Category Archives: coevolution

Milkweed’s bitter arms race against herbivores

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ResearchBlogging.orgPlants are locked in a long twilight struggle with herbivores, particularly insects – sometimes they evolve a new defensive mechanism, “escaping” to diversify into new groups [$-a], but mostly natural selection works with the traits they already have. That means arms races – plants evolving greater concentrations of defense chemicals, and herbivores evolving greater tolerance of those chemicals. In this month’s Evolution, a new study of defensive chemistry evolution in milkweed [$-a] documents exactly this process.


Asclepias viridis, a milkweed
Photo by gravitywave.

The study by Agrawal et al. follows up on earlier work in the same group, which established the evolutionary relationships between the members of the milkweed genus, Asclepias. Milkweeds are named for their defense against insect herbivores, a milky sap full of nasty chemicals – coumaric acids, caffeic acids, cardenolides, and flavonoids. The authors raised a large sample of milkweed species in a controlled environment, then measured the levels of these chemicals in each species. By mapping the chemical profiles onto the previously-developed phylogeny of Asclepias, they could estimate how milkweeds’ chemistry has evolved since the genus first arose.


Aphids on Asclepias
Photo by aroid.

This analysis revealed that milkweeds have gotten nastier over their evolutionary history. But it’s not that clear-cut: the diversity of defensive chemicals present in Asclepias decreased, even as the total production increased – so the plants seemed to be paring down an initial diversity of defenses into a few chemicals that worked especially well. Coumaric and caffeic acids, which are produced from the same biochemical precursors, forced a trade-off so that as one increased, the other decreased. On the other hand, cardenolides and flavonoids, which are both produced in another biochemical pathway, were positively associated.

If this sounds complicated, that’s because it is. As Agrawal and his coauthors point out, we actually don’t have a good sense at what timescale an arms race should manifest – that is, are we talking about plants evolving greater defenses over a few generations, or over millions of years, as this study? Natural selection can appear to be moving a population strongly in one direction for a year or two – and then turn out to be fluctuating all over the place [$-a] if you watch for decades. How year-to-year selection acting on multiple traits translates into the grand trends of evolution – whether the explosive diversification of flowering plants or the emergence of human intelligence – remains one of the big puzzles for those of us who study the living world.

Reference

A.A. Agrawal, J.-P. Salminen, M. Fishbein (2009). Phylogenetic trends in phenolic metabolism of milkweeds (Asclepias): Evidence for escalation. Evolution, 63 (3), 663-73 DOI: 10.1111/j.1558-5646.2008.00573.x

P.R. Ehrlich, P.H. Raven (1964). Butterflies and plants: a study in coevolution Evolution, 18, 586-608 DOI: http://www.jstor.org/pss/2406212

P.R. Grant, B.R. Grant (2002). Unpredictable evolution in a 30-Year study of Darwin’s finches Science, 296 (5568), 707-11 DOI: 10.1126/science.1070315

What puts the “co” in coevolution?

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ResearchBlogging.orgCoevolution is like the opposite of pornography – lots of scientists can define it with nicety, but most of us have trouble saying for sure whether any given pair of species are actually coevolving. “Coevolution” literally means “evolving together” – more formally, that an evolutionary change in one species causes a reciprocal change in another [$$]. But this process can be quite complicated to demonstrate in practice. In the latest example of this conundrum, a paper in this month’s Evolution suggests that one relationship we thought was coevolutionary maybe isn’t [$-a].


Leafcutter ants at work
Photo by rofanator.

Leafcutter ants have been thought to be involved in clear-cut coevolutionary relationships with a number of microbial species. Leafcutters, as is pretty well known, harvest leaf fragments to feed fungal gardens, which the ants use as a food source. That’s one relationship: ant-fungus. Less well-known are the ants’ relationships with bacteria – bacteria that fight off the fungus-garden-killing diseases, in the genus Pseudonocardia. Pseudonocardia grow on leafcutter ants’ exoskeletons [$-a], and the ants seem to regulate the bacteria’s growth depending on how much they need the antibiotics it produces. This seems like an obvious case of coevolution – the ants and their bacteria symbiotes live in close proximity to each other, and seem to rely on each other for their respective ways of life.

But the new paper, by Mueller et al., indicates that appearances can be deceiving. The authors present a new phylogeny of the bacterial family containing Pseudonocardia, which suggests that leafcutter ants frequently “recruit” new strains of Pseudonocardia from their environment. Coevolution, the authors argue, would mean that a single lineage of bacteria has been associated with the ants from the beginning of the relationship – but the phylogeny shows, instead, that ant-associated Pseudonocardia are often more closely related to free-living bacteria than to other strains of ant-associated Pseudonocardia. That is, the ant-associated strains are not monophyletic. Furthermore, individual ant species often carry Pseudonocardia from multiple different evolutionary lineages, which suggests that “recruitment” events don’t happen one after another, but continuously.

This result makes good biological sense. Ants using Pseudonocardia to control disease probably stimulate the evolution of resistant disease organisms, just the same problem that humans have found after less than a century of antibiotic use. Recruiting new strains of antibiotic-producing bacteria is just the way to deal with resistant disease organisms. It therefore makes about as much sense to say that ants are coevolving with Pseudonocardia as it would to say that humans are coevolving with penicillin – both the ant-associated bacterium and the mass-produced antibiotic are tools to be cast away when no longer useful.

Reference

C.R. Currie, J.A. Scott, R.C. Summerbell, D. Malloch (1999). Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature, 398 (6729), 701-4 DOI: 10.1038/19519

DH Janzen (1980). When is it coevolution? Evolution, 34 (3), 611-2 http://www.jstor.org/pss/2408229

U.G. Mueller, D. Dash, C. Rabeling, A. Rodrigues (2008). Coevolution between Attine ants and Actinomycete bacteria: A reevaluation. Evolution, 62 (11), 2894-912 DOI: 10.1111/j.1558-5646.2008.00501.x

Joshua tree genetics suggest coevolutionary divergence

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ResearchBlogging.orgThe latest results from the Pellmyr Lab’s ongoing study of Joshua tree and its pollinators are online as part of the new October issue of Evolution. It’s the cover article, no less. The study, whose lead author is Chris Smith (now on the faculty at Willamette University) compares patterns in the population genetics of Joshua trees and the moths that pollinate them, and shows that although the moths have become two separate species, the trees may not have followed suit [PDF].

Evolution cover
Photo by Chris Smith.

Female yucca moths carry pollen between Joshua tree flowers in special mouthparts. When she arrives at a new flower, the female moth lays her eggs inside it, then deliberately applies pollen to the flower’s receptive surface. When the fertilized flower develops into a fruit, the moth eggs hatch, and the larvae eat some of the seeds inside the fruit.

Among the yuccas, Joshua trees are unique because they’re pollinated by two species of moths, which are each other’s closest evolutionary relative. One species is found in the eastern part of Joshua tree’s range, the other in the west. Joshua trees from the east and west have differently-shaped flowers [PDF], which is consistent with the hypothesis that coevolution between moths and trees has driven both toward an evolutionary split.

“Western” Joshua trees at Joshua Tree National Park. Photo by me.

The new study goes deeper to look at genetic relationships between different populations of the moths and the trees, and what it finds isn’t as tidy as the earlier work might suggest: While Joshua trees’ morphology corresponds nicely to the split in the pollinators, the patterns visible in their chloroplast DNA does not. In some populations, trees look “eastern,” but have chloroplast DNA more closely related to “western” populations. This suggests that, although the moths have become separate species, they’re still moving between the two kinds of Joshua tree frequently enough that the trees haven’t quite split. Why do the two tree types look different, then? One possibility is coevolution with the two moth species, which might exert selection the trees in different ways.

There’s still a lot of work to do before we fully understand what’s going on here. Will Godsoe, the other doctoral student in our lab, is doing some intensive niche modeling to see how much environmental differences might be contributing to the patterns we see here. My own dissertation will look at whether the same incongruities turn up in nuclear DNA, which can have a different evolutionary history than that in the chloroplast.

References

W. Godsoe, J.B. Yoder, C.I. Smith, O. Pellmyr (2008). Coevolution and Divergence in the Joshua Tree/Yucca Moth Mutualism The American Naturalist, 171 (6), 816-23 DOI: 10.1086/587757

C.I. Smith, W.K.W. Godsoe, S. Tank, J.B. Yoder, O. Pellmyr (2008). Distinguishing coevolution from covicariance in an obligate pollination mutualism: asynchronous divergence in Joshua tree and its pollinators. Evolution, 62 (10), 2676-87 DOI: 10.1111/j.1558-5646.2008.00500.x

Species hiding in plain sight

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ResearchBlogging.orgIt’s a truism that biologists have cataloged only a fraction of the living things on Earth. This is a major problem for conservationists, ecologists, and evolutionary biologists, because many of the questions we want to answer (“Which parcel of rain forest should we preserve?” or “How do species interactions play out over millions of years?”) hinge how we count species.

One solution is DNA barcoding, which uses the evolutionary divergence encoded in DNA sequences to tell species apart [$-a]. Barcoding is supposed to help researchers identify species without being experts in the fiddly business of taxonomy based on physical traits. It can also differentiate species that might never be recognized as separate without a DNA analysis.


Caterpillar with braconid pupae
Photo by Anita Gould.

An open-access article in last week’s PNAS does exactly that for a group of wasps in the family Braconidae. Braconid wasps are parasitoids, laying their eggs in live hosts. Eventually the eggs hatch and the larvae eat their host alive, then emerge to form pupae like those on the Hog Sphinx Moth caterpillar in the photo. (Insert obligatory reference to Alien here.)

Parasitoid wasps are thought to be hugely diverse, in part because coevolutionary interactions between larvae and their hosts’ immune systems might force each wasp species to specialize on one or a few hosts. Smith and coauthors use barcoding based on nuclear and mitochondrial DNA to determine the diversity of braconid wasps within a Costa Rican conservation area, comparing the results to those produced from a traditional taxonomic survey. Traditional methods found 171 potential species – and barcoding turned up another 142! These additional species were basically identical to the eye, but in many cases they’re actually collections of similar species using different hosts.

So not only are there more wasp species than traditional methods would detect – they’re more specialized than we’d know without barcoding. DNA Barcoding can make some biologists (including me) a little squeamish; it’s worrying to picture a world where no one really knows the organisms they study except through DNA sequence data. But Smith et al. are applying the method to find diversity that would probably not be detected in any other way, with results that bear directly on how we think about the interactions between parasitoids and their hosts. That’s unquestionably a good thing.

References

P.D.N. Hebert, A. Cywinska, S.L. Ball, J.R. deWaard (2003). Biological identifications through DNA barcodes Proc. Royal Soc. B., 270 (1512), 313-21 DOI: 10.1098/rspb.2002.2218

M.A. Smith, J.J. Rodriguez, J.B. Whitfield, A.R. Deans, D.H. Janzen, W. Hallwachs, P.D.N. Hebert (2008). Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections PNAS, 105 (34), 12359-64 DOI: 10.1073/pnas.0805319105

How the chili got its hots

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In this week’s PNAS: capsaicin, the stuff that makes chili peppers hot, may have originally evolved as an anti-fungal agent [$-a].


Photo by bleu celt.

Tewksbury et al. examine variation in “pungency” (that is, concentration of capsaicin) in wild populations of the chili Capsicum chacoense and compare it to rates of fungal infection in the fruit. The result is interesting, and not necessarily clear-cut: more-pungent fruits are less frequently attacked by an assortment of true bugs, and when these bugs attack, they can introduce fungal spores into the fruit, which ultimately destroys the seeds inside. So more pungency means less bug damage, and lower rates of fungal infection, and potentially more seeds.

But the story of chili pungency is more complicated than that. Back in 2001, Tewksbury and Nabhan showed that capsaicin helps ensure that chilis are eaten by birds instead of mammals [$-a]. Birds make good seed dispersers – they eat a fruit, then, um, pass the seeds on undigested; mammals, on the other hand, like to eat the seeds specifically. Capsaicin irritates mammals, but doesn’t bother birds.

To complicate things still further, there’s a downside to producing capsaicin. In this January’s issue of the journal Ecology, Tewksbury and his coauthors showed that Capsicum chacoense seeds from more-pungent fruits also had thinner seed coats, which meant they were more likely to suffer damage in birds’ digestive tracts [$-a].

So why are chilies spicy? The answer is, probably for all these reasons, and maybe more that haven’t been discovered yet. This is a common situation in evolutionary biology – in many organisms, the traits that scientists find interesting may be useful in several different ways, and unhelpful in others. Very few traits experience natural selection in only one direction, as it turns out. The traits that we observe in nature are usually compromises between many different, sometimes directly conflicting, sources of natural selection.

References

J. J. Tewksbury, D. J. Levey, M. Huizinga, D. C. Haak, A. Traveset (2008). Costs and benefits of capsaicin-mediated control of gut retention in dispersers of wild chilies Ecology, 89 (1), 107-17 DOI: 10.1890/07-0445.1

J. J. Tewksbury, G. P. Nabhan (2001). Seed dispersal: Directed deterrence by capsaicin in chilies. Nature, 412 (6845), 403-4 DOI: 10.1038/35086653

J. J. Tewksbury, K. M. Reagan, N. J. Machnicki, T. A. Carlo, D. C. Haak, A. L. C. Penaloza, D. J. Levey (2008). Evolutionary ecology of pungency in wild chilies PNAS, 105 (33), 11808-11 DOI: 10.1073/pnas.0802691105

Against specialist herbivores, plants give up

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Plants put up with a lot – everyone wants to eat them! And, basically, there are two ways a plant might respond to being eaten. They can put energy into regrowing bits that get eaten, or they can put energy into making a lot of some nasty chemical, like the milky sap in milkweed. The trouble with the first option is obvious – it doesn’t do anything to stop the damage. But the trouble with the second is that, whenever plants evolve a new defensive strategy, herbivores evolve a way around it. Often, these herbivores do very well, because they can eat something no one else can – and they become specialists on their new favorite food.


Photo by Melete.

Evolutionary ecologists have been thinking about this plant-herbivore arms race ever since Darwin. Back in 1964, Paul Erhlich and Peter Raven proposed that plants and insects might go through alternating cycles of diversification [$-a] driven by the evolution of new plant defenses and insect counterdefenses. Now, in a new paper in last week’s PNAS, Anurag A. Agrawal (who is at the top of everyone’s reference list) and Mark Fishbein show that sometimes, plants just throw in the towel [$-a].

Agrawal and Fishbein examine the evolutionary history of milkweed, which has a number of interesting anti-herbivore defenses besides the eponymous sap – and a number of specialized herbivores, like the red milkweed beetle pictured here. Their analysis looks for long-term evolutionary trends in the degree to which milkweeds put their energy into defenses, and the degree to which they put energy into regrowth. Over evolutionary time, it seems that milkweeds have reduced their defenses, and increased their regrowth efforts.

References

A. A. Agrawal, M. Fishbein (2008). Phylogenetic escalation and decline of plant defense strategies PNAS, 105 (29), 10057-10060 DOI: 10.1073/pnas.0802368105

P.R. Ehrlich, P.H. Raven (1964). Butterflies and plants: A study in coevolution Evolution, 18 (4), 586-608

First Joshua tree article online

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The first publication from the Pellmyr Lab’s study of Joshua trees and their pollinators, in which we demonstrate significant, potentially coevolved, morphological differences in Joshua trees pollinated by different species of yucca moths, is now online at the American Naturalist’s website. My understanding is that it’ll be in the print edition this June.

Godsoe W, JB Yoder, CI Smith, and O Pellmyr. 2008. Coevolution and Divergence in the Joshua Tree/Yucca Moth Mutualism. The American Naturalist 171.

Parasites help figs control pollinators

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Fresh off the open-access press at PLoS Biology: parasites may help to stabilize the mutualism between figs and fig wasps.

In nature, mutualistic relationships usually conceal a tug-of-war between interacting species. This is especially clear in the case of pollinating seed parasites, like yucca moths (my favorite) and fig wasps. Both these insects pollinate their eponymous host plants, then lay eggs in the fertilized flowers so their larvae can eat some of the seeds produced. Natural selection should push each interactor to overexploit this deal: the pollinator “wants” to lay lots of eggs, but the plant “wants” to get as many seeds as possible. Yuccas keep yucca moths in check by killing off flowers with too many eggs inside [subscription], but there hasn’t been a similar mechanism found in figs.

Until now. In the new paper, Dunn et al. show that the figs might benefit from parasites that attack the pollinating wasps. Fig flowers grow in “synconia,” hollow globes like the one in the photo above, which are lined inside with tiny flowers. Fig wasps climb inside the synconia to pollinate and lay their eggs in the flowers. Another wasp species parasitizes the pollinators by laying its eggs near pollinator eggs, so their larvae can eat the pollinator larvae when they hatch. Turns out, the parasites lay their eggs from the outside of the synconium, and the flowers inside the synconium vary in how close they are to the outer wall. Any pollinator eggs laid too close to the outer wall of the synconium are nailed by parasites – so the pollinators have an incentive to only lay eggs in the innermost flowers. Neato!

Reference:
Dunn, D.W., S.T. Segar, J. Ridley, R. Chan, R.H. Crozier, D.W. Yu, and J.M. Cook. 2008. A Role for Parasites in Stabilising the Fig-Pollinator Mutualism. PLoS Biol 6(3): e59.

Trees ditch mutualist ants when herbivory stops

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Ant domatium on Acacia. Photo by Alastair Rae.

In this week’s issue of Science: African Acacia trees reduce support for a mutualistic species of ant when they aren’t experiencing herbivory [abstract only without subscription]. Normally, the whistling thorn tree (Acacia drepanolobium) enlists the help of an ant, Crematogaster mimosae, to fight off large herbivores and harmful insects. It works like this: The tree attracts ants by providing sugary nectar from glands at the base of its leaves and balloonlike growths called domatia (see photo), which the ants use for shelter. The ants attack anything that tries to eat the tree, for the very reasonable (and selfish) reason that it’s also their nest. It seems like a mutually beneficial arangement, but no one has tested the hypothesis that, if the trees no longer need defense, they’ll stop “paying” their ants to stick around.

Palmer et al. do exactly that by comparing ant provisioning on trees in plots that are fenced in (preventing access by big herbivores) with trees in control plots that aren’t. After ten years inside the fence, they found that Acacia trees had reduced their nectar output and the rate at which they developed new domatia. The mutualistic ants, dependent on these rewards, were displaced by another species, C. sjostedti, which doesn’t need nectar or domatia, but also doesn’t defend the tree as much.

None of the changes in trees’ provisioning for ants are the result of immediate natural selection – the time over which this happened is considerably less than one generation for Acacia. This is individual trees “judging” that they no longer need ant protection because they’re not under attack, a response that is expected to evolve over long periods of balancing the need for protection against the cost of provisioning ants. Another ant species that uses Acacia nectar and domatia, C. nigriceps, didn’t suffer from the lack of large herbivores, probably because it prunes the trees it occupies, which the authors think may be enough to make the tree “think” it’s still being eaten.

Reference:
Palmer T.M., M.L. Stanton, T.P. Young, J.R. Goheen, R.M. Pringle, and R. Karban. 2008. Breakdown of an Ant-Plant Mutualism Follows the Loss of Large Herbivores from an African Savanna. Science 319:192-5.

Red means stop?

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New in the Journal of Evolutionary Biology: An article asks whether autumnal leaf colors could act as a deterrent to insect herbivores [abstract free; subscription needed for more].

It may seem odd to think that trees could be interested in defending leaves that are about to drop off anyway; but the authors’ idea is that trees with brighter red leaves are signaling a “commitment” to producing more defensive chemicals in next year’s leaf crop. To test this hypothesis, the authors measured aphids’ preference for leaf color in the fall, and whether fall leaf color predicted aphids’ performance on the same trees in the spring.

The aphids showed a significant preference for green autumn leaves over red, but there was no correlation between fall color and aphid performance on the next spring’s leaves. So, interesting idea, but no dice. The authors say, reasonably, that their results suggest aphids’ color preferences have more to do with finding the most nutritious leaves in the fall than avoiding defensive chemicals in the spring.

It’s important to note that this result is not necessarily coevolution, in the strict sense of reciprocal natural selection between the aphids and the trees. The aphids seem to have adapted to their host plant, but it’s not clear (base on this study, anyway) that the aphids exert significant selection on the plant in return.

Reference:
Ramirez, C. C., B. Lavandero, and M. Archetti. 2008. Coevolution and the adaptive value of autumn tree colours: colour preference and growth rates of a southern beech aphid. Journal of Evolutionary Biology 21:49-56.