular diversity. On a smaller scale, this means that we’re interested in the reasons that specific insects and plants interact in the first place—what evolutionary trails leads one insect species to specialize on a single host while others eat pretty much any plant they land on.

A new study of one group of plant-eating insects suggests that the kind of interaction between insects and their host plants also determines how specific those interactions are. Examining a group of moths that, like the yucca moths I study, pollinate their host plant and then eat some of its seeds, the authors of the new study find that related, non-pollinating moths use more host plant species than the pollinators [$a]. I think it makes a particularly nice companion piece to my post about the evolutionary origins of yucca moths, because it provides an example of one or two other things biologists can deduce from phylogenies—and, as we’ll see, some things they can’t.

Epicephala: like a yucca moth without the snappy name

The moths in question are in the genus Epicephala, and they have an obligate pollination relationship with trees in the genus Glochidion, a diverse group of plant species found in southern Asia. That is, female moths carry pollen between Glochidion flowers in special mouthparts, deliberately apply pollen to the flower, and then lay eggs in the flower so that, when it develops into a fruit, her larvae can eat some of the seeds inside. Epicephala species are highly specialized, with most species only using one species of Glochidion [$a]. That’s a higher degree of specialization than what’s seen in yucca moths, in fact.

Pollinating moths (genus Ephicephala, left) use fewer host plant species than related non-pollinating moths (genus Caloptilia, right). Photos by CharlesLam and Bettaman.

The family of which Epicephala is a member happens to include other moths that interact with Glochidion, but only as herbivores: species in the genera Caloptilia and Diphtheroptila, whose larvae all eat Glochidion leaves. Do these antagonistic moths use more, or fewer, species of the host plant than the mutualistic Epicephala? Kawakita and his coauthors set out to answer that question by reconstructing the phylogenies of Caloptilia and Diphtheroptila.

Finding species in evolutionary trees

Most biologists agree that two groups of organisms are separate species if there is no gene flow between them. A consequence of genetic isolation between species is that, if they’re isolated long enough, they become monophyletic within phylogenies. That is, all the individuals within each species share a common ancestor that is not shared with any other species. You can see this by contrasting two monophyletic species (on the left in the figure below) with two groups that turn out to be paraphyletic—some individuals of the red species are more closely related to individuals of the blue species than to other individuals of their own species.

Monophyletic and paraphyletic groupings. Image by jby.

The reasoning behind this is a bit subtle. Paraphyletic groups might still be separate species—they just haven’t been isolated long enough to become monophyletic. As a good example, I’m a coauthor on a recent study that did this kind of analysis on non-pollinating “bogus” yucca moths that use three different yucca species. In that case, the moths were paraphyletic with respect to which yucca species they used, but more analysis showed that there is currently very little gene flow between moths using different hosts [PDF].

In the case of the Glochidion-using Caloptilia and Diphtheroptila, Kawakita et al. found something more complicated. Each genus broke up into several monophyletic groupings, or clades of genetically similar individuals—but in most cases each clade included moths collected from at least two different Glochidion species. Kawakita et al. note that the clades also correspond to differences in the moths’ wing coloration, larval feeding behavior, and genitalia, and conclude that each clade is a different species. That would mean that the two antagonist genera tend to use multiple host plants.

Interesting question, but is this the way to answer it?

Except I’m not sure I buy this usage of phylogenies to define species. Kawakita et al. have shown that within the clades they call species, the individuals all have very similar genetics, but only for the two commonly-used genetic markers from which the phylogenies are reconstructed. It’s not impossible that within each clade the moths might be adapted to individual host plant species, and reproductively isolated by that adaptation—and this could have happened recently enough that not many genetic differences would have built up in the two markers.

To really answer the question Kawakita et al. have posed would require a study of each clade in the two antagonist genera at a much finer scale. The question of how specialized Caloptilia and Diphtheroptila are hinges on how many species are in each genus, and that’s better addressed by examining population genetics, not ancient relationships among these genera.

Reference

Drummond, C., Xue, H., Yoder, J., & Pellmyr, O. (2009). Host-associated divergence and incipient speciation in the yucca moth Prodoxus coloradensis (Lepidoptera: Prodoxidae) on three species of host plants. Heredity, 105 (2), 183-96 DOI: 10.1038/hdy.2009.154

Kawakita, A., & Kato, M. (2006). Assessment of the diversity and species specificity of the mutualistic association between Epicephala moths and Glochidion trees. Molecular Ecology, 15 (12), 3567-81 DOI: 10.1111/j.1365-294X.2006.03037.x

Kawakita, A., Okamoto, T., Goto, R., & Kato, M. (2010). Mutualism favours higher host specificity than does antagonism in plant-herbivore interaction. Proc. Royal Soc. B, 277 (1695), 2765-74 DOI: 10.1098/rspb.2010.0355

Freeloading cuckoos force their hosts to diversify

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ResearchBlogging.orgAshy-throated parrotbills have a problem every time breeding season rolls around: how do they know whether the eggs in their nests are their own, or those of the common cuckoo? A study recently released in PLoS ONE suggests that one population of parrotbills fights this brood parasitism by laying eggs of different colors.

Common cuckoos lay eggs that mimic those of the host birds they trick into raising cuckoo chicks. Photo by Sergey Yeliseev.

Brood parasitism, in which one bird species lays its eggs in another bird’s nest, has long been considered a likely cause of coevolution [$a] between brood parasites and their hosts, because the interaction exerts strong natural selection on both species. Hosts suffer major fitness consequences if they take on the raising of another bird’s chick—and brood parasite chicks are often bigger, and more aggressive, than their adoptive “siblings,” sometimes pushing them right out of the nest. On the other hand, brood parasites run the risk of losing their offspring to hosts who can recognize a strange egg and eject it from the nest.

One way to avoid raising a cuckoo chick is to lay eggs that look different from cuckoo eggs. Cuckoos counteract this defense by evolving eggs that match their most common hosts—a selective regime proposed to explain rapid rates of species formation in parasitic cuckoo lineages. In the new study, Yang et al. show that this pattern plays out within a single population of ashy-throated parrotbills and the cuckoos that parasitize them. At a forested nature reserve in southwestern China, the team found that parrotbills lay eggs of three different colors: white, blue, or (rarely) pale blue. Common cuckoos in the same area also laid eggs of those three colors, in about the same proportions as the parrotbills—and cuckoo eggs were usually found in host nests with eggs of the same color. Experimental introduction of eggs into parrotbill nests confirmed that parrotbills were more likely to reject eggs colored differently from their own.

That result captures many of the necessary conditions for coevolution between ashy-throated parrotbills and the local cuckoo population; the frequency with which parrotbills reject eggs unlike their own should exert strong selection on the cuckoos, and (conversely) the frequency with which parrotbills fail to reject cuckoo eggs that look like their own should exert selection on the hosts. This isn’t the first case in which brood parasites have apparently forced their hosts to diversify, however—notably, African village weaverbirds evolved less varied egg patterning after being introduced into parasite-free habitats on Mauritius and Hispaniola.

References

Krüger, O., Sorenson, M., & Davies, N. (2009). Does coevolution promote species richness in parasitic cuckoos? Proc. Royal Soc. B, 276 (1674), 3871-9 DOI: 10.1098/rspb.2009.1142

Lahti, D. (2005). Evolution of bird eggs in the absence of cuckoo parasitism. Proc. Nat. Acad. Sci. USA, 102 (50), 18057-62 DOI: 10.1073/pnas.0508930102

Rothstein, S. (1990). A model system for coevolution: Avian brood parasitism. Ann. Rev. Ecology and Systematics, 21 (1), 481-508 DOI: 10.1146/annurev.es.21.110190.002405

Yang, C., Liang, W., Cai, Y., Shi, S., Takasu, F., Møller, A., Antonov, A., Fossøy, F., Moksnes, A., Røskaft, E., & Stokke, B. (2010). Coevolution in action: Disruptive selection on egg colour in an avian brood parasite and its host. PLoS ONE, 5 (5) DOI: 10.1371/journal.pone.0010816

Caught between birds and squirrels, limber pines go both ways

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ResearchBlogging.orgResponding to natural selection often means compromising between different selective forces. A brief paper published online early at Evolution documents one such case – limber pine trees’ compromise between protecting their seeds from squirrels, and making them accessible to the birds that disperse them. Pulled between these conflicting selective sources, some limber pine populations grow cones in a wider variety of shapes [$a].



Cones of the limber pine must balance protection against squirrels with accessibility for seed-dispersing Clark’s nutcrackers. Photos by Fool-On-The-Hill and almiyi.

Seeds of the limber pine are cache-dispersed by Clark’s nutcrackers. That is, the birds collect pine seeds to cache as a winter food source, but they collect many more than they need, and forget lots of them, and forgotten seeds are often able to sprout. However, squirrels also like pine seeds, and they harvest them before the birds start caching seeds. These two seed-harvesters generate conflicting selection on limber pine cones [$a]. Nutcrackers go for cones with lots of seeds protected by thinner scales; but so do squirrels.

However, pine-nut-eating squirrels are not present everywhere limber pines grow. The new study’s authors, Siepielski and Benkman, take advantage of this quirk of distributions to perform a natural experiment, comparing pines that only need to satisfy their seed dispersers with pines that also need to defend against seed predators. Surveying cone shapes in populations of each class, they found that limber pine populations facing conflicting selection were bimodal, with trees mainly growing either squirrel-defended short, thick-scaled cones, or nutcracker-friendly longer, thin-scaled cones. Populations growing in regions without squirrels produced only nutcracker-friendly cones.

This apparently simple pattern conceals more complicated dynamics – in fact, as the authors disclose in the Discussion section, many other limber pine populations are solely composed of trees producing squirrel-defended cones. This is because, when pines establish in areas with large squirrel populations, nutcrackers may never colonize the area, or may visit less frequently and disperse fewer seeds. Without nutcracker dispersal, seeds are mainly dispersed after the cones fall, by rodent species that (unlike squirrels) forage on the ground. This makes squirrel defense the only selective priority. Populations displaying both cone types probably only arise in unique conditions, the authors say, where squirrels are present but not at high density.

References

Siepielski, A., & Benkman, C. (2007). Convergent patterns in the selection mosaic for two North American bird-dispersed pines. Ecological Monographs, 77 (2), 203-20 DOI: 10.1890/06-0929

Siepielski, A., & Benkman, C. (2009). Conflicting selection from an antagonist and a mutualist enhances phenotypic variation in a plant. Evolution DOI: 10.1111/j.1558-5646.2009.00867.x

Dethroning the Red Queen?

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ResearchBlogging.orgRegular readers of Denim and Tweed know that I’m fascinated by the evolution of species interactions: interactions between plants and nitrogen-fixing bacteria, Joshua trees and yucca moths, parasitoid wasps and butterflies, and between ants and the trees they guard. I tend to think that coevolutionary interactions not only determine the health of natural populations, but shape their evolutionary history. But would I feel that way if I were a paleontologist?

Running just to stay in place

The idea that interactions between species matter goes all the way back to the origins of evolutionary biology in the writing of Charles Darwin:

What a struggle between the several kinds of trees must here have gone on during long centuries, each annually scattering its seeds by the thousand; what war between insect and insect – between insects, snails, and other animals with birds and beasts of prey – all striving to increase, and all feeding on each other or on the trees or their seeds and seedlings, or on the other plants which first clothed the ground and thus checked the growth of the trees! (On the Origin of Species, 1859: 74-5)

This image of constant struggle among living things was more formally encapsulated in a 1973 paper by Leigh Van Valen (which paper is not, alas, available online), who proposed that constant coevolution with other species should mean that natural populations of living things are constantly adapting – in response to competitors, mutualists, predators, parasites – without gaining ground in the struggle, because the other species are also adapting. Van Valen lifted an image from Lewis Carroll’s Through the Looking-Glass, in which the Red Queen tells Alice that, in the strange world of Looking-Glass Land, “… it takes all the running you can do, to keep in the same place.”

They were running hand in hand, and the Queen went so fast that it was all she could do to keep up with her … The most curious part of the thing was, that the trees and the other things around them never seemed to changed their places at all.


“… it takes all the running you can do, to keep in the same place.” Image from Through the Looking-Glass, via VictorianWeb.

Thus, this idea that fuels much of my research, and a great deal of scientific study over the last three decades, is often identified with the Red Queen. What is interesting about this result is that Van Valen wasn’t interested in species interactions as such; he was trying to explain a pattern in the fossil record – that, for a wide variety of living things, the probability that a species would go extinct was independent of its age. That is, species that have been around for ten million years are no better adapted to their environments than species that have just formed; the probability of extinction is constant.

Van Valen’s explanation for this result was that something must constantly act to prevent living things from becoming better adapted, and better able to resist extinction, over time – specifically, the Red Queen’s race against other living things. Whenever a species “loses” the race, it goes extinct, regardless of how long the race has been up to that point. A similar pattern applies to the creation of new species – if coevolutionary interactions often help create reproductive isolation, then new species should also form at a roughly constant rate [$a]. Since this is what we observe, many biologists conclude that coevolution is responsible for the diversity of life on Earth.

What if the race doesn’t matter?

Fortunately for the advance of knowledge, however, not all evolutionary biologists have the same perspective. Paleontologists, for instance, tend to think that the year-to-year dynamics of the Red Queen race don’t make much difference in the longer run, over millions of years. They’d argue that most of the evolutionary change induced by coevolution between species is too variable and fleeting to have much effect on the rates at which species are formed and go extinct. Under this view, random geological events – continents splitting, mountain ranges rising, volcanoes erupting – are more likely to create new species and force them to extinction.


What matters more in the history of life, the biological environment, or the physical environment? Photos by Martin Heigan and Cedric Favero.

This competing model should also lead to a roughly constant rate of species formation and extinction, but it predicts a different pattern of variation around that constant rate than the coevolutionary Red Queen does. If most speciation and extinction events are caused by coevolution, then the time periods between speciation events should follow a normal distribution – forming a “bell curve” with most periods close to the average length, and symmetrical tails of longer and shorter periods of time. On the other hand, if many different, individually rare geological events are the most common cause of speciation and extinction, the periods between speciation events should follow an exponential distribution, with most periods being shorter than the average, but a long tail of longer periods as well.

This contrast is the crux of a study recently published in Nature. The paper’s authors, Venditti et al., examined 101 evolutionary trees estimated from genetic data, including groups like the dog family, roses, and bees. For each group’s evolutionary tree, they determined the distribution of the lengths of time periods between speciation events. A majority of the trees – 78% – supported the exponential model. That is, 78% of the groups of organisms examined had evolved and diversified in a fashion best explained by geology, not coevolution. None of the groups fit the normal distribution, and only 8% fit the related lognormal distribution.

The Red Queen is dead, long live the Red Queen!

This result suggests that within many groups of organisms, the physical environment is a more common cause of reproductive isolation or extinction than the biological environment. However, this isn’t to say that species interactions don’t matter. As Van Valen originally noted, extinction rates may be roughly constant within large groups of organisms, like those examined by Venditti et al., but those constant rates vary from group to group. These differences in rate may still depend on species interactions, because species interactions can shape how prone a population is to reproductive isolation.

For instance, a group of plants that has lousy seed dispersers may form new species in response to much smaller, and more common, geological barriers than a group of plants whose seeds can travel for hundreds of miles. Additionally, species interactions that promote diversity within the interacting species may mean that when geology creates isolation, the resultant daughter species are more different from each other than they would otherwise be, and less likely to re-merge if they come into contact again. Under that scenario, speciation caused by the physical environment would act to preserve variation [$a] created by the biological environment.

So, perhaps the Red Queen doesn’t operate the way we thought she did, with constant coevolutionary races spinning off new species and killing off others. But that hardly means that Red Queen processes don’t matter in the long run.

References

Benton, M. (2010). Evolutionary biology: New take on the Red Queen. Nature, 463 (7279), 306-7 DOI: 10.1038/463306a

Futuyma, D. (1987). On the role of species in anagenesis. The American Naturalist, 130 (3), 465-73 DOI: 10.1086/284724

Stenseth, N., & Maynard Smith, J. (1984). Coevolution in ecosystems: Red Queen evolution or stasis? Evolution, 38 (4), 870-80 DOI: 10.2307/2408397

Van Valen, L. (1973). A new evolutionary law. Evolutionary Theory, 1 (1), 1-30

Venditti, C., Meade, A., & Pagel, M. (2009). Phylogenies reveal new interpretation of speciation and the Red Queen. Nature, 463 (7279), 349-52 DOI: 10.1038/nature08630

Evolving from pathogen to symbiont

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This post was chosen as an Editor's Selection for ResearchBlogging.orgRecently the open-access PLoS Biology published a really cool study in experimental evolution, in which a disease-causing bacterium was converted to something very like an important plant symbiont. The details of the process are particularly interesting, because the authors actually used natural selection to identify the evolutionary change that makes a pathogen into a mutualist.

Life as we know it needs nitrogen – it’s a key element in amino acids, which mean proteins, which mean structural and metabolic molecules in every living cell. Conveniently for life as we know it, Earth’s atmosphere is 78% nitrogen by weight. Inconveniently, that nitrogen is mostly in a biologically inactive form. Converting that inactive form to biologically useful ammonia is therefore extremely important. This process is nitrogen fixation, and it is best known as the reason for one of the most widespread mutualistic interactions, between bacteria capable of fixing nitrogen and select plant species that can host them.


Clover roots, with nodules visible (click through to the original for a nice, close view. Photo by oceandesetoile.

In this interaction, nitrogen-fixing bacteria infect the roots of a host plant. In response to the infection, the host roots form specialized structures called nodules, which provide the bacteria with sugars produced by the plant. The bacteria produce excess ammonia, which the plant takes up and puts to its own uses. The biggest group of host plants are probably the legumes, which include the clover pictured to the right, as well as beans – this nitrogen fixation relationship is the reason that beans are the best source of vegetarian protein, and why crop rotation schemes include beans or alfalfa to replenish nitrogen in the soil.

For the nitrogen-fixation mutualism to work, free-living bacteria must successfully infect newly forming roots in a host plant, and then induce them to form nodules. The chemical interactions between bacteria and host plant necessary for establishing the mutualism are pretty well understood, and in fact genes for many of the bacterial traits, including nitrogen-fixation and nodule-formation proteins thought to be necessary to make it work are conveniently packaged on a plasmid, a self-contained ring of DNA separate from the rest of the bacterial genome, which is easily transferred to other bacteria.

This is exactly what the new study’s authors did. They transplanted the symbiosis plasmid from the nitrogen-fixing bacteria Cupriavidus taiwanensis into Ralstonia solanacearum, a similar, but disease-causing, bacterium. With the plasmid, Ralstonia fixed nitrogen and produced the protein necessary to induce nodule formation – but host plant roots infected with the engineered Ralstonia didn’t form nodules. Clearly there was more to setting up the mutualism than the genes encoded on the plasmid.


Wild-type colonies of Ralstonia (tagged with fluorescent green) are unable to enter root hairs (A), but colonies with inactivated hrcV genes are able to enter and form “infection threads,” like symbiotic bacteria (B). Detail of Marchetti et al. (2010), figure 2.

This is where the authors turned to natural selection to do the work for them. They generated a genetically variable line of plasmid-carrying Ralstonia, and used this population to infect host plant roots. If any of the bacteria in the variable population bore a mutation (or mutations) necessary for establishing mutualism, they would be able to form nodules in the host roots where others couldn’t. And that is what happened: three strains out of the variable population successfully formed nodules. The authors then sequenced the entire genomes of these strains to find regions of DNA that differed from the ancestral, non-nodule-forming strain.

This procedure identified one particular region of the genome associated with virulence – the disease-causing ability to infect and damage a host – that was inactivated in the nodule-forming mutant strains. As seen in the figure I’ve excerpted above, plasmid-bearing Ralstonia with this mutation were able to form infection threads, an intermediate step to nodule-formation, where plasmid-bearing Ralstonia without the mutation could not. Clever use of experimental evolution helped to identify a critical step in the evolution from pathogenic bacterium to nitrogen-fixing mutualist.

References

Amadou, C., Pascal, G., Mangenot, S., Glew, M., Bontemps, C., Capela, D., Carrere, S., Cruveiller, S., Dossat, C., Lajus, A., Marchetti, M., Poinsot, V., Rouy, Z., Servin, B., Saad, M., Schenowitz, C., Barbe, V., Batut, J., Medigue, C., & Masson-Boivin, C. (2008). Genome sequence of the  beta-rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia. Genome Research, 18 (9), 1472-83 DOI: 10.1101/gr.076448.108

Gitig, D. (2010). Evolving towards mutualism. PLoS Biology, 8 (1) DOI: 10.1371/journal.pbio.1000279

Marchetti, M., Capela, D., Glew, M., Cruveiller, S., Chane-Woon-Ming, B., Gris, C., Timmers, T., Poinsot, V., Gilbert, L., Heeb, P., Médigue, C., Batut, J., & Masson-Boivin, C. (2010). Experimental evolution of a plant pathogen into a legume symbiont. PLoS Biology, 8 (1) DOI: 10.1371/journal.pbio.1000280