Article

Parallel Evolution of Sexual Isolation in Sticklebacks

Department of Zoology, University of Wisconsin, Madison, Wisconsin 53706, USA.
Evolution (Impact Factor: 4.61). 03/2005; 59(2):361-73. DOI: 10.1554/04-153
Source: PubMed

ABSTRACT

Mechanisms of speciation are not well understood, despite decades of study. Recent work has focused on how natural and sexual selection cause sexual isolation. Here, we investigate the roles of divergent natural and sexual selection in the evolution of sexual isolation between sympatric species of threespine sticklebacks. We test the importance of morphological and behavioral traits in conferring sexual isolation and examine to what extent these traits have diverged in parallel between multiple, independently evolved species pairs. We use the patterns of evolution in ecological and mating traits to infer the likely nature of selection on sexual isolation. Strong parallel evolution implicates ecologically based divergent natural and/or sexual selection, whereas arbitrary directionality implicates nonecological sexual selection or drift. In multiple pairs we find that sexual isolation arises in the same way: assortative mating on body size and asymmetric isolation due to male nuptial color. Body size and color have diverged in a strongly parallel manner, similar to ecological traits. The data implicate ecologically based divergent natural and sexual selection as engines of speciation in this group.

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    • "We evaluated the consequence of excluding non-nesting males from the analyses, and of using apparent mating success (amount of eggs guarded) instead of fertilizations success as the fitness measure. The measured male traits were male length and male weight, which are under sexual selection through both male–male competition and female mate choice (Rowland 1989; Largiader et al. 2001; Candolin and Voigt 2003; Boughman et al. 2005). Our sexual selection measurements could include a component of natural selection beyond sexual selection, as embryo survival depends also on nest site characteristics and male parental care (Ahnesjö et al. 2001). "

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    • "Additionally, there is some mate discrimination that is not based on ecological divergence. Males that occur in the same light environment but in separate lakes are phenotypically similar but females do discriminate against males that are not from their own lake (Rundle et al. 2000; Boughman et al. 2005). It is not known whether color divergence occurred as habitat divergence occurred, or whether these sexual signals evolved only after there was strong ecological divergence. "
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    ABSTRACT: Using experimental evolution, we investigated the contributions of ecological divergence, sexual selection, and genetic drift to the evolution of reproductive isolation in Caenorhabditis remanei. The nematodes were reared on two different environments for 100 generations. They were assayed for fitness on both environments after 30, 64, and 100 generations, and hybrid fitnesses were analyzed after 64 and 100 generations. Mating propensity within and between populations was also analyzed. The design allowed us to determine whether local adaptation was synchronous with pre- and post-zygotic reproductive isolation. Pre-zygotic isolation evolved quickly but was unconnected with adaptation to the divergent environments. Instead, pre-zygotic isolation was driven by mate preferences favoring individuals from the same replicate population. A bottleneck treatment, meant to enhance the opportunity for genetic drift, had no effect on pre-zygotic isolation. Post-zygotic isolation occurred in crosses where at least one population had a large fitness advantage in its 'home' environment. Taken together, our results suggest that pre-zygotic isolation did not depend on drift or adaptation to divergent environments, but instead resulted from differences in sexual interactions within individual replicates. Furthermore, our results suggest that post-zygotic isolation can occur between populations even when only one population has greater fitness in its home environment. This article is protected by copyright. All rights reserved.
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    • "For example, experimental and correlational evidence strongly establishes the importance of ecology in driving divergence between limnetic and benthic sticklebacks, including in traits we measured, such as size and shape (McPhail 1994;Head et al. 2013). Many of these traits have also been implicated in female choice (size and shape:Boughman et al. 2005;Conte & Schluter 2013;Head et al. 2013;colour: Boughman 2001;Boughman et al. 2005). Interestingly, the divergent selection from male competition we detected is synergistic with other sources of selection quantified in past studies. "
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    ABSTRACT: Speciation is facilitated when selection generates a rugged fitness landscape such that populations occupy different peaks separated by valleys. Competition for food resources is a strong ecological force that can generate such divergent selection. However, it is unclear whether intrasexual competition over resources that provide mating opportunities can generate rugged fitness landscapes that foster speciation. Here we use highly variable male F2 hybrids of benthic and limnetic threespine sticklebacks, Gasterosteus aculeatus Linnaeus, 1758, to quantify the male competition fitness landscape. We find that disruptive sexual selection generates two fitness peaks corresponding closely to the male phenotypes of the two parental species, favouring divergence. Most surprisingly, an additional region of high fitness favours novel hybrid phenotypes that correspond to those observed in a recent case of reverse speciation after anthropogenic disturbance. Our results reveal that sexual selection through male competition plays an integral role in both forward and reverse speciation.
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