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

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. ◼


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

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

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

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. ◼


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

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. ◼


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

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.


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

Snake-eating opossums have evolved venom-resistant blood

The humble Virginia opossum can shrug off snakebites that would kill larger mammals. Photo by TexasEagle.

ResearchBlogging.orgIf you were going to pick the traits of a single animal to confer on a superhero, you probably wouldn’t pick the Virginia opossum. Possums are ubiquitous, scruffy, ratlike marsupials, their toothy grins giving the not entirely inaccurate impression that they don’t have much going on upstairs. Until recently, the nicest thing I could think to say about them is that they eat a lot of ticks.

Blood-sucking Lyme disease vectors are only a small part of the opossum’s eclectic diet, however. They also eat quite a few poisonous snakes, and this has apparently led them to evolve a trait I could call a superpower without exaggeration: opossum blood is resistant to snake venom.

This curious and useful ability was first documented by J.A. Kilmon in a 1976 paper [$a], in which Kilmon reported field observations and laboratory trials showing that opossums tolerate snakebites without visible ill effect. (If animal experimentation makes you queasy, you might want to go read something else about now. Perhaps a nice post about gerbils?)

A natural bite was observed in the field by a 160 cm eastern diamondback on an adult opossum, Didelphis virginiana. The opossum displayed no apparent distress and this suggested a remarkable tolerance by that animal to envenomation. In order to ascertain if an actual envenomation did take place, Mr. Seashole conducted field experiments by manually causing snakes to inflict actual bites on captured opossums. None of the bites caused visible signs of distress to the opossums.

Kilmon brought possums back to the lab, anesthetized them, hooked them up to heart monitors, and “inflicted” bites on them from diamondback and timber rattlesnakes, water moccasins, and at least one cobra. (Kilmon reports he used 15 snakes in total, but doesn’t break that number down by species.) “None of the five opossums,” he wrote, “developed observable local reactions other than trauma attributable to fang penetration and none developed observable systemic effect, exhibiting negligible alteration of heart rate and respiration.”

A timber rattlesnake—no big deal to an opossum. Photo by Tom Sprinker.

Finally Kilmon injected an anesthetized opossum with enough water moccasin venom to kill five fifteen-kilogram dogs, and observed no reaction beyond a brief drop in blood pressure and small spike in pulse rate—when the possum awoke, it was “apparently healthy.” Upon sacrificing and dissecting the animal, Kilmon found no evidence of organ damage.

Kilmon concludes his brief scientific report with a weird aside about the evolutionary history of opossums, which, had he been writing in 2011, would have made me think his research consisted mainly of skimming the Wikipedia entry for Didelphis virginiana. In the course of reporting the opossum’s taxonomic affiliations and known diet, Kilmon notes offhandedly,

This polyprotodont marsupial is a primitive but also very successful mammal. The opossums of varying species are the only marsupials surviving in the placental world, the predominant marsupial and monotreme mammals of Australia having probably survived due to their isolation. The opossum has remained unchanged for millions of years and probably reached his peak of evolutionary specialization several millions of years ago.

I don’t think he could’ve gotten away with that last sentence in an evolutionary biology journal. It’s true that the common ancestor of opossums and placental mammals (i.e., us) diverged quite a long time ago, that opossum-like critters are known from the fossil record going back that far, and that many opossum traits are thought to be shared with early mammals. But that doesn’t mean opossums “remained unchanged for millions of years.” The lineage leading to modern opossums has been evolving exactly as long as the lineage leading to modern humans—and if the opossum’s lifestyle hasn’t led it to such evolutionary heights as the wheel, war, New York and so forth, then it also hasn’t left the opossum unchanged.

As it happens, a pretty good illustration of this point is the paper that led me to Kilmon’s morbid little study in the first place. Mammalogists Sharon Jansa and Robert Voss have just published a study of one blood protein that may underlie opossums’ resistance to venom. The venom of pit vipers like rattlesnakes and water moccasins targets the blood clotting system—one of the unpleasant effects of a snake bite is internal hemorrhage. So Jansa and Voss examined the evolution of a venom-targeted clotting protein called von Willebrand Factor, or vWF, comparing it across the entire family of opossums, the didelphidae.

Photo by Maggie Osterberg.

Since the evolutionary origin of the family, the vWF of opossum species that prey on snakes has accumulated more changes than vWF in non-snake-eating species. That’s circumstantial evidence for the effect of natural selection continuously acting on vWF over millions of years. Jansa and Voss picked out several specific changes that are unique to snake-eating opossums, and found that they’re associated with a region of vWF that is known to bind with one of the toxins in pit viper venom.

The authors suggest that opossums may have been engaged in a evolutionary “arms race” against snake venom toxins since they first developed a taste for rattlesnake. In other words, not only is the opossum not unchanged since the early history of mammals, one of the traits that has changed continuously since then may be the very feature that piqued Kilmon’s interest.


Jansa, S., & Voss, R. (2011). Adaptive evolution of the venom-targeted vWF protein in opossums that eat pitvipers. PLoS ONE, 6 (6) DOI: 10.1371/journal.pone.0020997

Kilmon, J., Sr. (1976). High tolerance to snake venom by the Virginia opossum, Didelphis virginiana. Toxicon, 14 (4), 337-40 DOI: 10.1016/0041-0101(76)90032-5

Passive aggression: Parasitic wasp larvae interfere with each other via their host’s host plant

A large white butterfly caterpillar weaves a cocoon around the wasp larvae infesting its body. Photo by EntomoAgricola.

ResearchBlogging.orgI’m embarrassed to admit that I’ve only just gotten around to picking up Carl Zimmer’s book Parasite Rex. It’s turned out to be a wonderful compendium of all the peculiar ways parasites evade, confound, and resist the defenses of their hosts. Some of the wildest cases Zimmer examines, though, are parasites that manipulate their hosts’ behavior.

One grotesque and well-studied example is the wasp Cotesia glomerata. Female C. glomerata wasps inject their eggs into butterfly caterpillars, and when the eggs hatch, the wasp larvae eat the caterpillar from the inside, saving critical organs so the poor thing stays alive the whole time. Then, when the wasp larvae are ready to burrow out of the caterpillar and form pupae to complete their devlopment, they induce the half-dead caterpillar to spin a web around them and stand guard against predators. (In technical language, this life history makes the wasp a parasitoid, rather than a parasite.) Christie Wilcox has written up a fuller description of the whole grisly process, if you want more detail.

That sounds like a pretty incredible set of manipulations for one clutch of wormy-looking wasp larvae, but they’re not all that Cotesia glomerata can do. New evidence published in Ecology Letters suggests that C. glomerata can somehow make the plants that its host caterpillar feeds on less hospitable [$a] to the larvae of another caterpillar-infesting wasp. In other words, the wasp larvae may manipulate not just their host, but their host’s host.

First off, here’s video of Cotesia glomerata in action. Don’t watch this on your lunch break.

Now, the wasp’s plant manipulations. Lots of plants have what are called induced defenses against herbivores like the butterfly larvae that host C. glomerata larvae. Induced defenses are usually protective toxins that plants produce in response to herbivore damage [PDF]. Erik Poelman and his collaborators reasoned that, since C. glomerata can manipulate it’s host’s behavior, the parasites might change how plants respond to herbivory by infested caterpillars.

To test this, the team first had to induce plant responses. They grew Brassica oleracea—Brussels sprouts—plants in the greenhouse, then infested them with either un-parasitized caterpillars of the cabbage white butterfly Pieris rapae, cabbage white caterpillars infected with Cotesia glomerata, or cabbage white caterpillars infected with larvae of the related wasp C. rubecula. Once the caterpillars had nibbled on the plants enough to induce defensive responses, Poelman et al. removed the caterpillars in preparation for the experiment proper.

The team then introduced parasitoid-free caterpillars and caterpillars infested with one or the other parasitoid species onto host plants that had been through one of the three induction treatments, or that had never been exposed to herbivores. They then tracked the development of the caterpillars, and whether or not the wasp larvae inside them survived.

A healthy cabbage white butterfly caterpillar feeds on a piece of broccoli stem. Photo by Sam Fraser-Smith.

Larvae of C. rubecula fared more-or-less equally well no matter what kind of plant their host caterpillar fed on. But C. glomerata larvae had substantially higher mortality when their hosts fed on plants induced by caterpillars infested with the competitor species. While about 50 percent of C. glomerata larvae died if their hosts fed on plants induced by uninfested caterpillars or caterpillars infested with C. glomerata, almost 75 percent of C. glomerata larvae died when their hosts fed on plants that had previously been occupied by caterpillars infested with C. rubecula.

This impact isn’t because the host caterpillars fared poorly—in fact, caterpillars developed a little faster on plants induced by rubecula-infested caterpillars. So somehow, Cotesia rubecula seems to have influenced its hosts in a way that makes their host plants less hospitable to C. glomerata.

Poelman et al. are scrupulous to point out that this effect might not be anywhere nearly as strong in nature—host plants and host caterpillars might be plentiful enough that Cotesia glomerata can simply avoid the competitor species. On top of that, any natural selection that C. rubecula could be exerting on C. glomerata via induced responses in their shared hosts’ host plants is occurring at multiple removes. The effect Poelman et al. documented is probably not an adaptation for competition with C. glomerata so much as a side effect of C. rubecula‘s effect on its host.

So although this result shows that one parasitoid wasp can reach out and influence another through three other organisms—its own host, that host’s host plant, and the other wasp’s host—it’s not clear how strong that impact has been over the evolutionary history of these two Cotesia species. That said, this is a pretty nifty proof-of-concept.


Agrawal, A., Conner, J., Johnson, M., & Wallsgrove, R. (2002). Ecological genetics of an induced plant defense against herbivores: Additive genetic variance and costs of phenotypic plasticity. Evolution, 56 (11), 2206-2213 DOI: 10.1111/j.0014-3820.2002.tb00145.x

Poelman, E., Gols, R., Snoeren, T., Muru, D., Smid, H., & Dicke, M. (2011). Indirect plant-mediated interactions among parasitoid larvae. Ecology Letters DOI: 10.1111/j.1461-0248.2011.01629.x

Pesticides and parasites add up to an evolutionary Catch-22

When Daphnia evolve resistance to pesticides, they become more vulnerable to bacterial parasites. Photo by Chantal Wagner.

ResearchBlogging.orgIf you haven’t read Joseph Heller’s classic Catch-22, cancel your plans for next weekend and spend the time with a copy from the nearest library. It’s a hilarious, bracingly bleak satire of military bureaucracy, as epitomized in the titular clause governing when bomber pilots can be grounded for reason of insanity:

There was only one catch and that was Catch-22, which specified that a concern for one’s safety in the face of dangers that were real and immediate was the process of a rational mind. Orr was crazy and could be grounded. All he had to do was ask; and as soon as he did, he would no longer be crazy and would have to fly more missions.

Heller conceived Catch-22 as a product of malicious middle management, but a similar situation crops up in the natural world when living things are under natural selection from conditions that favor contradictory traits. Biologists most commonly call these tradeoffs.

Over the course of evolution, tradeoffs set up “choices” that natural selection must make—a population can adapt to one alternative set of conditions, or another, or settle on a middle ground. A trivial example is that elephants have long ago “chosen” not to fly (Dumbo notwithstanding) in the course of evolving large, un-aerodynamic bodies suitable for massive-scale herbivory. A more relevant example is a new finding that the evolution of pesticide resistance creates vulnerability to parasites [$a].

The US Environmental Protection Agency estimated [PDF] that in 2006 and 2007 (the latest years for which reports are online) we used upwards of five billion pounds of pesticides to kill unwanted plants, insects, fungi, and other organisms worldwide. Once they’re sprayed, we don’t have much control over where pesticides end up—rain runoff takes them into lakes, ponds, and the ocean. In those bodies of water, critters at the base of the food chain are the first to feel the effects—critters like the tiny, translucent crustacean Daphnia magna.

Of course, those critters may be able to evolve resistance to the pesticides contaminating their environment—but that resistance may come at a cost.

Pesticide application, via the most picturesque method available. Photo by Scott Butner.

Anja Coors and Luc De Meester had already found a hint of this cost [$a] in an experiment using a single clonal line of Daphnia, in which Daphnia exposed to both sublethal concentrations of the widely-used insecticide carbaryl and a parasitic bacterium fared much worse than Daphnia exposed to only carbaryl or bacteria.

In the new study, Coors, De Meester, and three collaborators expand on that initial observation by determining whether Daphnia become more vulnerable to parasites as they evolve resistance to carbaryl, and whether this costly evolution could occur in natural populations. The coauthors took samples of Daphnia from natural populations in four separate lakes and exposed them to carbaryl over several generations—then sampled the resultant evolved populations and tested their vulnerability to the bacterium. Compared to Daphnia left unexposed to carbaryl, the evolved populations were more resistant to the pesticide—and were also more badly hurt by bacterial infection.

It’s hard to say how general this particular result is to the many, many other species that, like Daphnia, must cope with pesticides and other pollutants humans have introduced into the environment. Evolution to resist one pesticide leads to lowered resistance to infection in one aquatic crustacean; in other species, facing different chemicals, maybe such costs are different or lesser or nonexistent. But living things are not infinitely pliable as they evolve in response to the many and rapid changes we’re making in the world. To slow the extinction crisis going on around us, we need to avoid trapping other living things in Catch-22.


Coors, A., & De Meester, L. (2008). Synergistic, antagonistic and additive effects of multiple stressors: predation threat, parasitism and pesticide exposure in Daphnia magna.Journal of Applied Ecology, 45 (6), 1820-8 DOI: 10.1111/j.1365-2664.2008.01566.x

Jansen, M., Stoks, R., Coors, A., van Doorslaer, W., & de Meester, L. (2011). Collateral damage: Rapid exposure-induced evolution of pesticide resistance leads to increased susceptibility to parasites. Evolution DOI: 10.1111/j.1558-5646.2011.01331.x

What’s in that dissertation, anyway?

About to take the plunge. Photo by jby.

So, what with getting my sparrows in a row for my dissertation defense on Friday, I haven’t written any new science post for this week. But! As it happens, I have written about most of the component chapters of my dissertation—so in lieu of something new this week, why not check out those posts?

  • The first chapter of my dissertation is a literature review about the phenomenon ecologists call ecological opportunity, and how it may or may not explain big, rapid evolutionary changes. I’ve also written about this topic for the Scientific American guest blog.
  • The second chapter uses phylogenetic methods to reconstruct what yucca moths were like before they were yucca moths.
  • The third chapter presents a mathematical model of coevolution between two species, and determines what kind of interactions—predation, parasitism, mutualism, competition—can cause those species to evolve greater diversity.
  • The fourth chapter is the latest work on my lab’s big study of Joshua trees and their pollinators. The material I’m including in this chapter hasn’t been reviewed and published yet, but you can read the most recent Joshua tree post to learn what we know so far, and what kinds of questions we still want to answer.

Regular posting resumes next week, provided that I pass my defense and the celebrating afterward doesn’t interfere with my blogging capacity.