Density‐related changes in selection pattern for major histocompatibility complex genes in fluctuating populations of voles

Abstract

Host-pathogen interactions are of particular interest in studies of the interplay between population dynamics and natural selection. The major histocompatibility complex (MHC) genes of demographically fluctuating species are highly suitable markers for such studies, because they are involved in initiating the immune response against pathogens and display a high level of adaptive genetic variation. We investigated whether two MHC class II genes (DQA1, DRB) were subjected to contemporary selection during increases in the density of fossorial water vole (Arvicola terrestris) populations, by comparing the neutral genetic structure of seven populations with that estimated from MHC genes. Tests for heterozygosity excess indicated that DQA1 was subject to intense balancing selection. No such selection operated on neutral markers. This pattern of selection became more marked with increasing abundance. In the low-abundance phase, when populations were geographically isolated, both overall differentiation and isolation-by-distance were more marked for MHC genes than for neutral markers. Model-based simulations identified DQA1 as an outlier (i.e. under selection) in a single population, suggesting the action of local selection in fragmented populations. The differences between MHC and neutral markers gradually disappeared with increasing effective migration between sites. In the high-abundance year, DQA1 displayed significantly lower levels of overall differentiation than the neutral markers. This gene therefore displayed stronger homogenization than observed under drift and migration alone. The observed signs of selection were much weaker for DRB. Spatial and temporal fluctuations in parasite pressure and locus-specific selection are probably the most plausible mechanisms underlying the observed changes in selection pattern during the demographic cycle.

Genetic structure and contrasting selection pattern at two major histocompatibility complex genes in wild house mouse populations

“…This has led to the hope that studying a single MHC gene will reveal patterns of evolution representative of the MHC as a whole. Based on this assumption, most studies are restricted to only one MHC gene (see exceptions, for example, in Edwards et al, 1997;Sommer, 2003;Bryja et al, 2007;Tollenaere et al, 2008;Babik et al, 2008.). However, there are at least two reasons for analysing more MHC genes.…”

MHC genetic structure and divergence across populations of Chinook salmon (Oncorhynchus tshawytscha)

“…The MHC often displays considerable differentiation across geographical landscapes as has been found in populations of mammals, birds, and fishes (for example, Landry and Bernatchez, 2001;Miller et al, 2001;Wegner et al, 2003;Bryja et al, 2007;Dionne et al, 2007;Ekblom et al, 2007). Population subdivision at the MHC may arise because of mutation, gene flow, genetic drift, or local adaptation (Schierup et al, 2000).…”

Contrasting responses to selection in class I and class IIα major histocompatibility-linked markers in salmon

“…In contrast, Kruiswijk et al (2005) found a complete divergence in class II, but not in class I of a barbs species flock. Differences in evolutionary rates and the response to selection between both genes have been observed not only in fish but also in mammals and birds (Go et al, 2003;Bryja et al, 2007). Class I and class II molecules differ in the nature of the peptides that they bind, in how they bind and process them (Castellino et al, 1997;Kaufman et al, 1999;Grommé and Neefjes, 2002;Go et al, 2003) and in the T cells they react with (Housset and Malissen, 2003;Huseby et al, 2003).…”

“…In comparison to studies of geographic patterns in MHC variation, there have been relatively few studies on MHC which also include a temporal dimension, despite the possibility that selective forces across time within a population may differ from those across populations (Smulders et al, 2003;Sommer, 2003;Beacham et al, 2004;Seddon and Ellegren, 2004;Westerdahl et al, 2004;Coughlan et al, 2006;Oliver et al, 2009). Moreover, most studies focus on a single class of MHC gene (most commonly class IIb), whereas selection can affect differentially the genetic diversity of both genes (Bryja et al, 2007).…”

“…More recently, an increasing number of descriptions of the geographic distribution of MHC variation (or variation at markers tightly linked to MHC loci)-often in conjunction with the analysis at other (putatively), neutral loci-have provided further insight into the selective influences on MHC loci in a range of species (Miller et al, 2001;Aguilar and Garza, 2006;Bryja et al, 2007;Ekblom et al, 2007;Alcaide et al, 2008). In general, MHC heterozygosity within populations is higher than that for neutral loci (Huang and Yu, 2003;Aguilar et al, 2004; but see, Boyce et al, 1997).…”