How phenotypic matching based on neutral mating cues enables speciation in locally adapted populations

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.

Sexual imprinting leads to speciation in locally adapted populations

“…. Our results show quantitatively the balance required mechanism by which sexual imprinting is achieved, but results are nearly identical if offspring imprint on one of the parents, fathers, say, because this case differs from strict phenotype matching only for the case of DD offspring of CD X CD parents(Sibly et al, 2019).…”

“…To see if, given a suitable mechanism for phenotype matching, local adaptation leads to speciation if a new neutral mating trait arises by mutation, we ran computer simulations of a model developed from Sibly et al (2019) and applied it to the cases of local adaptation shown in Figure 2. In the model of Sibly et al (2019), one of the local adaptation alleles is dominant to the other, but now we need to accommodate intermediate dominance as shown in Table 1.…”

“…Here we study the case that initial variation in the mating trait is the result of a mutation in the mating trait in populations that already differ in an ecological trait as a result of local adaptation. This case was studied by Sibly et al (2019), who used a simple diploid population genetic model to show how phenotypic matching based on neutral mating cues enables speciation in locally adapted populations. Crucially, the mating cues occur at a locus not linked to the adaptation locus.…”

“…Crucially, the mating cues occur at a locus not linked to the adaptation locus. Sibly et al's (2019) analysis revealed that in the presence of local adaptation a mating trait can rapidly enable speciation given a suitable mechanism for phenotype matching. Only a limited number of cases of local adaptation were examined, however, so this raises the question, studied here, as to whether speciation is favored wherever local adaptation exists.…”

“…We begin with a systematic study to map the migration rates and selection strengths that allow the existence of local adaptation (i.e., migration‐selection balance). Then we extend the model of Sibly et al (2019) to include intermediate levels of dominance, and apply this extended model to our map of the set of migration and selection rates for which local adaptations can occur. This shows that local adaptations always lead to speciation if a new neutral mating trait arises by mutation.…”