Mechanisms of Assortative Mating in Speciation with Gene Flow: Connecting Theory and Empirical Research

Abstract

The large body of theory on speciation with gene flow has brought to light fundamental differences in the effects of two types of mating rules on speciation: preference/trait rules, in which divergence in both (female) preferences and (male) mating traits is necessary for assortment, and matching rules, in which individuals mate with like individuals on the basis of the presence of traits or alleles that they have in common. These rules can emerge from a variety of behavioral or other mechanisms in ways that are not always obvious. We discuss the theoretical properties of both types of rules and explain why speciation is generally thought to be more likely under matching rather than preference/trait rules. We furthermore discuss whether specific assortative mating mechanisms fall under a preference/trait or matching rule, present empirical evidence for these mechanisms, and propose empirical tests that could distinguish between them. The synthesis of the theoretical literature on these assortative mating rules with empirical studies of the mechanisms by which they act can provide important insights into the occurrence of speciation with gene flow. Finally, by providing a clear framework we hope to inspire greater alignment in the ways that both theoreticians and empiricists study mating rules and how these rules affect speciation through maintaining or eroding barriers to gene flow among closely related species or populations.

Vocal divergence is concordant with genomic evidence for strong reproductive isolation in grasshopper mice (Onychomys)

“…Alternatively, the call frequency shift in sympatric O. arenicola may reflect response to selection to minimize reproductive interactions with O. torridus . Since both sexes call and calls are sexually monomorphic, divergence in call frequency and the frequency to which conspecifics respond could be explained by a simple matching rule whereby animals respond to call frequencies that match their own (Kopp et al, ). Under this model, selection to minimize reproductive interactions with O. torridus could drive call divergence if, for example, O. arenicola with lower frequency calls had lower reproductive success because they attracted (and were attracted to) O. torridus more often than animals with higher frequency calls.…”

Sexual imprinting and speciation between two Peromyscus species

“…Under a “one‐allele mechanism” of reproductive isolation, a single allele yields assortative mating—for example, because of self‐referent matching, mechanical assortment, or philopatry (Kopp et al. ). Sexual imprinting, a process in which offspring learn to prefer familial traits at a young age (i.e., those of a mother, father, or siblings), has been considered an “one‐allele mechanism” (Verzijden et al.…”

Does divergent selection predict the evolution of mate preference and reproductive isolation in the tropical butterfly genus Melinaea (Nymphalidae: Ithomiini)?

“…Synchrony between assortative mating and divergent selection can trigger rapid speciation. Indeed, when mate choice is based on an ecologically important trait, divergence in that trait can facilitate reproductive isolation and speciation, even with gene flow (Kopp et al., ; Servedio et al., and references therein). Mimicry is a good example of a trait under strong ecological divergent selection that can also be used as a mating cue, and this has been shown for many different organisms, including fish (Hypoplectrus coral reef fishes: Puebla, Bermingham, Guichard, & Whiteman, ), frogs (Dendrobates: Reynolds & Fitzpatrick, ) and butterflies (Heliconius: Jiggins et al., ; Merrill et al., ).…”