Abstract

Maynard Smith's (American Naturalist, 1966, 100, 637) suggestion that in some cases a prerequisite for speciation is the existence of local ecological adaptations has not received much attention to date. Here, we test the hypothesis using a model like that of Maynard Smith but differing in the way animals disperse between niches. In previous studies, males disperse randomly between niches but females stay put in their natal niche. As a first step toward generalizing the model, we here analyze the case that equal proportions of the two sexes disperse between niches before breeding. Supporting Maynard Smith's (1966) hypothesis, we find that once local adaptations are established, a neutral mating cue at an independent locus can rapidly enable speciation in populations with a suitable mechanism for phenotype matching. We find that stable ecological polymorphisms are relatively insensitive to the strength of selection, but depend crucially on the extent of dispersal between niches, with a threshold of ~5% if population sizes in two niches are equal. At higher levels of dispersal, ecological differentiation is lost. These results contrast with those of earlier studies and shed light on why parapatric speciation is limited by the extent of gene flow. Our testable model provides a candidate explanation for the rapid speciation rates, diversity of appearance and occurrence of “species flocks” observed among some African cichlids and neotropical birds and may also have implications for the occurrence of punctuational change on phylogenies.

Highlights

  • Darwin identified the importance of mate choice in allowing females to discriminate between potential mates, but missed its potential role in avoiding cross‐species mating (Bastock, 1967)

  • We find that stable ecological polymorphisms are relatively insensitive to the strength of selection, but depend crucially on the extent of dispersal between niches, with a threshold of ~5% if population sizes in two niches are equal

  • Our results support Maynard Smith's (1966) suggestion that in some cases a prerequisite for speciation is the existence of local ecologi‐ cal adaptations

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Summary

| INTRODUCTION

Darwin identified the importance of mate choice in allowing females to discriminate between potential mates, but missed its potential role in avoiding cross‐species mating (Bastock, 1967). |2 here quantitative conditions for speciation, in the presence of gene flow between ecological niches, that is consistent with established mechanisms of mate choice Two such mechanisms are sexual im‐ printing and phenotype matching achieved through self‐referential pleiotropy we term Matchmaker. In Heliconius butterflies, a single gene encodes both female wing pattern (white or yellow spot color) and male preference for that pattern (Naisbit, Jiggins, & Mallet, 2003) Both sexual imprinting and Matchmaker can produce assortative mating, but despite extensive theoretical effort (reviewed in Butlin et al, 2012; Gavrilets, 2004; Gavrilets, 2014; Kopp et al, 2018; Yeh & Servedio, 2015), more analysis is needed of how these mate‐choice mechanisms affect speciation in the presence of local genetic adapta‐ tion to differing ecological niches. We consider priorities for future theoretical work, suggest field testing of predictions of where higher diversity is to be expected, and discuss the implications of our results for rates of speciation, factors promoting diversity, and the selective forces that keep the underlying neurophysiological mechanisms in place

| METHODS
| DISCUSSION
Findings
CONFLICT OF INTEREST
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