Coevolution of male and female mate choice can destabilize reproductive isolation

Thomas G Aubier,Mathieu Joron,Hanna Kokko

doi:10.1038/s41467-019-12860-9

Abstract

Sexual interactions play an important role in the evolution of reproductive isolation, with important consequences for speciation. Theoretical studies have focused on the evolution of mate preferences in each sex separately. However, mounting empirical evidence suggests that premating isolation often involves mutual mate choice. Here, using a population genetic model, we investigate how female and male mate choice coevolve under a phenotype matching rule and how this affects reproductive isolation. We show that the evolution of female preferences increases the mating success of males with reciprocal preferences, favouring mutual mate choice. However, the evolution of male preferences weakens indirect selection on female preferences and, with weak genetic drift, the coevolution of female and male mate choice leads to periodic episodes of random mating with increased hybridization (deterministic ‘preference cycling’ triggered by stochasticity). Thus, counterintuitively, the process of establishing premating isolation proves rather fragile if both male and female mate choice contribute to assortative mating.

Highlights

Sexual interactions play an important role in the evolution of reproductive isolation, with important consequences for speciation
We model the evolution of assortative mating in sympatry, based on three diploid biallelic loci that segregate independently
Preference cycling may occur if the evolution of choosiness leads to nearly perfect reproductive isolation between ecotypes. This is the case if choosiness per se is nearly perfect (Supplementary Figs. 13 and 14), or if reproductive isolation is strengthened by additional barriers to gene flow. Under these conditions, which intuitively seem conducive to speciation, we show that coevolution of male and female choosiness has the potential to strongly destabilize reproductive isolation

Summary

Introduction

Sexual interactions play an important role in the evolution of reproductive isolation, with important consequences for speciation. Of particular interest is the case of homotypic mate preferences (“matching mating rule”11), where individuals preferentially choose mates with which they share phenotypic traits such as colors[12,13] or acoustic signals[14] When these traits are simultaneously under divergent or disruptive ecological selection (socalled “magic traits”15,16), choosy individuals with homotypic mate preferences are less likely to produce offspring with unfit intermediate phenotypes. This effect creates indirect selection favoring a further increase in choosiness (i.e., stronger homotypic preferences), establishing, or strengthening premating isolation between diverging populations[11,17,18,19,20,21,22]. Under idealized conditions of polygyny and unlimited male mating potential, males can be thought of as an unlimited resource for females and all females have equal mating success[33]

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Results

Conclusion