Sex-specific selection for MHC variability in Alpine chamois

Abstract

BackgroundIn mammals, males typically have shorter lives than females. This difference is thought to be due to behavioural traits which enhance competitive abilities, and hence male reproductive success, but impair survival. Furthermore, in many species males usually show higher parasite burden than females. Consequently, the intensity of selection for genetic factors which reduce susceptibility to pathogens may differ between sexes. High variability at the major histocompatibility complex (MHC) genes is believed to be advantageous for detecting and combating the range of infectious agents present in the environment. Increased heterozygosity at these immune genes is expected to be important for individual longevity. However, whether males in natural populations benefit more from MHC heterozygosity than females has rarely been investigated. We investigated this question in a long-term study of free-living Alpine chamois (Rupicapra rupicapra), a polygynous mountain ungulate.ResultsHere we show that male chamois survive significantly (P = 0.022) longer if heterozygous at the MHC class II DRB locus, whereas females do not. Improved survival of males was not a result of heterozygote advantage per se, as background heterozygosity (estimated across twelve microsatellite loci) did not change significantly with age. Furthermore, reproductively active males depleted their body fat reserves earlier than females leading to significantly impaired survival rates in this sex (P < 0.008). This sex-difference was even more pronounced in areas affected by scabies, a severe parasitosis, as reproductively active males were less likely to survive than females. However, we did not find evidence for a survival advantage associated with specific MHC alleles in areas affected by scabies.ConclusionsIncreased MHC class II DRB heterozygosity with age in males, suggests that MHC heterozygous males survive longer than homozygotes. Reproductively active males appear to be less likely to survive than females most likely because of the energetic challenge of the winter rut, accompanied by earlier depletion of their body fat stores, and a generally higher parasite burden. This scenario renders the MHC-mediated immune response more important for males than for females, which implies a relatively stronger selection pressure on MHC genes in males than in females.

MHC influences infection with parasites and winter survival in the root vole Microtus oeconomus

“…In frogs, alleles from the MHC class IIB locus were associated with increased survival following experimental infection with chytridiomycosis, an emerging disease (Savage and Zamudio 2011). In contrast, although MHC heterozygosity increased survival in male chamois, there was no evidence for an MHC-related survival advantage in populations exposed to scabies (Schaschl et al 2012).…”

Adult survival selection in relation to multilocus heterozygosity and body size in a tropical bird species, the Zenaida dove, Zenaida aurita

“…Regarding the influence of genetic quality, both genomewide heterozygosity and heterozygosity at specific loci have been associated with increased survival in some vertebrate species (Schmeller et al 2007;Banks et al 2010;Evans et al 2010;Schaschl et al 2012;Kloch et al 2013;Forcada and Hoffman 2014), including birds (Redfield 1974;Markert et al 2004;Worley et al 2010;Sepil et al 2013). However, evidence for a direct effect of genomewide heterozygosity on survival remains limited, possibly because of methodological issues.…”

Population genetic data pertinent to the conservation of Bulgarian chamois (Rupicapra rupicapra balcanica)

“…However, we used genotype data of the latter two populations (KAW, DLB) only for individual-based analyses (STRUCTURE, FCA; see below), as their respective sample sizes were very small and thus most likely not reliable for analyses on the population level (Hale et al 2012). Most of the Austrian samples have already been included in an earlier study (Schaschl et al 2012).…”

“…We used the GenElute TM Mammalian Genomic DNA Miniprep kit to extract total DNA, and screened allelic variability at the following twelve dinucleotide microsatellite loci: RMO26, RMO29, INRA005, INRA011, INRA023, NRA036, ETH10, ETH225, SR-CRSP01, SR-CRSP05, SR-CRSP08, SR-CRSP09 (Kossarek et al 1994;Peréz et al 2000;Lorenzini 2005;Schaschl et al 2012). PCR products were electrophoresed on a LI-COR 4200 automated sequencer along with a fluorescently labelled size standard (50-350 bp sizing standard; LI-COR Ò Biotechnology Division), and allele lengths were determined using Gene ImageIR 3.52.…”