A reexamination of theoretical arguments that indirect selection on mate preference is likely to be weaker than direct selection

Abstract

Female preference for male ornaments or displays can evolve by indirect selection resulting from genetic benefits of mate choices, or by direct selection resulting from nongenetic benefits or selection on sensory systems occurring in other contexts. In an influential paper, Kirkpatrick and Barton used a good‐genes model and evolutionary rates estimated from the fossil record to conclude that indirect selection on preference is likely to be weak compared to typical strengths of direct selection. More recent authors have extrapolated from Kirkpatrick and Barton's conclusions to suggest that the presence of preference‐trait genetic correlations in equations for indirect but not direct selection gives a purely theoretical basis to the conclusion that the former is likely to be weaker than the latter. Here, I challenge these views, and argue that the relative importance of direct and indirect selection on preference is an empirical issue that defies simple generalizations. First, I show that Kirkpatrick and Barton based their conclusion on a questionable claim about typical rates of evolution due to direct selection. Second, I argue that claiming that direct selection on preference is stronger than indirect selection because only equations for the latter contain a genetic correlation mistakes the mathematical simplicity with which direct selection is usually represented for evidence regarding its magnitude. By comparing a simple equation for the selection response of preference caused by somatic (“direct”) benefits to Kirkpatrick and Barton's result for the response to indirect selection, I show that indirect selection on preference is not inherently weaker than direct selection. I also point out an important but overlooked reason why selection on preference under the sensory bias hypothesis can be expected to be less effective in the long run than that from either somatic or genetic benefits of mate choices.

Genetic compatibility exceeds possible ‘good genes’ effects of sexual selection in lake char

“…of male health and vigor) are predicted to be conspicuous behaviors, morphology, and/or coloration [6]. Their information content could theoretically be high [18] but is expected to vary, for example, depending on male age in iteroparous species [19].…”

The evolution of mating preferences for genetic attractiveness and quality in the presence of sensory bias

“…In contrast, “good genes” models posit that ornament expression is correlated with other aspects of genetic quality, such as fecundity, viability, or survival ( 10 , 17 – 22 ). Such correlations can be generated by condition-dependent life-history strategies, but there is some debate over whether correlations are strong enough in practice to drive evolution ( 23 – 26 ). All of the above models assume that mating preferences are largely adaptive.…”

A reformulation of Fisher's runaway identifies the heritability of mate choices as a key parameter and highlights limitations of the hypothesis

“…parental care, good genes). Unlike the situation for the runaway, however, under either good-genes or direct-benefit models, there is no threshold hM2 for preference to evolve, as long as it is not zero [48,49]. Evolution to the equilibrium may take a long time, but selection has many generations to work with.…”

“…In this respect, even though the hypothesis that male display traits are essentially arbitrary outcomes of a runaway process is often lumped with the good-genes hypothesis because both involve indirect selection on preference, the good-genes hypothesis has more in common with hypotheses based on direct benefits such as parental care. Moreover, there is no mathematical basis to the claim sometimes made (see [49] for references) that selection on preference resulting from genetic benefits is inherently weaker than that resulting from non-genetic benefits because of the dependence of the former on a genetic correlation [49]. (Authors making this argument have also overlooked the fact that for a display trait to evolve as an indicator of direct benefits, there would need to be a genetic correlation between female preference for the trait and degree of male investment in it [48].…”