Neff BD, Pitcher TE.. Mate choice for non-additive genetic benefits: a resolution to the lek paradox. J Theor Biol 254: 147-155

Department of Biology, University of Western Ontario, 1151 Richmond Street, London, Ontario, Canada N6A 5B7.
Journal of Theoretical Biology (Impact Factor: 2.12). 06/2008; 254(1):147-55. DOI: 10.1016/j.jtbi.2008.05.019
Source: PubMed


In promiscuous mating systems, females often show a consistent preference to mate with one or a few males, presumably to acquire heritable genetic benefits for their offspring. However, strong directional selection should deplete additive genetic variation in fitness and consequently any benefit to expressing the preference by females (referred to as the lek paradox). Here, we provide a novel resolution that examines non-additive genetic benefits, such as overdominance or inbreeding, as a source of genetic variation. Focusing on the inbreeding coefficient f and overdominance effects, we use dynamic models to show that (1) f can be inherited from sire to offspring, (2) populations with females that express a mating preferences for outbred males (low f) maintain higher genetic variation than populations with females that mate randomly, and (3) preference alleles for outbred males can invade populations even when the alleles are associated with a fecundity cost. We show that non-additive genetic variation due to overdominance can be converted to additive genetic variation and becomes "heritable" when the frequencies of alternative homozygous genotypes at fitness loci deviate from equality. Unlike previous models that assume an infinite population size, we now show that genetic drift in finite populations can lead to the necessary deviations in the frequencies of homozygous genotypes. We also show that the "heritability of f," and hence the benefit to a mating preference for non-additive genetic benefits, is highest in small populations and populations in which a smaller number of loci contribute to fitness via overdominance. Our model contributes to the solution of the lek paradox.

10 Reads
    • "Theoretical studies have shown that heterozygosity is heritable when allele frequencies are unequal (Borgia, 1979; Mitton et al., 1993; Neff and Pitcher, 2008), and a number of empirical studies have reported parent–offspring correlations in heterozygosity itself (Cothran et al., 1983; Mitton et al., 1993; Richardson et al., 2004; Hoffman et al., 2007; García-Navas et al., 2009; Oh, 2009; Thoß, 2010; Thonhauser et al., 2014), or inferred them from a parent–offspring correlation in inbreeding coefficients (Reid et al., 2006). Although the presence of substantial heritability of heterozygosity has been formally shown for two-allelic loci more than two decades ago (Mitton et al., 1993), this is not well known among evolutionary biologists (e.g., Coulson and Clegg, 2014). "
    [Show abstract] [Hide abstract]
    ABSTRACT: The maintenance of genetic diversity in fitness-related traits remains a central topic in evolutionary biology, for example, in the context of sexual selection for genetic benefits. Among the solutions that have been proposed is directional sexual selection for heterozygosity. The importance of such selection is highly debated. However, a critical evaluation requires knowledge of the heritability of heterozygosity, a quantity that is rarely estimated in this context, and often assumed to be zero. This is at least partly the result of the lack of a general framework that allows for its quantitative prediction in small and inbred populations, which are the focus of most empirical studies. Moreover, while current predictors are applicable only to biallelic loci, fitness-relevant loci are often multiallelic, as are the neutral markers typically used to estimate genome-wide heterozygosity. To this end, we first review previous, but little-known, work showing that under most circumstances, heterozygosity at biallelic loci and in the absence of inbreeding is heritable. We then derive the heritability of heterozygosity and the underlying variances for multiple alleles and any inbreeding level. We also show that heterozygosity at multiallelic loci can be highly heritable when allele frequencies are unequal, and that this heritability is reduced by inbreeding. Our quantitative genetic framework can provide new insights into the evolutionary dynamics of heterozygosity in inbred and outbred populations.Heredity advance online publication, 15 July 2015; doi:10.1038/hdy.2015.59.
    No preview · Article · Jul 2015 · Heredity
  • Source
    • "Similarly, although substantial literature exists on maternal influences on life-history traits (e.g., Bernardo 1996; Green 2008), their role in population responses to selection has received less attention (Mousseau and Fox 1998; Wilson et al. 2005; Räsänen and Kruuk 2007). For example, nonadditive genetic variance can be converted to additive genetic variance, the material that can be used by selection, during a bottleneck (Carson 1990; Neff and Pitcher 2008). Also, maternal effects (maternal additive genetic and maternal environmental) can modify the rate and direction of a change in response to selection (Mousseau and Fox 1998; Wilson et al. 2005; Räsänen and Kruuk 2007). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Although studies addressing natural selection have primarily focused on additive genetic effects because of their direct relationship with responses to selection, nonadditive genetic and maternal effects can also significantly influence phenotypes. We partitioned the phenotypic variance of survival and fitness-related traits in juvenile Atlantic salmon (Salmo salar) from three allopatric populations (LaHave, Sebago, and Saint-Jean) into additive genetic, nonadditive genetic, and maternal environmental effects using a full-factorial breeding design. We also modelled the potential increase in offspring performance if nonrandom mating (e.g., mate choice) is considered instead of random mating. The three populations exhibited significant differences in trait values as well as the genetic architecture of the traits. Nevertheless, nonadditive genetic and maternal environmental effects tended to be larger than the additive genetic effects. There was also a shift from maternal environmental to genetic effects during development in two of the populations. That is, maternal environmental effects were larger at early (egg and alevin) life stages, whereas nonadditive effects were larger at the later (fry) life stage. The amount of additive genetic effects was small, suggesting the traits will respond slowly to selection. We discuss how different maternal environmental effects across years may influence the genetic architecture of offspring traits. © 2015, National Research Council of Canada. All Rights Reserved.
    Full-text · Article · May 2015 · Canadian Journal of Fisheries and Aquatic Sciences
  • Source
    • "However, there is an increasing evidence that non-additive genetic effects are key components of phenotypes (Crnokrak and Roff, 1995; Roff and Emerson, 2006). Furthermore, non-additive genetic effects are a cause of inbreeding depression (Crnokrak and Roff, 1999; Keller and Waller, 2002) and can be converted to additive genetic effects, for example, during a bottleneck, which can then provide genetic variation for natural selection to act on (Carson, 1990; also see Neff and Pitcher, 2008). Phenotypic variance can also be explained by maternal environmental effects (Falconer and Mackay, 1996) and these effects can also affect evolutionary trajectories (Räsänen and Kruuk, 2007). "
    [Show abstract] [Hide abstract]
    ABSTRACT: The additive genetic effects of traits can be used to predict evolutionary trajectories, such as responses to selection. Non-additive genetic and maternal environmental effects can also change evolutionary trajectories and influence phenotypes, but these effects have received less attention by researchers. We partitioned the phenotypic variance of survival and fitness-related traits into additive genetic, non-additive genetic and maternal environmental effects using a full-factorial breeding design within two allopatric populations of Atlantic salmon (Salmo salar). Maternal environmental effects were large at early life stages, but decreased during development, with non-additive genetic effects being most significant at later juvenile stages (alevin and fry). Non-additive genetic effects were also, on average, larger than additive genetic effects. The populations, generally, did not differ in the trait values or inferred genetic architecture of the traits. Any differences between the populations for trait values could be explained by maternal environmental effects. We discuss whether the similarities in architectures of these populations is the result of natural selection across a common juvenile environment.Heredity advance online publication, 14 August 2013; doi:10.1038/hdy.2013.74.
    Full-text · Article · Aug 2013 · Heredity
Show more