Abstract
Plague (Yersinia pestis infection) is a highly virulent rodent disease that persists in many natural ecosystems. The black rat (Rattus rattus) is the main host involved in the plague focus of the central highlands of Madagascar. Black rat populations from this area are highly resistant to plague, whereas those from areas in which the disease is absent (low altitude zones of Madagascar) are susceptible. Various lines of evidence suggest a role for the Major Histocompatibility Complex (MHC) in plague resistance. We therefore used the MHC region as a candidate for detecting signatures of plague-mediated selection in Malagasy black rats, by comparing population genetic structures for five MHC-linked microsatellites and neutral markers in two sampling designs. We first compared four pairs of populations, each pair including one population from the plague focus and one from the disease-free zone. Plague-mediated selection was expected to result in greater genetic differentiation between the two zones than expected under neutrality and this was observed for one MHC-class I-linked locus (D20Img2). For this marker as well as for four other MHC-linked loci, a geographic pattern of genetic structure was found at local scale within the plague focus. This pattern would be expected if plague selection pressures were spatially variable. Finally, another MHC-class I-linked locus (D20Rat21) showed evidences of balancing selection, but it seems more likely that this selection would be related to unknown pathogens more widely distributed in Madagascar than plague.
Highlights
Immune genes have been shown to be strongly affected by natural selection [1,2]
Major Histocompatibility Complex (MHC) class III includes a diverse array of structurally unrelated genes, including several involved in innate immunity
Studied loci and within-population analyses Five MHC-linked microsatellite markers designed on the basis of genome sequence of R. norvegicus were analyzed, each corresponding to one of the three MHC classes [4] (Table 2)
Summary
Immune genes have been shown to be strongly affected by natural selection [1,2]. In particular, the genes of the Major Histocompatibility Complex (MHC) have attracted the attention of evolutionary biologists, because of their extraordinary polymorphism and fundamental role in vertebrate immunity [3]. Various studies have shown that natural selection acts on MHC genes and have investigated its underlying mechanisms by comparing the population genetic structure of MHC genes with that of neutral loci (see for example [9,10]; reviewed in [6]). In addition to shedding light on the theoretical question of the way in which selection shapes MHC variation in wild rodents, this research is a step towards a better understanding of plague circulation in the central highlands of Madagascar, which remains one of the most important plague foci in the world [24,39] To this purpose, we used a population genetics approach based on the comparison of MHC-linked and neutral microsatellites in two contrasting population designs. Spatial variation in plague selection pressure may result in more marked geographic patterns of genetic differentiation at these markers than at neutral markers [3]
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