Multilocus Models of Sympatric Speciation: Bush Versus Rice Versus Felsenstein

Abstract

In populations of phytophagous insects that use the host plant as a rendezvous for mating, divergence in host preference could lead to sympatric speciation. Speciation requires the elimination of "generalist" genotypes, that is, those with intermediate host preference. This could occur because such genotypes have an inherent fitness disadvantage, or because preference alleles become associated with alleles that are oppositely selected on the two hosts. Although the former mechanism has been shown to be plausible, the latter mechanism has not been studied in detail. I consider a multilocus model (the "Bush model") in which one set of biallelic loci affects host preference, and a second set affects viability on the hosts once chosen. Alleles that increase viability on one host decrease viability on the other, and all loci are assumed to be unlinked. With moderately strong selection on the viability loci, preference alleles rapidly become associated with viability alleles, and the population splits into two reproductively isolated host specialist populations. The conditions for speciation to occur in this model, as measured by the strength of selection required, are somewhat more stringent than in a model in which preference and viability are controlled by the same loci (one-trait model). In contrast, the conditions are much less stringent than in a model in which speciation requires buildup of associations between viability loci and loci controlling a host-independent assortative mating trait (canonical two-trait model). Moreover, in the one-trait model, and to a lesser extent the Bush model, the strength of selection needed to initiate speciation is only slightly greater than that needed to complete it. This indicates that documenting instances of sympatric species that are reproductively isolated only by host or habitat preference would provide evidence for the plausibility of sympatric speciation in nature.

Theoretical predictions strongly support decision accuracy as a major driver of ecological specialization

“…The central results of this study (that extreme specialists outperform extreme generalists cognitively when, and only when, the fitness consequences of using a non-host resource are neutral or slightly positive) are important, following as they do a succession of theoretical models that essentially indicate increased suitability of non-host resources inhibits specialization and attendant speciation (19)(20)(21)(22)(23). Although some models have indicated that specialization can be promoted despite nonnegative fitness correlations of different resources (24)(25)(26), to our knowledge, this is the first study to have some degree of suitability of non-hosts as a necessary central component.…”

On the scent of speciation: the chemosensory system and its role in premating isolation

“…Where local adaptation selects for habitat preferences (for example, Fry, 2003), it can have a more direct impact on the evolution of habitat isolation. The most widely accepted scenario for the evolution of pollinator isolation involves geographic separation of plant populations, divergence in floral traits then occurring as a result of disruptive selective pressures exerted by pollinators: for instance, plant populations experiencing completely different groups of pollinators or experiencing very different pollinator's preferences due to changes of the chemical environment (Coyne and Orr, 2004).…”

Divergence with gene flow as facilitated by ecological differences: within-island variation in Darwin's finches

“…parapatric or purely sympatric speciation. One mechanism likely to be important here is strong disruptive selection (owing to competition or discrete resources) that acts on traits also linked to assortative mating (Fry 2003;Gavrilets 2004;Bolnick & Fitzpatrick 2007). 'Context 3' is hybridization between groups following their secondary contact, which can sometimes cause the formation of a new hybrid species (Seehausen 2004;Mallet 2007).…”