Enhanced Selection for MHC Diversity in Social Tuco-Tucos

Abstract

Abstract. To explore the effects of behavior and demography on balancing selection at major histocompatibility complex (MHC) loci, we examined allelic diversity at exon 2 of the MHC class II DQ␤ locus in a social and a solitary species of tuco-tuco (Rodentia: Ctenomyidae: Ctenomys), both of which occur in the same valley in southwestern Argentina. By comparing patterns of diversity at this MHC gene to the diversity evident at fifteen microsatellite loci, we demonstrate that balancing selection at the DQ␤ locus is enhanced in the social species compared to its solitary congener. These findings have intriguing implications for the role of behavioral and demographic parameters in maintaining diversity at MHC loci. Behavioral and demographic attributes may significantly affect patterns of genetic variation in natural populations of vertebrates (Hartl and Clark 1989;Ross et al. 1999). While interactions among behavior, demography, and genetic structure are well-documented for neutral genetic markers such as microsatellites (Nielsen 1997;Kimmel et al. 1998), the role of these variables in shaping variation at major histocompatibility complex (MHC) loci is considerably less well understood. Both molecular-and population-level patterns of allelic variation indicate that at least some MHC genes are subject to strong balancing selection (Hughes and Nei 1989; Edwards and Hedrick 1998). The functional role of these genes in the immune response, together with the discovery of specific pathogen-MHC allele interactions, suggests that pathogen exposure contributes to this selection (Hill et al. 1994;Paterson et al. 1998;Voeten et al. 2000). Because behavioral and demographic parameters are expected to influence pathogen exposure (May and Anderson 1979) as well as the movement of alleles within and among populations, variation in these parameters may also influence balancing selection and, hence, allelic variation at MHC loci.At the same time, behavioral and demographic factors may affect our ability to detect selection at MHC genes. Because these loci evolve within populations, they are subject to the same evolutionary forces (e.g., genetic drift) that shape variation at neutral loci. These forces, which are influenced by behavioral and demographic patterns, are expected to affect the impact of selection at functional loci (Hartl and Clark 1989). As effective population size decreases, the ability of natural selection to overcome the effects of drift is decreased (Kimura 1983;Li 1997). The effects of these forces may vary among populations, with the result that conspecifics in different populations may experience markedly different levels of selection on MHC loci, but these differences in selection may be difficult to detect unless patterns of neutral genetic structure are taken into account. Specifically, data from neutral markers provide a critical backdrop against which to 1 Present address: Centers for Disease Control, MS G-13, 1600 Clifton Road NE, Atlanta, Georgia 30333; E-mail: thambuch@ cdc.gov.evaluate the nature and i...

The evolutionary ecology of the major histocompatibility complex

“…Watterson (1978) proposed that deviation from such an equilibrium is an indicator of departures from neutrality and hence selection. The so-called Ewens-Watterson test of neutrality has been used to confirm the effects of balancing selection acting on the MHC in both non-model species (Paterson, 1998;Miller et al, 2001;Hambuch and Lacey, 2002) and humans (Mack et al, 2000;Begovich et al, 2001).…”

“…Understanding how social structure affects MHC dynamics may be especially important given that social structure will influence the transmission of parasites and disease at a local scale, and also the potential for mate choice decisions will vary in response to levels of local inbreeding. Such processes do appear to be pertinent - Hambuch and Lacey (2002) compared the strength of balancing selection between a social and a solitary species of tuco-tuco (Ctenomys sociabilis and C. haigi, respectively), testing the hypothesis that sociality affects parasite transmission that will influence selection. Selection coefficients were more than 50 times greater in the social species.…”

Patterns of variability at the major histocompatibility class II alpha locus in Atlantic salmon contrast with those at the class I locus

“…PBRs, for example, are commonly deduced by comparing MHC sequences from a species of interest with human counterparts (e.g. Grimholt et al 1993;Kim et al 1999;Hoelzel et al 1999;Hambuch and Lacey 2002), where the crystal structure has been analysed (Brown et al 1993). Often, patterns of selection on MHC genes are then studied with respect to PBRs/non-PBRs identified in this manner.…”

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

“…Among-population differentiation at MHC loci has been observed to range from lower than (Sommer, 2003;Aguilar et al, 2004), similar to (Boyce et al, 1997;Parker et al, 1999;Hedrick et al, 2001;Huang and Yu, 2003), to higher than that at neutral loci (Miller et al, 2001;Beacham et al, 2004), reflecting differences in the relative strengths of natural selection, genetic drift and gene flow across species (Eizaguirre et al, 2010). Indeed, the relative levels of neutral and MHC variation within and among populations can vary across closely related species (Hambuch and Lacey, 2002;Jarvi et al, 2004), and even within a species depending on the spatial scale of analysis . 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).…”