The dilemma of Fisherian sexual selection: Mate choice for indirect benefits despite rarity and overall weakness of trait-preference genetic correlation

Abstract

Fisher's mechanism of sexual selection is a fundamental element of evolutionary theory. In it nonrandom mate choice causes a genetic covariance between a male trait and female preference for that trait and thereby generates a positive feedback process sustaining accelerated coevolution of the trait and preference. Numerous theoretical models of Fisher's mechanism have confirmed its mathematical underpinnings, yet biologists have often failed to find evidence for trait-preference genetic correlation in populations in which the mechanism was expected to function. We undertook a survey of the literature to conduct a formal meta-analysis probing the incidence and strength of trait-preference correlation among animal species. Our meta-analysis found significant positive genetic correlations in fewer than 20% of the species studied and an overall weighted correlation that is slightly positive. Importantly, a significant positive correlation was not found in any thorough study that included multiple subgroups. We discuss several ways in which the dynamic, multivariate nature of mate choice may reduce the trait-preference genetic correlation predicted by Fisher's mechanism. We then entertain the possibilities that Fisherian-like processes sometimes function without genetic correlation, and that mate choice may persist in a population as long as genetic correlation, and therefore Fisher's mechanism, occurs intermittently. Fisher's mechanism of sexual selection (Fisher 1915(Fisher , 1930(Fisher , 1958 has dominated biological thought on the genetics of mate choice over the past 40 years. The mechanism is central to most sexual selection models (Prum 2010) and has been formally modeled on numerous occasions beginning in the early 1980s (O'Donald

Indirect genetic effects in behavioral ecology: does behavior play a special role in evolution?

“…Accumulation of genetic covariances between sexual traits and preferences are a fundamental property of Fisher's original model of sexual selection (Fisher 1915(Fisher , 1958, but incorporating IGEs counterintuitively suggested that trait-preference covariances can be smaller than expected while still allowing runaway to occur. This finding may help to reconcile a pervasive lack of evidence for expected trait/preference genetic covariances in empirical studies (Greenfield et al 2014). IGEs have also been modeled in sexual conflict scenarios, and when strong, they are predicted to stimulate rapid evolutionary proliferation of adaptations and counter-adaptations above standard predicted rates (Moore and Pizzari 2005).…”

Mate-choice copying: A fitness-enhancing behavior that evolves by indirect selection

“…Our assumption that innate preferences do not alter female survival or fecundity and might coevolve with the male traits violates this conclusion. This suggests that Fisherian sexual selection might be widespread, and also that there might be a long-term balance between the loss of genetic variation and other forces such as mutation, migration, and changes in the direction of selection that maintain genetic variation for preference (Bakker and Pomiankowski 1995; Greenfield et al 2014). This suggests that Fisherian sexual selection might be widespread, and also that there might be a long-term balance between the loss of genetic variation and other forces such as mutation, migration, and changes in the direction of selection that maintain genetic variation for preference (Bakker and Pomiankowski 1995; Greenfield et al 2014).…”

The causes of variation in the presence of genetic covariance between sexual traits and preferences

“…It has been nearly 20 years since the first comprehensive review of studies on the topic (Bakker & Pomiankowski, ), and in the intervening time, there has been a substantial increase in the number of empirical tests for trait–preference genetic covariance. A recent review examining the incidence of trait–preference covariance among studies testing for covariance in the same species found overall weak levels of covariance but a large range of variation in its strength (Greenfield et al ., ). Here we aim to explain this type of variation in results by examining potential underlying factors determining whether covariance is detected or not.…”