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


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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    • "The breeding grounds of lake and stream fish thus certainly overlap (at least in streams where physical dispersal barriers are absent), providing the opportunity for lake-stream gene flow. However, phenotypic plasticity maintains a prominent body size difference between the habitats, and body size to govern reproductive interactions in several population within this species (Dufresne et al. 1990; Nagel and Schluter 1998; Ishikawa and Mori 2000; Albert 2005; Boughman et al. 2005; McKinnon et al. 2004, 2012; Conte and Schluter 2013). We therefore propose that in lake and stream stickleback in the Lake Constance basin, the colonization of ecologically distinct habitats immediately promotes reproductive isolation via sexual barriers. "
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    ABSTRACT: Speciation can be promoted by phenotypic plasticity if plasticity causes populations in ecologically different habitats to diverge in traits mediating reproductive isolation. Although this pathway can establish reproductive barriers immediately and without genetic divergence, it remains poorly investigated. In threespine stickleback fish, divergence in body size between populations represents a potent source of reproductive isolation because body size often influences reproductive behavior. However, the relative contribution of phenotypic plasticity and genetically based divergence to stickleback body size evolution has not been explored. We here do so by using populations residing contiguously in Lake Constance (Central Europe) and its tributaries, a system where lake fish exhibit strikingly larger size and greater age at maturity than stream fish. Laboratory experiments reveal the absence of substantial genetic divergence in intrinsic growth rates and maturation size thresholds between lake and stream fish. A field transplant experiment further demonstrates that lake fish display the life history typical of stream fish when exposed to stream habitats for one year, confirming that life history divergence in this system is mainly plastic. This plasticity appears to be driven by restricted food availability in the lake relative to the stream habitat. We thus propose that in this stickleback system, the exploitation of different trophic niches immediately promotes reproductive isolation via resource-based plasticity in life history.
    Evolutionary Biology 05/2015; 42(3). DOI:10.1007/s11692-015-9327-6 · 2.61 Impact Factor
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    • "Divergent natural selection between distinct feeding and mating habitats has generated species dierences in color, size, and shape (Bentzen and McPhail 1984; Bentzen et al. 1984; Schluter 1993, 1995; Boughman 2001), each of which females pay attention to during mate choice within and/or between species (Nagel and Schluter 1998; Boughman 2001; Boughman et al. 2005; Head et al. 2009; Kozak et al. 2009; Conte and Schluter 2013; Head et al. 2013). Furthermore, these male traits are at least in part environmentally mediated (male nuptial color: Boughman 2001; Lewandowski and Boughman 2008, body size: Nagel and Schluter 1998; McKinnon et al. 2004; Boughman et al. 2005, body shape: Day et al. 1994; Day and McPhail 1996; Head et al. 2013). Sexual selection via male competition also generates divergent selection on male traits in dierent habitats (Lackey and Boughman 2013a). "
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    ABSTRACT: Environmental differences can cause reproductive isolation to evolve. Distinct habitats can be particularly important for the evolution of genetically based sexual isolation, which occurs when divergent preferences and mating traits reduce mating between species. Yet, we know little about environmental effects on the potentially plastic expression, and thus the current maintenance, of sexual isolation. This is especially intriguing in the context of reverse speciation, where previously isolated taxa begin hybridizing and merge. Environmental change could weaken reproductive isolation underlain by plastic traits even before any genetic change occurs. Here, we examine how differences in mating habitats affect the expression of both female discrimination between species and male traits that underlie sexual isolation. We used 2 species pairs of threespine stickleback fish (Gasterosteus spp.): an intact species pair and a formerly distinct but now hybridizing species pair, where habitat change presumably triggered reverse speciation. The expression of female discrimination was fairly insensitive to habitat, despite the central importance of habitat differences to the initial evolution of sexual isolation. Only the ecotype being subsumed by hybridization showed habitat sensitivity, suggesting this plasticity may have contributed to reverse speciation either as a cause or consequence of gene flow. Also, we found plasticity in male courtship across habitats that could further erode sexual isolation. Thus, environmental differences may play different roles in the genetic evolution versus plastic maintenance of sexual isolation, with implications for the forward versus reverse processes of speciation.
    Behavioral Ecology 07/2014; 25(5). DOI:10.1093/beheco/aru111 · 3.18 Impact Factor
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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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    ABSTRACT: Measuring sexual selection in changing environments is challenging, as the targets and mechanisms of selection can vary with the environment. Here, we present the results of an unusually comprehensive study of the influence of human-disturbed habitat structure on sexual selection in the threespine stickleback Gasterosteus aculeatus. We included all episodes of sexual selection, used molecular parentage assignments, and applied several metrics of sexual selection. The results show that the influence of altered habitat structure on sexual selection dynamics is more complex than previously thought, with the influence varying among selection episodes and male groups. Increased habitat structure relaxed the opportunity for sexual selection across episodes, but incorrect conclusions were reached if the analysis was restricted to resource-holding males or based on mating success. A novel finding, revealed by the parentage analysis, is a reduction in sneak fertilization in disturbed environments. This relaxed the opportunity for sexual selection as sneaking had increased the skew in mating success in less structured habitats, because of nesting males with a high mating success sneaking the most. Thus, the influence of environmental change on an alternative reproductive behavior amplified alterations in sexual selection. This emphasizes the need to consider more hidden processes than previously done when investigating how human disturbances modify sexual selection.
    Evolutionary Biology 12/2013; 40(4). DOI:10.1007/s11692-013-9234-7 · 2.61 Impact Factor
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