Sympatric and allopatric divergence of MHC genes in threespine stickleback.

Kerry B. Marchinko,Luke J. Harmon,Jeff Demuth,Blake Matthews,Leithen M'Gonigle,Helmut Schaschl

doi:10.1371/journal.pone.0010948

Abstract

Parasites can strongly affect the evolution of their hosts, but their effects on host diversification are less clear. In theory, contrasting parasite communities in different foraging habitats could generate divergent selection on hosts and promote ecological speciation. Immune systems are costly to maintain, adaptable, and an important component of individual fitness. As a result, immune system genes, such as those of the Major Histocompatability Complex (MHC), can change rapidly in response to parasite-mediated selection. In threespine stickleback (Gasterosteus aculeatus), as well as in other vertebrates, MHC genes have been linked with female mating preference, suggesting that divergent selection acting on MHC genes might influence speciation. Here, we examined genetic variation at MHC Class II loci of sticklebacks from two lakes with a limnetic and benthic species pair, and two lakes with a single species. In both lakes with species pairs, limnetics and benthics differed in their composition of MHC alleles, and limnetics had fewer MHC alleles per individual than benthics. Similar to the limnetics, the allopatric population with a pelagic phenotype had few MHC alleles per individual, suggesting a correlation between MHC genotype and foraging habitat. Using a simulation model we show that the diversity and composition of MHC alleles in a sympatric species pair depends on the amount of assortative mating and on the strength of parasite-mediated selection in adjacent foraging habitats. Our results indicate parallel divergence in the number of MHC alleles between sympatric stickleback species, possibly resulting from the contrasting parasite communities in littoral and pelagic habitats of lakes.

Highlights

Competition and predation are central mechanisms of ecological speciation [1,2], but the role of parasitism in the evolution of host reproductive incompatability is less clear [3,4,5]
We found that the limnetics tended to have lower allelic richness than benthics in both Paxton Lake and Priest Lake (Table 1, ARMHC)
We found that limnetics had lower allelic richness than benthics in both Paxton (t77 = 26.1, pv0.001) and Priest Lake (t42 = 23.4, pv0.001, Table 1, Figure 1)

Summary

Introduction

Competition and predation are central mechanisms of ecological speciation [1,2], but the role of parasitism in the evolution of host reproductive incompatability is less clear [3,4,5]. Theory suggests that speciation is more likely when functional traits [10], such as those underlying ecological performance, are under both divergent natural selection and sexual selection [11]. Such traits have been dubbed ‘magic traits’ [11], and are common elements of sympatric speciation models [5,12]. From an empirical perspective, the role of parasites in host speciation is highly understudied [4], and so the consequences of parasite-mediated selection for host diversification remain uncertain [5,12]

Methods

Results

Conclusion