Mutation‐order divergence by sexual selection: diversification of sexual signals in similar environments as a first step in speciation

Abstract

The origin of species remains a central question, and recent research focuses on the role of ecological differences in promoting speciation. Ecological differences create opportunities for divergent selection (i.e. 'ecological' speciation), a Darwinian hypothesis that hardly requires justification. In contrast, 'mutation-order' speciation proposes that, instead of adapting to different environments, populations find different ways to adapt to similar environments, implying that speciation does not require ecological differences. This distinction is critical as it provides an alternative hypothesis to the prevailing view that ecological differences drive speciation. Speciation by sexual selection lies at the centre of debates about the importance of ecological differences in promoting speciation; here, we present verbal and mathematical models of mutation-order divergence by sexual selection. We develop three general cases and provide a two-locus population genetic model for each. Results indicate that alternative secondary sexual traits can fix in populations that initially experience similar natural and sexual selection and that divergent traits and preferences can remain stable in the face of low gene flow. This stable divergence can facilitate subsequent divergence that completes or reinforces speciation. We argue that a mutation-order process could explain widespread diversity in secondary sexual traits among closely related, allopatric species.

Behavioral Isolation due to Cascade Reinforcement in Lucania Killifish

“…Sexual selection can also cause behavioral isolation when the coevolution of mating traits and preferences leads to divergence between geographically separated populations (Ritchie 2007;M'Gonigle et al 2012). However, sexual selection rarely generates behavioral isolation between populations without some corresponding ecological divergence (Boughman 2001;Boughman et al 2005; Maan and Seehausen 2011; but see Mendelson et al 2014). Ecological divergence and reinforcement are frequent and interacting contributors to behavioral isolation (Nosil et al 2003;Pfennig and Pfennig 2010).…”

Consequences of divergence and introgression for speciation in Andean cloud forest birds

“…There is a strong expectation that gene flow will prevent divergence under mutation‐order conditions, a prediction that has generally been supported by population genetic simulations (Nosil and Flaxman ; Anderson and Harmon ; Mendelson et al. ). However, in contrast to widespread empirical demonstration of divergence in the face of gene flow among ecologically disparate populations (Nosil ; Schluter ; Marques et al.…”

“…Analyses are particularly lacking in systems wherein phenotypic differences among populations are not obviously coupled with environmental variation and thus speciation may be less likely to proceed via adaptive divergence (West‐Eberhard ; Svensson ; Langerhans and Riesch ; Mendelson et al. ).…”

“…For example, social selection may be involved in the plumage divergence of populations separated by the Marañón, but the mechanisms of social selection that drive and maintain phenotypic divergence in ecologically similar scenarios have received less attention than cases with an obvious link between phenotype, fitness in the environment, and mate choice (West‐Eberhard ; Prum ; Martin and Mendelson ; Mendelson et al. ). How long must populations facing similar selection pressures be isolated to evolve differences in social signals important to speciation (Winger and Bates ; Cutter and Gray ; Zamudio et al.…”

Limited flexibility in female Pacific field cricket (Teleogryllus oceanicus) exploratory behaviors in response to perceived social environment

“…Sexual signals are critical for successful reproduction and maintenance of species boundaries because they are often required for mate localization and attraction. Thus, rapid changes in sexual traits can pose major implications for the signaler, receiver, and population viability (Mendelson, Martin, & Flaxman, ; Panhuis, Butlin, Zuk, & Tregenza, ; Safran, Scordato, Symes, Rodriguez, & Mendelson, ). Understanding how populations adapt, or not, to such a dramatic shift in the mating system is of critical importance, but remains difficult to study because so few contemporary examples of rapid sexual signal evolution are known (Svensson & Gosden, ).…”