Category Archives: coevolution

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

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Joshua tree, diverged. Photo by jby.

Cross-posted from Nothing in Biology Makes Sense!

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

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

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

Joshua trees, diverged. Photo by jby.

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

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

Installing a Joshua tree chastity device. Photo by jby.

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

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

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

Camp Tikaboo, 2012 edition. Photo by jby.

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

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

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

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

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

References

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

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

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

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

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Photo by Thomas Hawk.

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

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

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

In flour beetles, coevolution mixes things up

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A red flour beetle. Photo via Wikimedia Commons.

Cross-posted from Nothing in Biology Makes Sense.

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

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

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

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

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

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

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

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

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

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

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

References

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

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

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

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

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

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

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

Can’t keep us apart: Brood parasitic birds have specialized on the same hosts for millions of years

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A male greater honeyguide. Photo via Safari Ecology.

ResearchBlogging.orgBrood parasitic birds lay their eggs in other birds’ nests, a lazy approach to parenting that shapes the behavior and evolution of brood parasites in all sorts of interesting ways.

Brood parasite chicks often kill their adoptive nestmates, and can grow up confused about their species identity. To better trick their hosts into accepting “donated” eggs, many brood parasites have evolved eggs that mimic the hosts’—and some hosts have evolved contrasting eggs in response. A recent genetic study now shows an even subtler pattern arising from this host-parasite coevolutionary chase: lines of parasitic females that have specialized on the same host species for millions of years.

The brood parasite in question is the greater honeyguide, an African bird best known for helping people find bee colonies (though the story that honeyguides also guide honey badgers don’t have much factual basis). However, honeyguide females also lay their eggs in the nests of several host species—including hoopoes, greater scimitarbills, green woodhoopoes, little bee-eaters, and striped kingfishers. Although the honeyguides’ eggs aren’t colored like their hosts’, they do have matching shapes—the hosts all nest in tree cavities, where lighting is too poor to notice a mis-colored egg, but an oversized or oddly shaped one would stand out.

A hoopoe, one of the birds that “adopts” greater honeyguide eggs. Photo by Hiyashi Haka.

There’s an evolutionary catch, though: hoopoes, scimitarbills, and woodhoopoes lay oblong eggs, while the bee-eaters and kingfishers lay spherical eggs. Yet honeyguide females manage to lay eggs of matching shape and size in the nest of each host. Individual brood parasites can’t adjust the shapes of their eggs to match those in a host nest—they find hosts with eggs that will match their own.

How do they do it? Maybe each female honeyguide actually goes looking for nests like the one she grew up in, either because she is compelled to by some genetic instinct, or because she learns to recognize a potential host in the course of being raised by that host. Or maybe the host birds are so good at recognizing and rejecting oddly-shaped parasite eggs that only well-matched eggs make it to adulthood. Any of these processes could result in long lineages of female honeyguides laying eggs in the nests of the same host species their mothers, grandmothers, and great-grandmothers used. This is precisely the pattern Claire Spottiswoode and her coauthors found in the population genetics of greater honeyguides.

Spottiswoode et al. collected genetic data from honeyguides using all five of the host species mentioned above, and compared the patterns of relatedness from different genetic markers to patterns of host use. The pattern of differentiation in a marker from the mitochondrial genome—genes contained in the mitochondria, which mothers pass on to their offspring but fathers do not—neatly divides the honeyguides between hosts with oblong eggs and the hosts with spherical eggs. By applying a molecular clock to the mitochondrial data, the team found that the division between oblong-egg and spherical-egg honeyguides dates back as long as 3 million years ago. So honeyguide females have been tracking the same hosts, or very similar ones, for quite some time!

However, no such pattern is evident in four genetic markers from the nuclear genome, which is inherited via both parents. That suggests male honeyguides don’t discriminate among females based on host fidelity—mates pair off regardless of what host species they each grew up with. Spottiswoode et al. also note that this result hints at how honeyguide egg characteristics and host preferences could be inherited: via the female sex chromosome. In birds, biological sex is determined by the Z and W chromosomes—individuals with two Z chromosomes develop as males, and individuals with a Z and a W chromosome develop as females. Host preferences and egg shape inherited via the W chromosome would then be carried only by females.

However, the data presented here don’t directly test the W-chromosome hypothesis. That would require markers—or better yet complete sequence data—from the W chromosome itself, and (to be really thorough) lots more markers from the rest of the nuclear genome as well. That’s a lot of genetic data to collect, but we are very close to the day when such data are easily collectible. ◼

Reference

Spottiswoode, C., Stryjewski, K., Quader, S., Colebrook-Robjent, J., & Sorenson, M. (2011). Ancient host specificity within a single species of brood parasitic bird. Proc. Nat. Acad. Sciences USA, 108 (43), 17738-42 DOI: 10.1073/pnas.1109630108

Nothing in Biology Makes Sense: Timing is everything

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A euglossine bee gathers scent compounds inside an orchid. Photo by Alex Popovkin, Russian in Brazil.

This week at Nothing in Biology Makes Sense, the big science post comes from … me. It’s about a big new study of orchids and the perfume-collecting euglossine bees that pollinate them.

The study by a team out of Harvard—lead-authored by Santiago R. Ramírez—tests three predictions arising from the proposition that bees and orchids are equally dependent on the scent-collection mutualism. First, as I noted above, a mutually-dependent relationship should mean that bee and orchid species often form in tandem, and that the euglossine bees and the orchids have spent most of their histories together. Second, the euglossines should rely mainly on scents from orchids, not from other sources. Finally, euglossines and orchids should show similar degrees of dependency. An orchid that relies on only one bee species should use a bee species that only collects scent from that one orchid; bees that collect scent from multiple orchids should use orchids that are, themselves, involved with multiple bee species.

To find out whether or not these predictions are borne out, go read the whole post. ◼

Nothing in Biology Makes Sense: Two parasites, one host

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Daphnia, a water flea. Photo via Nothing in Biology Makes Sense!.

This week at Nothing in Biology Makes Sense!, the still shiny new collaborative science blog, contributor Devin Drown describes what happens when two different parasite species infect the same water flea.

Octosporea bayeri needs the host to produce offspring for vertical transmission, that is the host and parasite have an aligned interest in producing offspring. On the other hand, Pasteuria ramosa is using host resources, including the reproductive tissues, to produce spores for infecting other hosts. Because of the alignment of interests between host and the vertically transmitting parasite, the question becomes: does infection by O. bayeri provide host protection from future infection by P. ramosa?

The answer, of course, is in the full post. ◼

The joy of sex (well, one, anyway): Fewer parasites

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Natural selection does not necessarily love sex. Photo by xcode.

Hey, don’t knock [selfing]! It’s sex with someone I love.
—Woody Allen, in Annie Hall

Sex is a puzzle to evolutionary biologists. I don’t mean that we’re socially awkward—I mean that sexual reproduction, which involves mixing your genes with someone else’s to produce one or more children, seems to be at odds with natural selection. Every child produced by sexual reproduction carries only half the genetic material of each of her parents; but parents who can make children without sex pass on all their genes to every child.

Over time, individuals who can make babies without sex should become more common in the population than individuals who have to have sex to reproduce, simply because every baby produced without sex “counts” twice as much for its parent. We know of cases (for instance, stick insects) where asexual reproduction has apparently evolved and spread multiple times.

And yet, not only is sexual reproduction widespread in the natural world, there are many species of living things in which some individuals reproduce sexually and some reproduce without sex, and the two types coexist more-or-less stably. This is particularly common in plants, but it’s also seen in lots of other taxa. That suggests there must be something useful about sexual reproduction that offsets the cost associated with making only half a copy of your genome for every child you have.

One popular hypothesis is that sexual reproduction helps generate new combinations of genes to fight parasites and diseases—this is called the Red Queen Hypothesis, after the character in Through the Looking-Glass who tells Alice that “… it takes all the running you can do, to keep in the same place.” Sex, the thinking goes, means that your children are more likely to have new parasite-fighting gene combinations, and that populations can “run faster” in the coevolutionary race against parasites. And now, a new study in a population of peculiar little fish provides some reasonably direct evidence [$a] for that proposed benefit of sex.

A mangrove killifish. Photo via USGS, used under fair use rationale.

The mangrove killifish, Rivulus marmoratus, leads a pretty remarkable life even before you consider its reproductive strategy. Mangrove killifish live in coastal mangrove swamps, where they must contend with changes in water salinity and water level—and they deal with dry spells by packing into hollows in mangrove tree trunks. Jammed together in a hollow log, the killifish can survive up to two months entirely out of water.

They’re also one of very few vertebrate species known to be able to reproduce asexually. Most mangrove killifish are hermaphrodites, capable of making both eggs and sperm and combining them—or “selfing”—to lay fertilized eggs. A few killifish develop as “pure” males instead, capable of producing only sperm, and therefore only capable of sexual reproduction. Why that small fraction of males persists in killifish populations is probably related to the selective costs and benefits of sex, both for mangrove killifish and for living things in general.

The Red Queen hypothesis predicts that sex is beneficial because it creates new combinations of genes, which in turn lead to greater parasite resistance. Therefore, if killifish produced by sexual reproduction should have more diverse genomes, and are better able to resist parasites than killifish who only have one hermaphroditic parent, then the Red Queen may be the reason why male killifish haven’t gone the way of the dodo.

This is what Amy Ellison and her coauthors found in a population of mangrove killifish from four sites in Belize. They collected killifish and took their genetic fingerprints to identify individuals that were most likely descended from a single selfing lineage, or those that carried genes from multiple lineages. They also checked each fish for infection by three major groups of parasites—bacteria, a common protozoan parasite of killifish, and parasitic worms.

Their total sample size is a bit small, but the team found a pattern generally quite consistent with the Red Queen. Fish descended from sexually-reproducing parents were more likely to be heterozygous—to carry two different forms of a gene—than fish descended from asexual lines. More importantly, fish descended from sexually-reproducing parents also generally had fewer parasites of all three classes, and were generally less likely to carry any protozoans or worms, than those descended from hermaphrodites. That’s consistent with the Red Queen, and it shows the perfectly good selective “reason” for a hermaphrodite to mate with a “pure” male—even though the hermaphrodite is giving up half the selective benefit of the offspring thus produced, those offspring are more likely to be healthy.

A broader prediction that follows from these results is that mangrove killifish populations with higher rates of parasite attack should have more males, or at least more individuals with two parents. What would really be cool, though, is if hermaphroditic killifish can respond to parasite infections by choosing to reproduce sexually—self-medicating, like monarch butterflies, but with sex instead of a toxic host plant. It’s been observed that the hermaphroditic nematode worm Caenorhabditis elegans responds to environmental stress by giving birth to more male offspring, but I know of no such result in a vertebrate. ◼

Reference

Ellison, A., Cable, J., & Consuegra, S. (2011). Best of both worlds? Association between outcrossing and parasite loads in a selfing fish. Evolution, 65 (10), 3021-6 DOI: 10.1111/j.1558-5646.2011.01354.x

Making themselves at home: Spider mites disable plant defenses, then spin their own

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Tomatoes, one of many plants that play unwilling host to red spider mites. Photo by sylvar.

ResearchBlogging.orgPlant-eating insects must overcome some of the cleverest weaponry in the living world—from poisonous latex to sticky hairs—just to find a meal or a place to lay eggs. Many deal with their host plants’ toxic defenses by digesting them or sequestering them safely for personal use, but the red spider mite Tetranychus evansi simply turns them off.

Tetranychus evansi eats a wide range of plants, from tomatoes to potatoes. One female mite can eat enough to lay 50%-70% of her weight in eggs every day, and while that isn’t much on the scale of a single, miniscule red mite, it adds up quickly when colonies build into dense clusters on host plants, sucking them dry and covering them in webs of spun silk.

Most host plants respond to such an onslaught by ramping up production of chemicals that make them unpalatable to herbivores, or that interfere with the mites’ ability to digest plant tissue. However, a team of Dutch and Brazilian biologists recently found that T. evansi somehow short-circuits this response [$a].

The team, whose senior author is the Dutch biologist Arne Jannsen, discovered that mites raised on leaf tissue from tomato plants previously attacked by T. evansi survived longer and laid more eggs than mites raised on tissue from plants that had never been attacked. Analsyis of RNA from tomato leaves attacked by the mites revealed that they were producing fewer of the signalling proteins associated with responding to insect damage than leaves damaged by another, related mite species—and one protein was produced at lower rates than in undamaged leaves!

Mites, up close. Photo via AgroLink.

In other words, the mites were not just preventing the host plant from boosting its defences in response to a mite attack—they were suppressing the defenses below what they would be without an immediate threat. Like a burglar cutting the power to a home security system, T. evansi can somehow prompt a hostile host to become more hospitable.

This raises another problem, however. With its defenses down, the host plant is also more hospitable to other insect herbivores, which could reduce the plant’s value to T. evansi, or even activate the alarms the mites have managed to suppress. A second study by the same team suggests that this may be part of the function of the webs T. evansi spins as it consumes its host.

In this second round of experiments, the group returned to the closely related mite Tetranychus urticae, which was used to stimulate plant defenses in the first study. Earlier work had found that some strains of T. urticae can tolerate or suppress host plant defenses [$a], though not nearly as effectively as T. evansi. That earlier work found that non-suppressing mite strains could benefit from living on the same plant as a suppressing strain, and the new study first demonstrated that this effect is even stronger when T. urticae shares a plant with T. evansi.

A whole lot of (presumably happy) mites. Photo via AgroLink.

In contrast, T. evansi colonies fared worse in the presence of the non-suppressing mites, whether fed leaves that had already been attacked by T. urticae, or placed on a mite-free leaf of a plant with another leaf infested by the non-suppressing species. All else being equal, T. urticae benefits from the defense-suppressing activity of T. evansi, but reduces the value of the host plant to T. evansi.

Faced with this freeloading competitor, T. evansi apparently replaces the disabled plant defenses with webbing. The team found that even though T. urticae thrived when given evansi-chewed tomato leaves, the non-suppressing mites had difficulty colonizing leaves covered in T. evansi webs. Moreover, T. evansi introduced onto a plant with the non-suppressing mites spun more webbing than when introduced onto a mite-free plant; but they didn’t ramp up web-spinning when sharing a plant with another colony of their own species, suggesting that the mites can respond to competition by building up their defenses.

So not only does T. evansi possess the means to turn off its hosts’ biological security system, it erects its own defenses to protect the plant from one competitor that might try to take advantage of the situation. How, exactly, the mites interfere with plants’ defensive responses will be an interesting future line of study. I’d also be very interested to see whether other herbivorous insects—things larger than other mites, and not so easily put off by some silk security fencing—also preferentially attack plants disabled by T. evansi. ◼

References

Kant, M., Sabelis, M., Haring, M., & Schuurink, R. (2008). Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences Proc. Royal Soc. B, 275 (1633), 443-52 DOI: 10.1098/rspb.2007.1277

Sarmento, R., Lemos, F., Dias, C., Kikuchi, W., Rodrigues, J., Pallini, A., Sabelis, M., & Janssen, A. (2011). A herbivorous mite down-regulates plant defence and produces web to exclude competitors. PLoS ONE, 6 (8) DOI: 10.1371/journal.pone.0023757

Sarmento, R., Lemos, F., Bleeker, P., Schuurink, R., Pallini, A., Oliveira, M., Lima, E., Kant, M., Sabelis, M., & Janssen, A. (2011). A herbivore that manipulates plant defence. Ecology Letters, 14 (3), 229-36 DOI: 10.1111/j.1461-0248.2010.01575.x

Choosing your partner is only as helpful as the partners you have to choose from

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Picking teammates. Original photo by humbert15.

ResearchBlogging.orgWhen you need partners for some sort of cooperative activity—say, teammates for a game of kickball—you’d probably like to have a choice among several candidates. That lets you weigh considerations about kicking strength and running speed—and who promised to give you his dessert at lunch period—to build a winning team. However, if the other team captain snaps up the good players first, the fact that you have a choice among the others might not make much difference.

Plants and animals looking for mutualists face a similar situation. Being able to choose among possible partners should allow the chooser to work with helpful partners and avoid unhelpful ones, but a new study suggests that in one widespread mutualism the process of choosing between partners can leave the chooser worse off than if it had no choice at all [$a].

Coauthors Erol Akçay and Ellen Simms focus on the effects of partner choice in the mutualism between plants and nitrogen-fixing bacteria—the interaction I’m studying in my current postdoc position, as it happens. All living things need nitrogen, but only some strains of bacteria are able to collect nitrogen from the atmosphere and “fix” it into a form that other organisms can use. Many plants, particularly members of the big and diverse bean family, have evolved to allow nitrogen-fixing bacteria to infect their roots—the plants form a nodule of root tissue around the infection and supply the tissue with sugar for the bacteria to feed on as they fix nitrogen. Eventually the nodule dries up and dies off, and the bacteria are freed into the soil, having multiplied many times over thanks to the food supply from the host plant.

A plant’s root nodules, some cut open to show the interior. Photo by pennstatelive.

To see how this choice might work in practice, Akçay and Simms construct a mathematical model of a plant with two nodules. Each nodule produces some level of nitrogen, and recieves some level of sugar from the plant. The plant negotiates with the two nodules in what’s called a “war of attrition” game: whichever partner wants a better deal cuts off the exchange of services, and holds out until the cost of losing the service it recieves is greater than the benefit it hopes to gain in the war of attrition.

Rather like ant-defended plants, plants that host nitrogen-fixing bacteria don’t seem to screen potential mutualistic bacteria before allowing them to infect their roots. However, after root nodules are established, the success of the mutualism from the perspective of both partners depends on the genetics of each [PDF], and when host plants receive supplemental nitrogen, they put fewer resources into growing nodules [PDF]. Host plants have been observed with different strains of bacteria in different nodules, and some nodules could contain diligent nitrogen fixers while others are full of freeloaders. This may be the point at which the plant has a choice of partners—it can potentially direct sugar to helpful nodules, and cut off unhelpful ones.

Because the plant has two nodules to choose from, it can potentially outlast an uncooperative nodule by relying on the other one. This works if the plant can shunt more resources to the cooperative nodule and recieve more nitrogen from it in return. However, the success of this strategy depends on two traits of the bacteria inhabiting the nodules—how readily they ramp up nitrogen production in response to more sugar, and how stubborn they are in the war of attrition game.

If both nodules are stubborn but responsive to extra sugar, the plant can negotiate with one nodule by giving the other more sugar and receiving extra nitrogen. This lets the plant hold out longer in the war of attrition. On the other hand, nodules that are not responsive to extra sugar but also not very stubborn yield quickly in the war of attrition even though they don’t help much in negotiations. In either of these two cases, the negotiations find an equilibrium in which the plant receives a benefit about intermediate between what it would recieve if both nodules were infected by the same strain of bacteria.

However, if the plant hosts a stubborn-responsive bacterial strain in one nodule and a yielding-unresponsive strain in the other, it finds itself in a trap: the yielding-unresponsive strain is no help in negotiation against the stubborn-responsive strain, and the help provided by the stubborn-responsive strain isn’t an advantage in negotiating with the yielding-unresponsive strain. Over successive negotiations, the stubborn-responsive strain can ratchet up the sugar it extracts from the plant, and the plant ends up worse off than it would be if the two nodules were identical.

Just like humans haggling in a marketplace, the outcome of the interaction depends strongly on whether the other party plays along as expected.

Akçay and Simms find a way out of this trap by adding another wrinkle to the model. Much like the contract-theory models of mutualism I’ve discussed before, they modify the model to allow cooperative nodules to benefit from being cooperative. This makes a good deal of intuitive sense—if a nodule provides a better deal to the plant, the plant can potentially grow more leaves to produce more sugar, which would allow it to offer a better deal to the bacteria it hosts. Akçay and Simms call this “partner fidelity feedback,” and they find that, if it is sufficiently strong, it can allow the plant to out-negotiate a stubborn strain of bacteria.

Although it has a good deal of intuitive appeal, the model presented by Akçay and Simms does a fair bit of speculating in the absence of data. This is also a problem for the contract-theory model, and really all models of this widespread and important interaction. We know a great deal about the chemical details of plants’ interaction with nitrogen fixing bacteria. However, we don’t have a good sense of whether and how plants can redirect resources among nodules to haggle with the bacteria they host, and we don’t know whether and how bacteria could adjust their behavior to haggle with the plant. Akçay and Simms devote a big section of their online appendix [$a] to discussing just this point.

To figure out what’s going on inside those nodules, we need to determine how different models of interaction between plants and their bacterial mutualists may shape patterns in things that are easier to observe—both in the compatibility between plant genotypes and bacterial strains in greenhouse tests, and in the broader population genetics of both partners.

References

Akçay, E., & Simms, E. (2011). Negotiation, sanctions, and context dependency in the legume-rhizobium mutualism. The American Naturalist, 178 (1), 1-14 DOI: 10.1086/659997

Heath, K. (2010). Intergenomic epistasis and coevolutionary constraint in plants and rhizobia. Evolution DOI: 10.1111/j.1558-5646.2009.00913.x

Heath, K.D., Stock, A.J., & Stinchcombe, J.R. (2010). Mutualism variation in the nodulation response to nitrate Journal of Evolutionary Biology, 23 (11), 2494-2500 DOI: 10.1111/j.1420-9101.2010.02092.x