Adaptive speciation theory: a conceptual review

Abstract

Speciation—the origin of new species—is the source of the diversity of life. A theory of speciation is essential to link poorly understood macro-evolutionary processes, such as the origin of biodiversity and adaptive radiation, to well understood micro-evolutionary processes, such as allele frequency change due to natural or sexual selection. An important question is whether, and to what extent, the process of speciation is ‘adaptive’, i.e., driven by natural and/or sexual selection. Here, we discuss two main modelling approaches in adaptive speciation theory. Ecological models of speciation focus on the evolution of ecological differentiation through divergent natural selection. These models can explain the stable coexistence of the resulting daughter species in the face of interspecific competition, but they are often vague about the evolution of reproductive isolation. Most sexual selection models of speciation focus on the diversification of mating strategies through divergent sexual selection. These models can explain the evolution of prezygotic reproductive isolation, but they are typically vague on questions like ecological coexistence. By means of an integrated model, incorporating both ecological interactions and sexual selection, we demonstrate that disruptive selection on both ecological and mating strategies is necessary, but not sufficient, for speciation to occur. To achieve speciation, mating must at least partly reflect ecological characteristics. The interaction of natural and sexual selection is also pivotal in a model where sexual selection facilitates ecological speciation even in the absence of diverging female preferences. In view of these results, it is counterproductive to consider ecological and sexual selection models as contrasting and incompatible views on speciation, one being dominant over the other. Instead, an integrative perspective is needed to achieve a thorough and coherent understanding of adaptive speciation.

Disruptive ecological selection on a mating cue

“…Theoretical work suggests that traits under disruptive selection also used as mating cues (i.e. magic traits) may be especially effective in promoting speciation because they will form strong genetic associations with loci underlying premating isolation, and that use these cues as markers [4,5,8,38]. Despite this, it is perhaps often overlooked that the existence of magic traits does not make speciation automatic or inevitable [9].…”

“…Alternatively, selection acting against maladaptive hybrids may drive the evolution of assortative mating through reinforcement. This latter process is often invoked in the models of speciation where gene flow persists [4,5], but it relies on establishing linkage disequilibrium between genes under disruptive selection and those underlying assortative mating. Somehow the force of disruptive selection acting on the ecological trait needs to be transmitted to genes responsible for pre-mating isolation [6].…”

A dated molecular phylogeny of manta and devil rays (Mobulidae) based on mitogenome and nuclear sequences

“…Kashiwagi et al (2012) hypothesized that habitat specialization probably played an important role in the evolution of M. birostris and M. alfredi, since the two species generally exhibit habitat segregation between near-shore (M. alfredi) and offshore (M. birostris) environments (Marshall et al, 2009). Alternatively, due to the enormous migratory potential of (especially) M. birostris, it is conceivable that behavioral isolation and/or sexual selection for, e.g., size, played a more fundamental role in the divergence of the two species (Edelaar et al, 2008;Head et al, 2013;Weissing et al, 2011). Recently, a hybrid between M. alfredi and M. birostris was identified in the Red Sea, based on sequence analysis of the nuclear gene RAG1, which was heterozygous for two species-specific single nucleotide polymorphisms (Walter et al, 2014).…”

Within-host competition and diversification of macro-parasites

“…The theory of competitive speciation has been broadly extended in the last 10 years, using a wide range of models typically assuming that a quantitative trait is under disruptive selection generated by frequency and density-dependent intraspecific competition [24,25]. Some models consider that the ecological trait pleiotropically affects mate choice [26][27][28], while others explicitly describe the evolution of mating preferences according to the ecological trait under natural selection [26][27][28][29][30] or an additional neutral trait [26,31].…”