Ecological selection as the cause and sexual differentiation as the consequence of species divergence?

Abstract

Key conceptual issues about speciation go unanswered without consideration of non-mutually exclusive factors. With tests based on speciation theory, we exploit the island distribution and habitat differences exhibited by the Caribbean cricket Amphiacusta sanctaecrucis, and with an analysis of divergent ecological selection, sexually selected differentiation and geographical isolation, address how these different factors interact. After testing for divergent selection by comparing neutral genetic and morphological divergence in one ecological (mandible shape) and one sexual (male genitalia shape) trait, we examine whether ecological or sexual selection is the primary mechanism driving population divergence. We find that all three factors-isolation, ecological and sexual selection-contribute to divergence, and that their interaction determines the stage of completeness achieved during the speciation process, as measured by patterns of genetic differentiation. Moreover, despite the striking diversity in genitalic shapes across the genus Amphiacusta, which suggests that sexual selection drives speciation, the significant differences in genitalia shape between forest habitats revealed here implies that ecological divergence may be the primary axis of divergence. Our work highlights critical unstudied aspects in speciationdifferentiating the cause from the consequence of divergence-and suggests avenues for further disentangling the roles of natural and sexual selection in driving divergence in Amphiacusta.

Hemipenial Allometry inAnolis grahami

“…The study of genital variation should help not only to clarify the processes driving morphological evolution but also to understand the mechanisms of reproductive isolation and speciation (Oneal and Knowles, 2012). Indeed, closely related species often show diverged genitalia without remarkable differences in the nongenital morphology (Arnqvist, 1997), suggesting that genital traits may evolve rapidly and be an important component of reproductive isolation (Eberhard, 2009).…”

Community assembly in Lake Tanganyika cichlid fish: quantifying the contributions of both niche‐based and neutral processes

“…This may lead to an increase in the importance of limiting similarity, although depth segregation could manifest itself through heightened habitat filtering as well. Furthermore, a comparison between estimates obtained using only diet‐associated traits, using only traits associated with coloration and visual adaptation, or the combination of both these types of traits might partition the causes of diversity in causes directly related to diet, and causes more related to sexual selection, an ongoing debate in the literature (Doorn, Noest, & Hogeweg, 1998; Kocher, 2004; Maan & Seehausen, 2011; Oneal & Knowles, 2013; Seehausen et al., 2014; Sobel, Chen, Watt, & Schemske, 2010). …”

Genetic dissection of a major polymorphism underlying population divergence in sexually selected pheromones in Drosophila serrata

“…The mutation at hand is seemingly sexually antagonistic, affected by natural selection in females but through opposing sexual selection in males. The interaction between natural and sexual selection may significantly affect the manner in which traits evolve in nature (BLOWS 2002;RUNDLE et al 2009;HINE et al 2011;ONEAL and KNOWLES 2013). These two processes have been known to work in opposition under certain conditions (RUNDLE et al 2006;CANDOLIN and HEUSCHELE 2008) but usually within the same sex (DARWIN 1871;CANDOLIN and HEUSCHELE 2008).…”

“…When trait values favoured by sexual selection coincide with local adaptation, natural and sexual selection may work in unison (HINE et al 2011); divergent ecological selection pressures that enhance survival will also favour the evolution of unique sexual traits even in the face of gene flow (LANDE and KIRKPATRICK 1988; VAN DOORN et al 2009;ONEAL and KNOWLES 2013). Sexual selection can, likewise, also enhance adaptation (LORCH et al 2003;FRICKE and ARNQVIST 2007;CANDOLIN and HEUSCHELE 2008).…”

“…Within the context of adaptive speciation, for instance, natural and sexual selection reinforce each other's actions and the latter process may be regarded as a subset of the former ( VAN DOORN et al 2009). This notwithstanding, interaction between these two processes may substantially influence the direction and extent to which traits evolve in nature (BLOWS 2002;ONEAL and KNOWLES 2013). Sexual selection, renowned for aiding the persistence and exaggeration of seemingly detrimental traits (DARWIN 1871), may help in the purging of deleterious mutations (AGRAWAL 2001), sometimes favouring genotypes associated with enhanced survival or viability (ZAHAVI 1975;HAMILTON and ZUK 1982;KIRKPATRICK 1987) and lead to adaptive trait divergence (CANDOLIN and HEUSCHELE 2008).…”