Abstract

Inbreeding depression is a major evolutionary and ecological force influencing population dynamics and the evolution of inbreeding-avoidance traits such as mating systems and dispersal. Mating systems and dispersal are fundamental determinants of population genetic structure. Resolving the relationships among genetic structure, seasonal breeding-related mating systems and dispersal will facilitate our understanding of the evolution of inbreeding avoidance. The goals of this study were as follows: (i) to determine whether females actively avoided mating with relatives in a group-living rodent species, Brandt’s voles (Lasiopodomys brandtii), by combined analysis of their mating system, dispersal and genetic structure; and (ii) to analyze the relationships among the variation in fine-genetic structure, inbreeding avoidance, season-dependent mating strategies and individual dispersal. Using both individual- and population-level analyses, we found that the majority of Brandt’s vole groups consisted of close relatives. However, both group-specific FISs, an inbreeding coefficient that expresses the expected percentage rate of homozygosity arising from a given breeding system, and relatedness of mates showed no sign of inbreeding. Using group pedigrees and paternity analysis, we show that the mating system of Brandt’s voles consists of a type of polygyny for males and extra-group polyandry for females, which may decrease inbreeding by increasing the frequency of mating among distantly-related individuals. The consistent variation in within-group relatedness, among-group relatedness and fine-scale genetic structures was mostly due to dispersal, which primarily occurred during the breeding season. Biologically relevant variation in the fine-scale genetic structure suggests that dispersal during the mating season may be a strategy to avoid inbreeding and drive the polygynous and extra-group polyandrous mating system of this species.

Highlights

  • Inbreeding depression is a major evolutionary and ecological force influencing population dynamics and the evolution of inbreeding-avoidance traits such as mating systems and dispersal [1]

  • Population genetic structure is fundamentally determined by mating systems and dispersal, which have long been recognized as be the primary factors influencing the rate and outcome of evolution [2]

  • All 14 loci deviated from Hardy–Weinberg equilibrium (HWE) after the Bonferroni correction among some of the 29 sampled groups

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Summary

Introduction

Inbreeding depression is a major evolutionary and ecological force influencing population dynamics and the evolution of inbreeding-avoidance traits such as mating systems and dispersal [1]. Population genetic structure is fundamentally determined by mating systems and dispersal, which have long been recognized as be the primary factors influencing the rate and outcome of evolution [2]. Inbreeding depression is usually substantial enough to affect both individual and population performance [3,4] by increasing the chances of offspring being affected by recessive or deleterious traits [5]. The almost ubiquitous phenomenon of females mating with more than one male, polyandry, is proposed as a mechanism to avoid reproducing with genetically incompatible mates [11,12,13] and a means of inbreeding avoidance [14]. The idea that females engage in polyandry for genetic benefits is supported by a great deal of increasingly rigorous empirical evidence [11,12,13,15,16,17,18,19,20,21,22,23,24]

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