A red milkweed beetle, Tetraopes tertophthalmus, on its host plant (jby)
A new paper from the lab — coauthored with all three of the Yoder Lab’s graduate student alumni — is now online ahead of print in the journal Evolution Letters. In it, we analyze population genetic data from 20 pairs of plants and herbivores, parasites, and mutualists that live intimately on those plants to test for evidence that the associate species’ population genetic structure aligns with that of their host plants. This is an expected result if adaptation to the host plant drives diversification of the associates — and we found that it is indeed a recurring pattern. This is a pretty neat result, and, I think, a nice contribution to a long-established literature on how intimate associations with plants has driven the diversification of groups like butterflies and beetles.
A large white butterfly caterpillar weaves a cocoon around the wasp larvae infesting its body. Photo by EntomoAgricola.
I’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.
Reference
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
In natural communities, each species is embedded in a web of interactions with other species—predators, prey, competitors, mutualists, and parasites. The effects of all these other species combine in complex, unpredictable ways. I recently discussed a study of protozoans living inside pitcher plants that found predators and competitors can cancel out each others’ evolutionary effects. Now another study finds that parasites and predators can interact to make desert-living gerbils adopt less effective foraging strategies [$a].
Allenby’s gerbil is a small desert rodent native to Israel’s Negev Desert. They make a living foraging for seeds, which might seem simple enough—but for small desert mammals, it’s a constant balancing act. Foraging requires continuously judging how profitable it is to continue gathering seeds in one spot compared to looking for another, maybe better, spot; and all the while watching out for predators.
The red fox—a major threat if you’re a tiny rodent, but hard to watch for when you’re scratching fleas all the time. Photo by HyperViper.
For small mammals, parasites like fleas can impose a real physiological cost—but they might also cause irritation that interfere with effective foraging. This idea led a group of Israeli reserachers to experimentally infest captive gerbils with fleas, and release them into an enclosure with a red fox.
It’s okay—the fox was muzzled! The research group was interested in how effectively the gerbils foraged in standardized patches of resources (trays of seed mixed with sand) in the presence of predators, and how being flea-ridden changed that foraging behavior. As metrics of foraging efficiency, they recorded how rapidly the gerbils gave up foraging in a single tray before moving on to another, which approximates how many seeds they left behind.
With no fleas, gerbils spent slightly—but not significantly—less time foraging in a single tray when a fox was in the enclosure with them. But gerbils infested with fleas moved on to a new tray substantially faster in the presence of a fox, leaving behind more seeds in the process. The study’s authors suggest that this is because the irritation caused by fleas distracted the gerbils too much to keep watch for a predator and forage at the same time—so flea-ridden gerbils made up for being less watchful by moving between patches of resources more rapidly.
So for gerbils, the presence of a second, different kind of antagonist amplifies the effects of a nearby predator. Fleas and foxes aren’t just a double whammy—the effects of both together are worse than the sum of each individually.
Reference
Raveh, A., Kotler, B., Abramsky, Z., & Krasnov, B. (2010). Driven to distraction: detecting the hidden costs of flea parasitism through foraging behaviour in gerbils. Ecology Letters DOI: 10.1111/j.1461-0248.2010.01549.x
In epidemiology the importance of ecological and evolutionary processes comes into sharp relief: questions about the networks of interactions between species in a community, or about the evolution of parasite specificity, virulence, and contagiousness have immediate implications for human health, as well as in animal husbandry and conservation. One of the most basic of these questions is, what determines the community of parasites that infect a species? One answer is in this month’s issue of The American Naturalist, where a neat meta-analysis shows that the size of mammals’ home ranges shapes the number of parasite species they attract [$-a].
For mammals, we already know that parasite communities are shaped by the host’s body size, geographical range, and population density. In this new study, Bordes et al. propose another factor: the host’s home range, the area that a single individual occupies. There are two major ways that home range might shape the diversity of parasites infecting host. Greater home range could mean that the host encounters a broader array of habitats, and opportunities for infection, so that home range and parasite diversity are positively correlated. Alternatively, hosts with smaller home ranges effectively live at higher density, which should create more opportunities for parasite transmission between hosts, generating a negative correlation between home range and parasite diversity.
Bordes et al. test these hypotheses by collecting published studies of the number of parasitic worm (helminth) species infecting mammals, and then performing regressions (corrected for phylogenetic relationships between host species) of parasite species richness on a variety of possible causal factors, including home range. They find that host home range is a stronger predictor of parasite species diversity than host body size, and that home range is negatively correlated with parasite diversity.
In a way, then, this result confirms the importance of host density in host-parasite interactions. But it’s not an obvious outcome – it is intuitive that more densely populated hosts should be more susceptible to parasitism in general, but not that they should also be attacked by a wider array of parasites. Maybe dense host populations are more productive habitat to parasites, so that there’s ecological “space” to support a greater diversity of parasites. Or maybe these dynamics are a result of the specific biology of helminth parasites, many of which have different hosts for different parts of their life cycle.
Reference
F. Bordes, S. Morand, D.A. Kelt, D.H. Van Vuren (2009). Home range and parasite diversity in mammals The American Naturalist, 173 (4), 467-74 DOI: 10.1086/597227
