Balancing Selection in Species with Separate Sexes: Insights from Fisher’s Geometric Model

Abstract

How common is balancing selection, and what fraction of phenotypic variance is attributable to balanced polymorphisms? Despite decades of research, answers to these questions remain elusive. Moreover, there is no clear theoretical prediction about the frequency with which balancing selection is expected to arise within a population. Here, we use an extension of Fisher's geometric model of adaptation to predict the probability of balancing selection in a population with separate sexes, wherein polymorphism is potentially maintained by two forms of balancing selection: (1) heterozygote advantage, where heterozygous individuals at a locus have higher fitness than homozygous individuals, and (2) sexually antagonistic selection (a.k.a. intralocus sexual conflict), where the fitness of each sex is maximized by different genotypes at a locus. We show that balancing selection is common under biologically plausible conditions and that sex differences in selection or sex-by-genotype effects of mutations can each increase opportunities for balancing selection. Although heterozygote advantage and sexual antagonism represent alternative mechanisms for maintaining polymorphism, they mutually exist along a balancing selection continuum that depends on population and sex-specific parameters of selection and mutation. Sexual antagonism is the dominant mode of balancing selection across most of this continuum.O NE of the primary goals of population genetics is to evaluate how processes of mutation, selection, migration, recombination, and genetic drift account for the maintenance of genetic variation in natural populations. This "great obsession" with genetic variation (Gillespie 2004, p. 154) is reflected by a massive body of theoretical and empirical research that seeks to connect empirical patterns of population and quantitative genetic variability with the specific evolutionary processes that might account for them.Balancing selection-selection that maintains genetic variation at a locus-could potentially account for an important fraction of observed quantitative genetic variability (Dobzhansky 1955;Lewontin 1974;Charlesworth and Hughes 1999). Although relatively few unambiguous cases of balancing selection have been documented to date (see Charlesworth 2006;Hedrick 2012;Johnston et al. 2013;Leffler et al. 2013), empirical methods for detecting their population genetic signatures are highly conservative and may fail to identify many (or most) instances of balancing selection within a genome (Charlesworth 2006;Charlesworth and Charlesworth 2010). Furthermore, balanced polymorphisms may plausibly account for several empirical observations that are not easily explained by alternative models of variation maintained by recurrent mutation. For example, the high genetic variance in life history and reproductive traits (Houle 1992;Pomiankowski and Moller 1995) and the presence of intermediate-frequency alleles with large phenotypic effects (Long et al. 2000) are each potentially attributable to a subset of loci that segrega...

Coadapted genomes and selection on hybrids: Fisher's geometric model explains a variety of empirical patterns

“…For example, haplodiploidy might be modeled by setting $g_X=1$, and the uniparentally inherited loci (included via $g_{♀}$ and $g_{♂}$) might include the Y (or W) chromosome, organelles, selectively silenced regions of the X (or Z), or other imprinted loci (Turelli and Moyle 2007). With sex‐specific inheritance, we also require assumptions about sex‐specific selection, and this can be incorporated in several ways (Connallon and Clark 2014; Fraïsse et al. 2016b).…”

“…2016b). For example, sexual conflict can be modeled by assuming that there are differences in the optimal trait values for each sex (Connallon and Clark 2014). Alternatively, we could assume that some subset of the traits is under selection in only one sex, for example traits involved in spermatogenesis or oogenesis (Wu and Davis 1993; Coyne and Orr 2004).…”

“…With sex‐specific inheritance, we also require assumptions about sex‐specific selection, and this can be incorporated in several ways (Connallon and Clark 2014; Fraïsse et al. 2016b).…”

Sexually antagonistic polymorphism in simultaneous hermaphrodites

“…, those with separate sexes; see e.g. , Kidwell et al 1977; Charlesworth and Charlesworth 1980; Lande 1980; Rice 1984; Rice 1987; Prout 2000; Albert and Otto 2005; Bergero and Charlesworth 2008; Bonduriansky and Chenoweth 2009; Patten and Haig 2009; Patten et al 2010; Fry 2010; Arnqvist 2011; Immler et al 2012; Jordan and Charlesworth 2012; Connallon and Clark 2014a, 2014b). This theory serves as an important stimulant for experimental research on the evolutionary consequences of sexual antagonism ( e.g.…”

“…Sex-specific dominance has a particularly strong influence on the theoretical predictions for dioecious species ( e.g. , Rice 1984; Patten and Haig 2009; Fry 2010; Connallon and Clark 2010, 2014b; Jordan and Charlesworth 2012), yet its effects in partially-selfing hermaphrodite populations remain unclear. Finally, genetic drift is expected to play an important role in the evolutionary dynamics of SA alleles in dioecious species (Connallon and Clark 2012, 2013; Mullon et al 2012), and may additionally influence the detectability of population genetic signals of balancing selection (Charlesworth 2006; Connallon and Clark 2013).…”