Diversifying selection on MHC class I in the house sparrow (Passer domesticus)

Abstract

Genes of the major histocompatibility complex (MHC) are the most polymorphic loci known in vertebrates. Two main hypotheses have been put forward to explain the maintenance of MHC diversity: pathogen-mediated selection and MHC-based mate choice. Host-parasite interactions can maintain MHC diversity via frequency-dependent selection, heterozygote advantage, and diversifying selection (spatially and/or temporally heterogeneous selection). In this study, we wished to investigate the nature of selection acting on the MHC class I across spatially structured populations of house sparrows (Passer domesticus) in France. To infer the nature of the selection, we compared patterns of population differentiation based on two types of molecular markers: MHC class I and microsatellites. This allowed us to test whether the observed differentiation at MHC genes merely reflects demographic and/or stochastic processes. At the global scale, diversifying selection seems to be the main factor maintaining MHC diversity in the house sparrow. We found that (i) overall population differentiation at MHC was stronger than for microsatellites, (ii) MHC marker showed significant isolation by distance. In addition, the slope of the regression of F(ST) on geographical distance was significantly steeper for MHC than for microsatellites due to a stronger pairwise differentiation between populations located at large geographical distances. These results are in agreement with the hypothesis that spatially heterogeneous selective pressures maintain different MHC alleles at local scales, possibly resulting in local adaptation.

Plasmodium relictuminfection and MHC diversity in the house sparrow (Passer domesticus)

“…Diversifying selection has been investigated using a population genetics approach in fish and bird species [30,31]. Recently, we found that neutral processes are not sufficient to explain spatial variation in MHC class I among 13 house sparrow (Passer domesticus) populations [32]. In agreement with the prediction of diversifying selection [33], we found a stronger pattern of isolation by distance for MHC class I than for neutral markers (microsatellites).…”

Reduced MHC class II diversity in island compared to mainland populations of the black-footed rock-wallaby (Petrogale lateralis lateralis)

“…3, Table 4). However, very few DAB b1 alleles are actually shared between Barrow Island, Exmouth and the Wheat-belt, and possibly the lower level of population differentiation at the DAB b1 compared to neutral loci is a statistical artifact of the method we used (Ekblom et al 2007;Louiseau et al 2009) to analyse MHC alleles amplified from multiple loci. If it is true that there is lower population differentiation at DAB b1 than at microsatellites, then the selection pressures operating on DAB b1 are likely to be similar in the examined black-footed rock-wallaby populations, so that less population differentiation is present at DAB b1 than would be expected if only drift and gene flow were operating on this locus.…”

“…We applied the approach of Ekblom et al (2007) and Louiseau et al (2009) for statistical analysis of an MHC gene where more than one gene copy is amplified, using the software ARLEQUIN 3.1 (Excoffier et al 2005). Alleles were treated as haplotypic data: the DNA sequence of each allele was input in a haplotype list, and then for each population sample, the name of each sequence in the population and number of individuals containing that sequence were listed.…”

Immunity and Virulence in Bird-Parasite Interactions

“…Each of these factors has been shown to be variable: hosts differ in a number of genes involved in parasite resistance (see for instance the hyper-variable MHC genes) [41][42][43]; pathogens differ in genes responsible for infectivity and immune evasion [44,45]; finally, environmental conditions are seldom constant in time and space. Taking into account this variability is of prime importance for our understanding of the ecology of host-parasite interactions [46].…”