Parasite mediated homogenizing selection at the MHC in guppies

Abstract

Understanding the selective forces influencing genetic diversity is a fundamental goal of evolutionary ecology. The genes of the major histocompatibility complex (MHC) play a key role in the adaptive immune response of vertebrates and thus provide an excellent opportunity to examine the agents of selection on a functionally important gene. Here we examine the genetic architecture of the MHC class IIB genes in 10 wild populations of guppies (Poecilia reticulata) in Northern Trinidad. We have previously shown that these populations are significantly less diverged at the class IIB locus than expected based on neutral (microsatellite) loci. We now survey infection by Gyrodactylus turnbulli and G. bullatarudis, common parasitic worms that infect guppies, as a potential agent of homogenizing selection. We used a genetic algorithm to partition both additive and non-additive genetic effects of the five most common MHC allele types as well as a rare allele category. Although we found no evidence for non-additive effects, across the populations we found that one allele type (the a-type) had a significant negative additive effect on parasite load. Thus, individuals who had more copies of the a-type allele were infected with fewer gyrodactylus than individuals with fewer copies of the allele. These results not only link parasite infection with MHC genotype, they provide a mechanism of homogenizing selection across these otherwise disparate populations.

Testing for local host–parasite adaptation: an experiment with Gyrodactylus ectoparasites and guppy hosts

“…Yet another possible explanation is that guppies are leading the ''arms race'' and have become locally adapted to their sympatric parasites. Previous work has suggested that guppies from the Paria River, with common MHC alleles, have lower Gyrodactylus infection levels in the laboratory (Fraser and Neff, 2009), with similar observations in the wild , suggesting that, indeed, guppies could be locally adapted to their sympatric Gyrodactylus.…”

“…Infections by Gyrodactylus can cause high guppy mortality in the laboratory (Scott and Anderson, 1984;van Oosterhout et al, 2003;Cable and van Oosterhout, 2007a,b) and in nature (van Oosterhout et al, 2007). Not surprisingly, then, some evidence exists that guppy populations have evolved in response to Gyrodactylus, particularly through variation in the immune response (van Oosterhout et al, 2003) and at loci of the Major Histocompatibility Complex (MHC) (Fraser and Neff, 2009;Fraser et al, 2010).…”

Parasite diversity, patterns of MHC II variation and olfactory based mate choice in diverging three-spined stickleback ecotypes

“…Differences in MHC allele pools between populations have already been proposed while associated data on contrasting parasite communities is scarce (but see, Blais et al 2007;Bonneaud et al 2006). As mentioned previously, this pattern could theoretically arise from genetic drift, however, the likelihood that both rivers (as both lakes) evolved by chance independently in the same direction, seems rather low without invoking habitatspecific homogenizing selection (Frazer and Neff 2010). Thus, under a ''one event of colonization hypothesis'', (Reusch et al 2001b), a plausible scenario might be: genetic drift has acted on populations' divergence but similar parasite pressure slowed down divergence at MHC genes within habitat type.…”

Experimental evolution of parasite resistance in wild guppies: natural and multifarious selection

“…Similarly, guppies introduced from the Yarra River high-predation site into the previously guppy-free Damier River remained infected in the high-predation reach (prevalence 16%) but not the low-predation reach [6]. Finally, the low-predation population of the Guanapo River (upstream from the ancestral source population but downstream from the introduced populations) was Gyrodactylus-free before and during the experiment [6,7]. In short, populations introduced from high-to low-predation sites, either by colonization or by translocation seem to repeatedly evolve increased resistance to Gyrodactylus parasites, a pattern inconsistent with traditional ideas but that we were able to experimentally confirm.…”

“…In particular, low-predation guppies have lower Gyrodactylus loads than do high-predation guppies [6] and previous field introductions from Gyrodactylus-present sources (which did not report any anti-parasite treatments), all have no presence of Gyrodactylus (exception El Cedroprevalence 1.4%) [6], which confirms a general higher resistance to parasitism in low-predation populations. Moreover, the high frequency of an MHC allele [7] that correlates negatively with Gyrodactylus load [8] is retained in these populations. Even more directly, the historic Turure introduction used an ancestral population from the same site as we did (Guanapo source) over 60 years ago, and these fish remain Gyrodactylus-free [6,7].…”