Abstract

Numerous studies have reported correlations between the heterozygosity of genetic markers and fitness. These heterozygosity–fitness correlations (HFCs) play a central role in evolutionary and conservation biology, yet their mechanistic basis remains open to debate. For example, fitness associations have been widely reported at both neutral and functional loci, yet few studies have directly compared the two, making it difficult to gauge the relative contributions of genome‐wide inbreeding and specific functional genes to fitness. Here, we compared the effects of neutral and immune gene heterozygosity on death from bacterial infection in Antarctic fur seal (Arctocephalus gazella) pups. We specifically developed a panel of 13 microsatellites from expressed immune genes and genotyped these together with 48 neutral loci in 234 individuals, comprising 39 pups that were classified at necropsy as having most likely died of bacterial infection together with a five times larger matched sample of healthy surviving pups. Identity disequilibrium quantified from the neutral markers was positive and significant, indicative of variance in inbreeding within the study population. However, multilocus heterozygosity did not differ significantly between healthy and infected pups at either class of marker, and little evidence was found for fitness associations at individual loci. These results support a previous study of Antarctic fur seals that found no effects of heterozygosity at nine neutral microsatellites on neonatal survival and thereby help to refine our understanding of how HFCs vary across the life cycle. Given that nonsignificant HFCs are underreported in the literature, we also hope that our study will contribute toward a more balanced understanding of the wider importance of this phenomenon.

Highlights

  • A large and increasing number of studies are reporting positive correlations between heterozygosity, quantified from genetic markers such as microsatellites, and fitness

  • Model averaged effect size estimates for standardized multilocus heterozygosity (sMLH) based on the neutral loci, the immune loci, and all of the loci combined are given in Table 2. sMLH did not differ appreciably between healthy and infected pups, regardless of which class of marker was TA B L E 1 Alternative models of pup survival ranked in order of their AICc support

  • We deployed a large number of neutral microsatellites in combination with a newly developed panel of immune microsatellites to test for an heterozygosity–fitness correlations (HFCs) for neonatal mortality due to bacterial infection in a colonially breeding marine mammal

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Summary

Introduction

A large and increasing number of studies are reporting positive correlations between heterozygosity, quantified from genetic markers such as microsatellites, and fitness. These heterozygosity–fitness correlations (HFCs) have been documented for a wealth of traits in many animal and plant species (David, 1998; Hansson & Westerberg, 2002; Coltman & Slate, 2003; Chapman, Nakagawa, Coltman, Slate, & Sheldon, 2009; Szulkin, Bierne, & David, 2010) and suggest that heterozygosity could be a major component of individual fitness. Both mechanisms have been criticized on theoretical grounds, general effects because of simulations suggesting that inbred individuals are unlikely to be common in large unstructured populations (Balloux, Amos, & Coulson, 2004) and local effects due to the fact that balancing selection is perceived to be rare (Kreitman & Di Rienzo, 2004; Bubb et al, 2006)

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