Male-benefit sexually antagonistic genotypes show elevated vulnerability to inbreeding

Abstract

BackgroundThere is theoretical and empirical evidence for strong sexual selection in males having positive effects on population viability by serving to purify the genome of its mutation load at a low demographic cost. However, there is also theoretical and empirical evidence for negative effects of sexual selection on female fitness, and therefore population viability, known as the gender load. This can take the form of sexually antagonistic (SA) genetic variation where alleles with a selective advantage in males pose a detriment to female fitness, and vice versa. Here, using seed beetles, we shed light on a previously unexplored manifestation of the gender load: the effect of SA genetic variation on tolerance to inbreeding.ResultsWe found that genotypes encoding high male, but low female fitness exhibited significantly greater rates of extinction upon enforced inbreeding relative to genotypes encoding high female but low male fitness. Also, genotypes encoding low fitness in both sexes exhibited greater rates of extinction relative to generally high-fitness genotypes (though marginally non-significant), an expected finding attributable to variation in mutation load across genotypes. Despite follow-up investigations aiming to identify the mechanism(s) underlying these findings, it remains unclear whether the gender load and the mutation load have independent consequences for tolerance to inbreeding, or whether these two types of genetic architecture interact epistatically to render male-benefit genetic variation relatively intolerant to inbreeding.ConclusionsRegardless of the underlying mechanism(s), our results show that male-benefit/female-detriment SA genetic variation poses a previously unseen detriment to population viability due to its elevated vulnerability to inbreeding/homozygosity. This suggests that sexual selection in the context of SA genetic variance for fitness may enhance the gender load on population viability more than previously appreciated, due to selecting for male-benefit SA genetic variation that engenders lineages to extinction upon inbreeding. We note that our results imply that SA alleles that are sexually selected for in males may be underrepresented or even lacking in panels of inbred lines.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-0981-4) contains supplementary material, which is available to authorized users.

Sex-specific dominance reversal of genetic variation for fitness

“…Using a diallel cross among isogenic strains from a well-characterized population of C . maculatus known to exhibit predominantly SA genetic variance in fitness [37–38,53,71–72], we show that the dominant–recessive relationship between alternative alleles at the loci underlying fitness was reversed in heterozygous males versus females (Fig 3). Specifically, strains whose outcrossed male fitness values tended to covary with the inbred male fitness values of the strains they were crossed with tended not to exhibit this covariance with regard to female fitness and vice versa (see Materials and methods and S6 Fig).…”

“…The origin of our study population has been described by Berger and colleagues [37] and Grieshop and colleagues [53]. Briefly, the population was isolated from Vigna unguiculata seed pods collected at a small-scale agricultural field close to Lomé, Togo (06°10′N 01°13′E) during October and November 2010.…”

“…unguiculata seeds at 29°C, 55% RH and a 12L:12D light regime for about 12 generations prior to the sex-specific fitness assays conducted by Berger and colleagues [37]. The development of isogenic (inbred) strains from these isofemale lines is described by Grieshop and colleagues [53] and in the S1 Text. The 16 inbred strains used in the present study were reasonably evenly distributed about the population’s original intersexual genetic correlation for fitness (S7 Fig) and apparently captured an unbiased representation of the standing SA genetic variation for fitness exhibited by the wild population from which it was derived (see Results and S1 Text).…”

“…The BLUPs for a given inheritance class Q from separate male and female models ( q M and q F ) can be set as variance-standardized y and x axes, respectively (Fig 1). That coordinate system can be rotated 45° to derive BLUPs for SC ( q SC ) and SA ( q SA ) additive genetic variance (Fig 1) as done by Berger and colleagues [37] and Grieshop and colleagues [53], like so: and Note that no variance is lost during this rotation.…”

“…Here, we used a full diallel cross among 16 isogenic strains to partition genetic variance in sex-specific competitive lifetime reproductive success (hereafter “fitness”) in a wild-caught population of the seed beetle C . maculatus that is known to exhibit pronounced SA genetic variance in fitness [37–38,53]. This species exhibits a polyandrous mating system, X/Y sex determination, and pronounced sexual dimorphism and sex-biased gene expression [33,38,54–56].…”