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Community interactions govern host-switching with implications for host-parasite coevolutionary history.

ABSTRACT: Reciprocal selective effects between coevolving species are often influenced by interactions with the broader ecological community. Community-level interactions may also influence macroevolutionary patterns of coevolution, such as cospeciation, but this hypothesis has received little attention. We studied two groups of ecologically similar feather lice (Phthiraptera: Ischnocera) that differ in their patterns of association with a single group of hosts. The two groups, "body lice" and "wing lice," are both parasites of pigeons and doves (Columbiformes). Body lice are more host-specific and show greater population genetic structure than wing lice. The macroevolutionary history of body lice also parallels that of their columbiform hosts more closely than does the evolutionary history of wing lice. The closer association of body lice with hosts, compared with wing lice, can be explained if body lice are less capable of switching hosts than wing lice. Wing lice sometimes disperse phoretically on parasitic flies (Diptera: Hippoboscidae), but body lice seldom engage in this behavior. We tested the hypothesis that wing lice switch host species more often than body lice, and that the difference is governed by phoresis. Our results show that, where flies are present, wing lice switch to novel host species in sufficient numbers to establish viable populations on the new host. Body lice do not switch hosts, even where flies are present. Thus, differences in the coevolutionary history of wing and body lice can be explained by differences in host-switching, mediated by a member of the broader parasite community.

SUBMITTER: Harbison CW

PROVIDER: S-EPMC3111282 | biostudies-literature | 2011 Jun

REPOSITORIES: biostudies-literature

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Community interactions govern host-switching with implications for host-parasite coevolutionary history.

Harbison Christopher W CW Clayton Dale H DH

Proceedings of the National Academy of Sciences of the United States of America 20110523 23

Reciprocal selective effects between coevolving species are often influenced by interactions with the broader ecological community. Community-level interactions may also influence macroevolutionary patterns of coevolution, such as cospeciation, but this hypothesis has received little attention. We studied two groups of ecologically similar feather lice (Phthiraptera: Ischnocera) that differ in their patterns of association with a single group of hosts. The two groups, "body lice" and "wing lice, ...[more]

PMID: 21606369

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Project description:There is a long-standing interest in understanding host-parasite coevolutionary dynamics and associated fitness effects. Increasing amounts of genomic data for both interacting species offer a promising source to identify candidate loci and to infer the main parameters of the past coevolutionary history. However, so far no method exists to perform the latter. By coupling a gene-for-gene model with coalescent simulations, we first show that three types of biological costs, namely, resistance, infectivity and infection, define the allele frequencies at the internal equilibrium point of the coevolution model. These in return determine the strength of selective signatures at the coevolving host and parasite loci. We apply an Approximate Bayesian Computation (ABC) approach on simulated datasets to infer these costs by jointly integrating host and parasite polymorphism data at the coevolving loci. To control for the effect of genetic drift on coevolutionary dynamics, we assume that 10 or 30 repetitions are available from controlled experiments or several natural populations. We study two scenarios: 1) the cost of infection and population sizes (host and parasite) are unknown while costs of infectivity and resistance are known, and 2) all three costs are unknown while populations sizes are known. Using the ABC model choice procedure, we show that for both scenarios, we can distinguish with high accuracy pairs of coevolving host and parasite loci from pairs of neutrally evolving loci, though the statistical power decreases with higher cost of infection. The accuracy of parameter inference is high under both scenarios especially when using both host and parasite data because parasite polymorphism data do inform on costs applying to the host and vice-versa. As the false positive rate to detect pairs of genes under coevolution is small, we suggest that our method complements recently developed methods to identify host and parasite candidate loci for functional studies.

Dataset Information

Community interactions govern host-switching with implications for host-parasite coevolutionary history.

Publications

Community interactions govern host-switching with implications for host-parasite coevolutionary history.

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