Shared and unique patterns of embryo development in extremophile poeciliids

Background: Closely related lineages of livebearing fishes have independently adapted to two extreme environmental factors: toxic hydrogen sulphide (H2S) and perpetual darkness. Previous work has demonstrated in adult specimens that fish from these extreme habitats convergently evolved drastically increased head and offspring size, while cave fish are further characterized by reduced pigmentation and eye size. Here, we traced the development of these (and other) divergent traits in embryos of Poecilia mexicana from benign surface habitats (“surface mollies”) and a sulphidic cave (“cave mollies”), as well as in embryos of the sister taxon, Poecilia sulphuraria from a sulphidic surface spring (“sulphur mollies”). We asked at which points during development changes in the timing of the involved processes (i.e., heterochrony) would be detectible. Methods and Results: Data were extracted from digital photographs taken of representative embryos for each stage of development and each type of molly. Embryo mass decreased in convergent fashion, but we found patterns of embryonic fat content and ovum/embryo diameter to be divergent among all three types of mollies. The intensity of yellow colouration of the yolk (a proxy for carotenoid content) was significantly lower in cave mollies throughout development. Moreover, while relative head size decreased through development in surface mollies, it increased in both types of extremophile mollies, and eye growth was arrested in mid-stage embryos of cave mollies but not in surface or sulphur mollies. Conclusion: Our results clearly demonstrate that even among sister taxa convergence in phenotypic traits is not always achieved by the same processes during embryo development. Furthermore, teleost development is crucially dependent on sufficient carotenoid stores in the yolk, and so we discuss how the apparent ability of cave mollies to overcome this carotenoid-dependency may represent another potential mechanism explaining the lack of gene flow between surface and cave mollies

Are superficial neuromasts proprioceptors underlying fast copulatory behavior?

In male Poeciliid fishes, the modified anal fin (i.e., gonopodium) and its axial and appendicular support are repositioned within the axial skeleton, creating a novel sexually dimorphic ano-urogenital region. During copulation, the relative location of the gonopodium is crucial for successful insemination. Therefore, the repositioning of these structures and organ relied on the reorganization of the efferent circuitry that controls spinal motor neurons innervating appendicular muscles critical for the movement of the gonopodium, including the fast and synchronous torque-trust motion during insemination attempts. Copulation occurs when a male positions himself largely outside a female’s field of view, circumducts his gonopodium, and performs a rapid, complex maneuver to properly contact the female urogenital sinus with the distal tip of the gonopodium and transfers sperm. Although understanding of the efferent circuitry has significantly increased in the last 24 years, nothing is known about the cutaneous receptors involved in gonopodium movement, or how the afferent signals are processed to determine the location of this organ during copulation. Using Western mosquitofish, Gambusia affinis, as our model, we attempt to fill this gap in knowledge. Preliminary data showed cutaneous nerves and sensory neurons innervating superficial neuromasts surrounding the base of adult male gonopodium; those cutaneous nerves projected ventrally from the spinal cord through the 14th dorsal root ganglion and its corresponding ventral root towards the base and fin rays of the gonopodium. We asked what role the cutaneous superficial neuromasts play in controlling the positioning and timing of the gonopodium’s fast and synchronous movements for effective sperm transfer. First, we found a greater number of superficial neuromasts surrounding the base of the male’s gonopodium compared to the base of the female’s anal fin. Second, we systemically removed superficial neuromasts surrounding the gonopodium base and observed significant impairment of the positioning and timing of gonopodial movements. Our findings provide a first step to supporting the following hypothesis: during radical reorganization of the Poeciliid body plan, superficial neuromasts have been partially co-opted as proprioceptors that allow the gonopodium to control precise positioning and timing during copulatory attempts

Shared and unique features of predator-associated morphological divergence in three livebearing fishes

Divergent natural selection (fitness trade-offs) between environments often drives intraspecific diversification. When multiple species face a common environmental gradient their patterns of divergence might exhibit both shared and unique elements. We investigated shared and unique elements of diversification for three species of livebearing fishes (Poeciliidae) across a predator gradient (piscivorous fish vs. no piscivorous fish). All species (Gambuia affinis from the United States, G. hubbsi from the Bahamas and P. reticulata from Trinidad) exhibited a posterior shift in body allocation and more elongate bodies in predator populations. This morphological shift applied not only across species, but across age/gender classes, particular predator species and gross habitat types. Each species also had unique features of divergence, which may reflect peculiarities unique to their natal environments. We hypothesize much of the predator-associated morphology enhances fitness in the presence of predators but decreases fitness in the absence of predators. Preliminary evidence supports this hypothesis. We additionally found gonopodium size divergence in both Gambusia species that was opposite a trend previously found in P. reticulata. Partitioning phenotypic variation for multiple species into shared and unique responses across environmental gradients is a useful tool for elucidating general and localized mechanisms of diversification. Divergent natural selection (DNS) is a powerful mechanism that generates and maintains phenotypic diversity (Rice and Hostert 1993; Orr and Smith 1998; Schluter 2000b). DNS is created by functional trade-offs between alternative environments (Robinson and Wilson 1994; Robinson et al. 1996; Schluter 2000b). Depending on how environments vary (e.g. fine- or coarse-grained variation; sensu Levins 1968), DNS can lead to evolution of either canalized genetic differences between populations or phenotypic plasticity (West-Eberhard 1989; Robinson and Wilson 1994; Orr and Smith 1998; Schluter 2000b). DNS results in population differentiation through either of these mechanisms. That is, populations may differ from each other because of fixed genetic differences or because each is similarly plastic but their current environments differ. Environmental differences that typically produce population divergence include predation, competition, or abiotic stresses (Magurran and May 1999; Schluter 2000b). Consider the case where the sign of selection on focal traits differs across environments. Consider also that several species are evolving adaptive solutions in these environments. Some elements of evolutionary response will be similar across species. For example, species A and B may largely respond in a similar manner. Yet other aspects of response to DNS will be speciesspecific (A responds one way; B responds differently). In theory, after accounting for gross differences between species, the unique and shared elements of response to DNS can be identified. This approach allows one to integrate the study of phenotypic variation across selective environments, populations and species. Empirical studies of diversification in vertebrates has focused on resource competition and niche partitioning (Robinson and Wilson 1994; Van Valkenburgh and Wayne 1994; Smith and Skulason 1996; Schluter 2000a). However, predation is among the most important factors structuring natural populations (Sih et al. 1985; Kerfoot and Sih 1987; Jackson et al. 2001). Predators should not only change the distribution and abundance of species (via lethal and behavioral impacts on prey), but should also produce diversification—changes in the distribution and abundance of phenotypes within species (Endler 1995; DeWitt et al. 2000; Trussell 2000; Van Buskirk and Schmidt 2000). Although predation is often thought responsible for the evolution of inducible defenses among invertebrates (Harvell 1986; Havel 1987; Tollrian and Harvell 1999), studies investigating the importance of predation in vertebrate diversification are less common. Most studies of vertebrate evolutionary responses to predation center on life history changes (e.g. Skelly and Werner 1990; Rodd and Reznick 1997; Belk 1998; Johnson and Belk 2001; Reznick et al. 2001). Investigation of morphological divergence between alternative predator environments in vertebrates is less common (Brönmark and Miner 1992; Van Buskirk et al. 1997; Walker 1997; Lardner 2000; Relyea 2001). In this study, we examined body shape divergence in three species of livebearing fishes across alternative predator regimes. Furthermore we evaluate trends within and between species to identify both unique and shared aspects of diversification among prey species

Speciation through the lens of biomechanics: locomotion, prey capture and reproductive isolation

Speciation is a multifaceted process that involves numerous aspects of the biological sciences and occurs for multiple reasons. Ecology plays a major role, including both abiotic and biotic factors. Whether populations experience similar or divergent ecological environments, they often adapt to local conditions through divergence in biomechanical traits. We investigate the role of biomechanics in speciation using fish predator–prey interactions, a primary driver of fitness for both predators and prey. We highlight specific groups of fishes, or specific species, that have been particularly valuable for understanding these dynamic interactions and offer the best opportunities for future studies that link genetic architecture to biomechanics and reproductive isolation (RI). In addition to emphasizing the key biomechanical techniques that will be instrumental, we also propose that the movement towards linking biomechanics and speciation will include (i) establishing the genetic basis of biomechanical traits, (ii) testing whether similar and divergent selection lead to biomechanical divergence, and (iii) testing whether/how biomechanical traits affect RI. Future investigations that examine speciation through the lens of biomechanics will propel our understanding of this key process

Ecological correlates of risk and incidence of West Nile virus in the United States

West Nile virus, which was recently introduced to North America, is a mosquito-borne pathogen that infects a wide range of vertebrate hosts, including humans. Several species of birds appear to be the primary reservoir hosts, whereas other bird species, as well as other vertebrate species, can be infected but are less competent reservoirs. One hypothesis regarding the transmission dynamics of West Nile virus suggests that high bird diversity reduces West Nile virus transmission because mosquito blood-meals are distributed across a wide range of bird species, many of which have low reservoir competence. One mechanism by which this hypothesis can operate is that high-diversity bird communities might have lower community-competence, defined as the sum of the product of each species’ abundance and its reservoir competence index value. Additional hypotheses posit that West Nile virus transmission will be reduced when either: (1) abundance of mosquito vectors is low; or (2) human population density is low. We assessed these hypotheses at two spatial scales: a regional scale near Saint Louis, MO, and a national scale (continental USA). We found that prevalence of West Nile virus infection in mosquito vectors and in humans increased with decreasing bird diversity and with increasing reservoir competence of the bird community. Our results suggest that conservation of avian diversity might help ameliorate the current West Nile virus epidemic in the USA

Journal compilation C 2009 The Society for the Study of Evolution

We recently tested the hypothesis of ecological speciation in a post-Pleistocene radiation of Bahamas mosquitofish (Gambusia hubbsi) inhabiting inland blue holes (vertical, water-filled caves) on Andros Island, the Bahama

Data from: Origins of female genital diversity: predation risk and lock-and-key explain rapid divergence during an adaptive radiation

The study of male genital diversity has long overshadowed evolutionary inquiry of female genitalia, despite its non-trivial diversity. Here we identify four non-mutually exclusive mechanisms that could lead to genital divergence in females, and potentially generate patterns of correlated male-female genital evolution: (1) ecological variation alters the context of sexual selection (“ecology hypothesis”), (2) sexually antagonistic selection (“sexual-conflict hypothesis”), (3) female preferences for male genitalia mediated by female genital traits (“female-choice hypothesis”), and (4) selection against inter-population mating (“lock-and-key hypothesis”). We performed an empirical investigation of all four hypotheses using the model system of Bahamas mosquitofish inhabiting blue holes that vary in predation risk. We found unequivocal support for the ecology hypothesis, with females exhibiting a smaller genital opening in blue holes containing piscivorous fish. This is consistent with stronger postmating female choice/choice when predators are present, but greater premating female choice in their absence. Our results additionally supported the lock-and-key hypothesis, uncovering a pattern of reproductive character displacement for genital shape. We found no support for the sexual conflict or female choice hypotheses. Our results demonstrate a strong role for ecology in generating female genital diversity, and suggest that lock-and-key may provide a viable cause of female genital diversification

Individual-level wild-caught fish morphometric data

Morphometric data for the wild-caught fish MANOVA