Abstract

Although small populations are expected to lose genetic diversity through genetic drift and inbreeding, a number of mechanisms exist that could minimize this genetic decline. Examples include mate choice for unrelated mates and fertilization patterns biased toward genetically dissimilar gametes. Both processes have been widely documented, but the long-term implications have received little attention. Here, we combined over 25 years of field data with high-resolution genetic data to assess the long-term impacts of biased fertilization patterns in the endangered North Atlantic right whale. Offspring have higher levels of microsatellite heterozygosity than expected from this gene pool (effect size = 0.326, P < 0.011). This pattern is not due to precopulatory mate choice for genetically dissimilar mates (P < 0.600), but instead results from postcopulatory selection for gametes that are genetically dissimilar (effect size = 0.37, P < 0.003). The long-term implication is that heterozygosity has slowly increased in calves born throughout the study period, as opposed to the slight decline that was expected. Therefore, this mechanism represents a natural means through which small populations can mitigate the loss of genetic diversity over time.

Highlights

  • Mating closed populations are expected to lose genetic diversity over time through genetic drift and inbreeding (Fisher 1930; Wright 1931; Hartl and Clark 1997)

  • An observed excess of heterozygosity in offspring could be due to three possible processes: (1) precopulatory mate choice for genetically dissimilar mates; (2) genetic incompatibility based on fetal loss resulting from a breakdown in self-/non–self-recognition; and (3) genetic incompatibility based on heterozygosity

  • Our results show that microsatellite heterozygosity is higher in offspring North Atlantic right whales than is expected from the gene pool, which appears to result from fertilizations and/or pregnancies being more successful between n = 373 n = 195 n = 154

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Summary

Introduction

Mating closed populations are expected to lose genetic diversity over time through genetic drift and inbreeding (Fisher 1930; Wright 1931; Hartl and Clark 1997). Genetic diversity plays a key role in shaping individual fitness (Coltman et al 1999; Dunn and Byers 2008), and it is not surprising that a variety of mechanisms have evolved that can result in patterns of reproduction deviating from random expectations in ways that increase the genetic diversity (and subsequent fitness) of offspring (see Jordan and Bruford 1998; Tregenza and Wedell 2000; and Kempenaers 2007 for reviews) If such mechanisms are widespread in a population, these individual-based strategies can reduce the rate at which genetic diversity is lost from the population as a whole, and impact the overall extinction probability of the population (Saccheri et al 1998; Westemeier et al 1998; Spielman et al 2004).

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