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Abstract Influential models of speciation by sexual selection posit either a single shared preference for a universal display, expressed only when males are locally adapted and hence in high condition, or that shared loci evolve population‐specific alleles for displays and preferences. However, many closely related species instead show substantial differences across categorically different traits. We present a model of secondary contact whereby females maintain preferences for distinct displays that indicate both male condition and their match to distinct environments, fostering reproductive isolation among diverging species. This occurs even with search costs and with independent preference loci targeting independent displays. Such preferences can also evolve from standing variation. Divergence occurs because condition‐dependent display and female preference depend on local ecology, and females obtain different benefits of choice. Given the ubiquity of ecological differences among environments, our model could help explain the evolution of striking radiations of displays seen in nature.more » « less
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Synopsis The peripheral sensory systems, whose morphological attributes help determine the acquisition of distinct types of information, provide a means to quantitatively compare multiple modalities of a species’ sensory ecology. We used morphological metrics to characterize multiple sensory modalities—the visual, olfactory, and mechanosensory lateral line sensory systems—for Gasterosteus aculeatus, the three-spined stickleback, to compare how sensory systems vary in animals that evolve in different ecological conditions. We hypothesized that the dimensions of sensory organs and correlations among sensory systems vary in populations adapted to marine and freshwater environments, and have diverged further among freshwater lake-dwelling populations. Our results showed that among environments, fish differed in which senses are relatively elaborated or reduced. When controlling for body length, littoral fish had larger eyes, more neuromasts, and smaller olfactory tissue area than pelagic or marine populations. We also found differences in the direction and magnitude of correlations among sensory systems for populations even within the same habitat type. Our data suggest that populations take different trajectories in how visual, olfactory, and lateral line systems respond to their environment. For the populations we studied, sensory modalities do not conform in a predictable way to the ecological categories we assigned.more » « less
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ABSTRACT A major goal of evolutionary science is to understand how biological diversity is generated and altered. Despite considerable advances, we still have limited insight into how phenotypic variation arises and is sorted by natural selection. Here we argue that an integrated view, which merges ecology, evolution and developmental biology (eco evo devo) on an equal footing, is needed to understand the multifaceted role of the environment in simultaneously determining the development of the phenotype and the nature of the selective environment, and how organisms in turn affect the environment through eco evo and eco devo feedbacks. To illustrate the usefulness of an integrated eco evo devo perspective, we connect it with the theory of resource polymorphism (i.e. the phenotypic and genetic diversification that occurs in response to variation in available resources). In so doing, we highlight fishes from recently glaciated freshwater systems as exceptionally well‐suited model systems for testing predictions of an eco evo devo framework in studies of diversification. Studies on these fishes show that intraspecific diversity can evolve rapidly, and that this process is jointly facilitated by (i) the availability of diverse environments promoting divergent natural selection; (ii) dynamic developmental processes sensitive to environmental and genetic signals; and (iii) eco evo and eco devo feedbacks influencing the selective and developmental environments of the phenotype. We highlight empirical examples and present a conceptual model for the generation of resource polymorphism – emphasizing eco evo devo, and identify current gaps in knowledge.more » « less
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Individuals can reduce sampling costs and increase foraging efficiency by using information provided by others. One simple form of social information use is delayed local enhancement or increased interest in a location because of the past presence of others. We tested for delayed local enhancement in two ecomorphs of stickleback fish, benthic and limnetic, from three different lakes with putative independent evolutionary origins. Two of these lakes have reproductively isolated ecomorphs (species-pairs), whereas in the third, a previously intact species-pair recently collapsed into a hybrid swarm. Benthic fish in both intact species-pair lakes were more likely to exhibit delayed local enhancement despite being more solitary than limnetic fish. Their behaviour and morphology suggest their current perceived risk and past evolutionary pressure from predation did not drive this difference. In the hybrid swarm lake, we found a reversal in patterns of social information use, with limnetic-looking fish showing delayed local enhancement rather than benthic-looking fish. Together, our results strongly support parallel differentiation of social learning differences in recently evolved fish species, although hybridization can apparently erode and possibly even reverse these differences.more » « less
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Human-induced changes in climate and habitats push populations to adapt to novel environments, including new sensory conditions, such as reduced visibility. We studied how colonizing newly formed glacial lakes with turbidity-induced low-visibility affects anti-predator behaviour in Icelandic threespine sticklebacks. We tested nearly 400 fish from 15 populations and four habitat types varying in visibility and colonization history in their reaction to two predator cues (mechano-visual versus olfactory) in high versus low-visibility light treatments. Fish reacted differently to the cues and were affected by lighting environment, confirming that cue modality and light levels are important for predator detection and evasion. Fish from spring-fed lakes, especially from the highlands (likely more diverged from marine fish than lowland fish), reacted fastest to mechano-visual cues and were generally most active. Highland glacial fish showed strong responses to olfactory cues and, counter to predictions from the flexible stem hypothesis, the greatest plasticity in response to light levels. This study, leveraging natural, repeated invasions of novel sensory habitats, (i) illustrates rapid changes in anti-predator behaviour that follow due to adaptation, early life experience, or both, and (ii) suggests an additional role for behavioural plasticity enabling population persistence in the face of frequent changes in environmental conditions.more » « less
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Males in many species have elaborated sexual traits that females strongly prefer, and these traits often conspicuously differ among species. How novel preferences and traits originate, however, is a challenging evolutionary problem because the initial appearance of only the female preference or only the male trait should reduce the ability to find a suitable mate, which could reduce fitness for individuals possessing those novel alleles. Here, we present a hypothesis for how novel preferences, as well as the novel male traits that females prefer, can originate, be favoured and spread in polyandrous species. Novel preference mutations can arise as ‘veiled preferences’ that are not expressed when the corresponding male trait is not present in the population, allowing preferences to be hidden from selection, and thus persist. In those cases when a male trait is present, veiled preferences provide a selective advantage, and females disproportionately produce offspring from preferred males through either mate choice or cryptic female choice. This tips the fitness advantage for novel males, allowing both preference and trait to spread, and limiting selection against them in the absence of the corresponding trait or preference.more » « less