Maintenance of genetic variation in sexual ornaments: a review of the mechanisms

Abstract

Female preferences for elaborate male sexual traits have been documented in a number of species in which males contribute only genes to the next generation. In such systems, mate choice has been hypothesised to benefit females genetically. For the genetic benefits to be possible there must be additive genetic variation (V A) for sexual ornaments, such that highly ornamented males can pass fitter genes on to the progeny of choosy females. Here, I review the mechanisms that can contribute to the maintenance of this variation. The variation may be limited to sexual ornaments, resulting in Fisherian benefits in terms of the increased reproductive success of male progeny produced by choosy females. Alternatively, ornaments may capture V A in other life-history traits. In the latter case, "good genes" benefits may apply in terms of improved performance of the progeny of either sex. Some mechanisms, however, such as negative pleiotropy, sexually antagonistic variation or overdominance, can maintain V A in ornaments and other life-history traits with little variation in total fitness, leaving little room for any genetic benefits of mate choice. Distinguishing between these mechanisms has consequences not only for the theory of sexual selection, but also for evolution of sex and for biological conservation. I discuss how the traditional ways of testing for genetic benefits can usefully be supplemented by tests detecting benefits resulting from specific mechanisms maintaining V A in sexual ornaments.

A General Population Genetic Framework for Antagonistic Selection That Accounts for Demography and Recurrent Mutation

“…However, such criteria for maintaining genetic variation are overly conservative because recurrent mutation also maintains genetic variation in the absence of balancing selection (see Lynch and Walsh 1998, pp. 655-656;Radwan 2008). Assessing the potential impact of antagonistic selection on patterns of genetic variation requires a theoretical analysis of the full range of allele frequency dynamics and equilibria within balancing and nonbalancing selection domains of parameter space.…”

“…First, because the necessary parameter conditions for balancing selection are often highly restrictive, the contribution of antagonistically selected mutations to population or quantitative genetic variation is often predicted to be minor (e.g., Curtsinger et al 1994;Hedrick 1999). This interpretation has been criticized, as it ignores the important interaction between selection and recurrent mutation that likely mediates a large proportion of molecular and fitness variation, genome-wide (Lynch and Walsh 1998;Radwan 2008). Nevertheless, few theoretical studies explicitly consider mutation-selection equilibrium variation for antagonistically selected loci and how this might compare to a null model of variation maintained at nonantagonistically selected loci.…”

Queuing in space and time reduces the lek paradox on an antelope lek

“…Neglecting this can lead to inflated estimates of both the degree of male mating skew and the link between this mating skew and indirect benefits. I here show that directional selection on male genotypes in lekking species may be less extreme than widely believed due to queuing tactics in both space and time, and that this not a trivial point is borne out by the fact that the solutions proposed for the lek paradox are generally more plausible under weak than strong selection (Kotiaho et al 2001(Kotiaho et al , 2008Tomkins et al 2004;Petrie and Roberts 2007;Radwan 2008;Hall et al 2010).…”

“…Lek systems have inspired a considerable body of evolutionary research because they present a clear-cut example of a fundamental conundrum: the persistence of costly female preferences for mates who provide only indirect additive genetic benefits (Borgia 1979;Radwan 2008). The puzzle arises because directional selection due to strong female mate choice is expected to lead to fixation of preferred male genes, which precludes any benefits of the female mate preference (Falconer 1981;Johnson and Barton 2005).…”

An introduction to genetic quality in the context of sexual selection

“…Radwan (2008) provides an exhaustive survey of the various hypotheses that have been presented as solutions to the lek paradox. Radwan reviews the mechanisms that can contribute to the maintenance of variation in additive genetic variation in sexual ornamentation (that female preference selects upon).…”