Life history trade-offs at a single locus maintain sexually selected genetic variation

Abstract

Sexual selection, through intra-male competition or female choice, is assumed to be a source of strong and sustained directional selection in the wild. In the presence of such strong directional selection, alleles enhancing a particular trait are predicted to become fixed within a population, leading to a decrease in the underlying genetic variation. However, there is often considerable genetic variation underlying sexually selected traits in wild populations, and consequently, this phenomenon has become a long-discussed issue in the field of evolutionary biology. In wild Soay sheep, large horns confer an advantage in strong intra-sexual competition, yet males show an inherited polymorphism for horn type and have substantial genetic variation in their horn size. Here we show that most genetic variation in this trait is maintained by a trade-off between natural and sexual selection at a single gene, relaxin-like receptor 2 (RXFP2). We found that an allele conferring larger horns, Ho(+), is associated with higher reproductive success, whereas a smaller horn allele, Ho(P), confers increased survival, resulting in a net effect of overdominance (that is, heterozygote advantage) for fitness at RXFP2. The nature of this trade-off is simple relative to commonly proposed explanations for the maintenance of sexually selected traits, such as genic capture ('good genes') and sexually antagonistic selection. Our results demonstrate that by identifying the genetic architecture of trait variation, we can determine the principal mechanisms maintaining genetic variation in traits under strong selection and explain apparently counter-evolutionary observations.

Sexually selected skin colour is heritable and related to fecundity in a non-human primate

“…At 25-30%, skin darkness reaches levels of heritability similar to those reported for male body size and weaponry more commonly encountered in mammals (e.g. white-tailed deer, Odocoileus virginianus [66]; red deer, Cervus elaphus [67]; Soay sheep [7]). The difference between skin redness and darkness in patterns of selection and heritability is likely to be linked to the underlying mechanisms involved in expression of the signal.…”

“…Another mechanism of balancing selection is overdominance in which variation is maintained because the most successful males are heterozygous (e.g. Soay sheep, Ovis aries [7]). Finally, it remains possible that in some cases, traits have indeed been under strong directional selection and that the inter-individual variation in traits perceived by human observers or detected by our measuring tools is unrelated to variation in reproductive output, such that the perceived variation is not biologically meaningful.…”

International Union of Basic and Clinical Pharmacology. XCV. Recent Advances in the Understanding of the Pharmacology and Biological Roles of Relaxin Family Peptide Receptors 1–4, the Receptors for Relaxin Family Peptides

“…Thus INSL3 may have a role in bone physiology, and RXFP2 mutations may be linked with osteoporosis in men (Ferlin et al, 2013). Interestingly, recent studies suggest that RXFP2 is associated with horn growth in sheep (Johnston et al, 2013) and cows (Wiedemar et al, 2014), suggesting actions of INSL3 on bone is a common feature in male mammals.…”

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

“…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.…”