Inbreeding Avoidance Drives Consistent Variation of Fine-Scale Genetic Structure Caused by Dispersal in the Seasonal Mating System of Brandt’s Voles

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.

Kinship analysis reveals reproductive success skewed toward overwintered Brandt's voles in semi‐natural enclosures

“…The microsatellite marker method (Liu et al 2013) was used to precisely identify kinship among individuals in each enclosure. In total, 531 tissue samples (for details see Table S2) were collected during this experiment from the 3 enclosures.…”

“…Some researchers speculated that early broods could join in reproduction in their birth year (Zhong et al 1998) but lack direct evidence and details. In addition, overt social hierarchy exists in both wild and laboratory populations, and overwintered voles always have higher social status (Shi et al 1999b;Wan et al 2007;Zhang & Shi 2007;Liu et al 2013). Moreover, a male-biased dispersal is detected in Brandt's vole (Huo et al 2010;Liu et al 2013), which implies reproductive suppression through social hierarchy in this species.…”

“…In addition, overt social hierarchy exists in both wild and laboratory populations, and overwintered voles always have higher social status (Shi et al 1999b;Wan et al 2007;Zhang & Shi 2007;Liu et al 2013). Moreover, a male-biased dispersal is detected in Brandt's vole (Huo et al 2010;Liu et al 2013), which implies reproductive suppression through social hierarchy in this species. Thus, Brandt's vole provides a good model to investigate the seasonal differentiations of postnatal gonadal developmental patterns and reproductive skew in a small rodent.…”

Dynamic expressions of hypothalamic genes regulate seasonal breeding in a natural rodent population

“…Brandt's vole ( Lasiopodomys brandtii , Figure a) is a small, nonhibernating, herbivorous and social rodent that is mainly distributed in the steppes in China, the Republic of Mongolia and the Baikal Lake region of Russia (Liu, Yue, Wang, Li, & Cong, ; Wang et al, ; Yue, Wang, Huang, & Liu, ; Zhong, Wang, Zhou, & Wang, ; Zhong, Wang, & Wan, ). Following overt seasonal changes in its habitat (Figure b), Brandt's vole shows strong seasonal breeding and its population size increases dramatically from spring (early March) to autumn (late August) (Zhong et al, ; Zhong et al, ; Li, Hou, Wan, & Zhang, ; Li, Yin, et al, ; Figure c,d).…”

Parental care buffers against inbreeding depression in burying beetles

“…parental care | environmental stress | fitness | inbreeding depression | inbreeding tolerance I nbreeding is an important issue in evolutionary biology and ecology because of its profound implications for genetic variation and the evolution of mating systems and reproductive strategies (1)(2)(3)(4)(5). Inbreeding results from matings between related individuals and can cause a reduction in offspring fitness because the higher degree of homozygosity associated with inbreeding increases the risk that deleterious recessive alleles are expressed (6).…”