Predictability, an Orrery, and a Speciation Machine: Quest for a Standard Model of Speciation.

Accurate predictions are commonly taken as a hallmark of strong scientific understanding. Yet, we do not seem capable today of making many accurate predictions about biological speciation. Why? What limits predictability in general, what exactly is the function and value of predictions, and how might we go about predicting new species? Inspired by an orrery used to explain solar eclipses, we address these questions with a thought experiment in which we conceive an evolutionary speciation machine generating new species. This experiment highlights complexity, chance, and speciation pluralism as the three fundamental challenges for predicting speciation. It also illustrates the methodological value of predictions in testing and improving conceptual models. We then outline how we might move from the hypothetical speciation machine to a predictive standard model of speciation. Operationalizing, testing, and refining this model will require a concerted shift to large-scale, integrative, and interdisciplinary efforts across the tree of life. This endeavor, paired with technological advances, may reveal apparently stochastic processes to be deterministic, and promises to expand the breadth and depth of our understanding of speciation and more generally, of evolution.

Fluctuating selection maintains distinct species phenotypes in an ecological community in the wild.

Species' phenotypic characteristics often remain unchanged over long stretches of geological time. Stabilizing selection-in which fitness is highest for intermediate phenotypes and lowest for the extremes-has been widely invoked as responsible for this pattern. At the community level, such stabilizing selection acting individually on co-occurring species is expected to produce a rugged fitness landscape on which different species occupy distinct fitness peaks. However, even with an explosion of microevolutionary field studies over the past four decades, evidence for persistent stabilizing selection driving long-term stasis is lacking. Nonetheless, biologists continue to invoke stabilizing selection as a major factor explaining macroevolutionary patterns. Here, by directly measuring natural selection in the wild, we identified a complex community-wide fitness surface in which four Anolis lizard species each occupy a distinct fitness peak close to their mean phenotype. The presence of local fitness optima within species, and fitness valleys between species, presents a barrier to adaptive evolutionary change and acts to maintain species differences through time. However, instead of continuously operating stabilizing selection, we found that species were maintained on these peaks by the combination of many independent periods among which selection fluctuated in form, strength, direction, or existence and in which stabilizing selection rarely occurred. Our results suggest that lack of substantial phenotypic evolutionary change through time may be the result of selection, but not persistent stabilizing selection as classically envisioned.

Freshwater fishes maintain multi-trait phenotypic stability across an environmental gradient in aqueous calcium.

Reductions in a limiting nutrient might be expected to necessitate compromises in the functional traits that depend on that nutrient; yet populations existing in locations with low levels of such nutrients often do not show the expected degradation of functional traits. Indeed, logperch (Percina caprodes), pumpkinseed sunfish (Lepomis gibbosus) and yellow perch (Perca flavescens) residing in low-calcium water in the Upper St. Lawrence River were all previously found to maintain levels of scale calcium comparable to those of conspecific populations in high-calcium water. Yet it remains possible that the maintenance of one functional trait (i.e., scale calcium) under nutrient-limited (i.e., low calcium) conditions could come at the expense of maintaining other functional traits that depend on the same nutrient. The present study therefore examines other calcium-dependent traits, specifically skeletal element sizes and bone densities in the same fish species in the same area. Using radiographs of 101 fish from the three species across four locations (two in high-calcium water and two in low-calcium water), this new work documents multi-trait "homeostasis" along the gradient of water calcium. That is, no effect of calcium regime (low-calcium vs. high-calcium) was detected on any of the measured variables. Further, effect sizes for the skeletal traits were very low - lower even than effect sizes previously documented for scale calcium. These results thus show that native fishes maintain phenotypic stability across a suite of functional traits linked to calcium regulation, perhaps pointing to an "organismal-level homeostasis" scenario rather than a "trait-level homeostasis" scenario.

Sex matters: predator presence induces sexual dimorphism in a monomorphic prey, from stress genes to morphological defences.

Inducible defences allow prey to increase survival chances when predators are present while avoiding unnecessary costs in their absence. Many studies report considerable inter-individual variation in inducible defence expression, yet what underlies this variation is poorly understood. A classic vertebrate example of a predator-induced morphological defence is the increased body depth in crucian carp (Carassius carassius), which reduces the risk of predation from gape-size limited predators. Here, we report that among-individual variation in morphological defence expression can be linked to sex. We documented sexual dimorphism in lakes in which crucian carp coexisted with predators, where females showed shallower relative body depths than males, but not in a predator-free lake. When exposing crucian carp from a population without predators to perceived predation risk in a laboratory environment (presence/absence of pike, Esox lucius), we found that males expressed significantly greater morphological defence than females, causing sexual dimorphism only in the presence of predators. We uncovered a correlative link between the sex-specific inducible phenotypic response and gene expression patterns in major stress-related genes (POMC, MC3R, and MC4R). Together, our results highlight that sex-specific responses may be an important, yet underappreciated, component underlying inter-individual differences in the expression of inducible defences, even in species without pronounced sexual dimorphism.

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.

Resource competition explains rare cannibalism in the wild in livebearing fishes.

Cannibalism, the act of preying on and consuming a conspecific, is taxonomically widespread, and putatively important in the wild, particularly in teleost fishes. Nonetheless, most studies of cannibalism in fishes have been performed in the laboratory. Here, we test four predictions for the evolution of cannibalism by conducting one of the largest assessments of cannibalism in the wild to date coupled with a mesocosm experiment. Focusing on mosquitofishes and guppies, we examined 17 species (11,946 individuals) across 189 populations in the wild, spanning both native and invasive ranges and including disparate types of habitats. We found cannibalism to be quite rare in the wild: most populations and species showed no evidence of cannibalism, and the prevalence of cannibalism was typically less than 5% within populations when it occurred. Most victims were juveniles (94%; only half of these appeared to have been newborn offspring), with the remaining 6% of victims being adult males. Females exhibited more cannibalism than males, but this was only partially explained by their larger body size, suggesting greater energetic requirements of reproduction likely play a role as well. We found no evidence that dispersal-limited environments had a lower prevalence of cannibalism, but prevalence was greater in populations with higher conspecific densities, suggesting that more intense resource competition drives cannibalistic behavior. Supporting this conclusion, our mesocosm experiment revealed that cannibalism prevalence increased with higher conspecific density and lower resource levels but was not associated with juvenile density or strongly influenced by predation risk. We suggest that cannibalism in livebearing fishes is rare in the wild because preying on conspecifics is energetically costly and only becomes worth the effort when competition for other food is intense. Due to the artificially reduced cost of capturing conspecifics within confined spaces, cannibalism in captive settings can be much more frequent.

Antipredator phenotype in crucian carp altered by a psychoactive drug.

Predator-inducible defenses constitute a widespread form of adaptive phenotypic plasticity, and such defenses have recently been suggested linked with the neuroendocrine system. The neuroendocrine system is a target of endocrine disruptors, such as psychoactive pharmaceuticals, which are common aquatic contaminants. We hypothesized that exposure to an antidepressant pollutant, fluoxetine, influences the physiological stress response in our model species, crucian carp, affecting its behavioral and morphological responses to predation threat. We examined short- and long-term effects of fluoxetine and predator exposure on behavior and morphology in crucian carp. Seventeen days of exposure to a high dose of fluoxetine (100 µg/L) resulted in a shyer phenotype, regardless of the presence/absence of a pike predator, but this effect disappeared after long-term exposure. Fluoxetine effects on morphological plasticity were context-dependent as a low dose (1 µg/L) only influenced crucian carp body shape in pike presence. A high dose of fluoxetine strongly influenced body shape regardless of predator treatment. Our results highlight that environmental pollution by pharmaceuticals could disrupt physiological regulation of ecologically important inducible defenses.

Natural and anthropogenic sources of habitat variation influence exploration behaviour, stress response, and brain morphology in a coastal fish.

Evolutionary ecology aims to better understand how ecologically important traits respond to environmental heterogeneity. Environments vary both naturally and as a result of human activities, and investigations that simultaneously consider how natural and human-induced environmental variation affect diverse trait types grow increasingly important as human activities drive species endangerment. Here, we examined how habitat fragmentation and structural habitat complexity affect disparate trait types in Bahamas mosquitofish Gambusia hubbsi inhabiting tidal creeks. We tested a priori predictions for how these factors might influence exploratory behaviour, stress reactivity and brain anatomy. We examined approximately 350 adult Bahamas mosquitofish from seven tidal-creek populations across Andros Island, The Bahamas that varied in both human-caused fragmentation (three fragmented and four unfragmented) and natural habitat complexity (e.g. fivefold variation in rock habitat). Populations that had experienced severe human-induced fragmentation, and thus restriction of tidal exchange from the ocean, exhibited greater exploration of a novel environment, stronger physiological stress responses to a mildly stressful event and smaller telencephala (relative to body size). These changes matched adaptive predictions based mostly on (a) reduced chronic predation risk and (b) decreased demands for navigating tidally dynamic habitats. Populations from sites with greater structural habitat complexity showed a higher propensity for exploration and a relatively larger optic tectum and cerebellum. These patterns matched adaptive predictions related to increased demands for navigating complex environments. Our findings demonstrate environmental variation, including recent anthropogenic impacts (<50 years), can significantly affect complex, ecologically important traits. Yet trait-specific patterns may not be easily predicted, as we found strong support for only six of 12 predictions. Our results further highlight the utility of simultaneously quantifying multiple environmental factors-for example had we failed to account for habitat complexity, we would not have detected the effects of fragmentation on exploratory behaviours. These responses, and their ecological consequences, may be complex: rapid and adaptive phenotypic responses to anthropogenic impacts can facilitate persistence in human-altered environments, but may come at a cost of population vulnerability if ecological restoration was to occur without consideration of the altered traits.

Low-latitude zooplankton pigmentation plasticity in response to multiple threats.

Crustacean copepods in high-latitude lakes frequently alter their pigmentation facultatively to defend themselves against prevailing threats, such as solar ultraviolet radiation (UVR) and visually oriented predators. Strong seasonality in those environments promotes phenotypic plasticity. To date, no one has investigated whether low-latitude copepods, experiencing continuous stress from UVR and predation threats, exhibit similar inducible defences. We here investigated the pigmentation levels of Bahamian 'blue hole' copepods, addressing this deficit. Examining several populations varying in predation risk, we found the lowest levels of pigmentation in the population experiencing the highest predation pressure. In a laboratory experiment, we found that, in contrast with our predictions, copepods from these relatively constant environments did show some changes in pigmentation subsequent to the removal of UVR; however, exposure to water from different predation regimes induced minor and idiosyncratic pigmentation change. Our findings suggest that low-latitude zooplankton in inland environments may exhibit reduced, but non-zero, levels of phenotypic plasticity compared with their high-latitude counterparts.

Urbanization drives contemporary evolution in stream fish.

Human activities reduce biodiversity but may also drive diversification by modifying selection. Urbanization alters stream hydrology by increasing peak water velocities, which should in turn alter selection on the body morphology of aquatic species. Here, we show how urbanization can generate evolutionary divergence in the body morphology of two species of stream fish, western blacknose dace (Rhinichthys obtusus) and creek chub (Semotilus atromaculatus). We predicted that fish should evolve more streamlined body shapes within urbanized streams. We found that in urban streams, dace consistently exhibited more streamlined bodies while chub consistently showed deeper bodies. Comparing modern creek chub populations with historical museum collections spanning 50 years, we found that creek chub (1) rapidly became deeper bodied in streams that experienced increasing urbanization over time, (2) had already achieved deepened bodies 50 years ago in streams that were then already urban (and showed no additional deepening over time), and (3) remained relatively shallow bodied in streams that stayed rural over time. By raising creek chub from five populations under common conditions in the laboratory, we found that morphological differences largely reflected genetically based differences, not velocity-induced phenotypic plasticity. We suggest that urbanization can drive rapid, adaptive evolutionary responses to disturbance, and that these responses may vary unpredictably in different species.

Causes and Consequences of Genital Evolution.

The study of genital diversity has experienced rapidly burgeoning attention over the past few decades. This research has shown that male genitalia in internally fertilizing animals exhibit remarkably rapid and complex evolution. In recent years, a consensus has emerged that sexual selection is responsible for much of the observed genital diversity, with natural selection largely playing a subsidiary role. Despite enhanced understanding of the key proximate forms of selection responsible for genital evolution, we still have a poor grasp of the broader, ultimate causes and consequences of the striking diversity of genitalia. Here, we highlight three topics that have so far received comparatively little attention and yet could prove critically important. First, we encourage investigation of ecology's direct and indirect roles in genital diversification, as ecological variation can influence selection on genitalia in several ways, perhaps especially by influencing the context of sexual selection. Second, we need more research into the effects of genital divergence on speciation, as genital differences could enhance reproductive isolation through either a lock-and-key process (where selection directly favors reproductive isolation) or as an incidental by-product of divergence. Third, we echo recent calls for increased research on female genitalia, as non-trivial female genital diversity exists, and multiple mechanisms can lead to rapid diversification of female genitalia. For all three topics, we review theory and empirical data, and describe specific research approaches for tackling these questions. We hope this work provides a roadmap toward increased understanding of the causes and consequences of the conspicuous diversity of primary sexual traits, and thus toward new insights into the evolution of complex traits and the phenotypic causes of speciation.

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.

Extremophile Poeciliidae: multivariate insights into the complexity of speciation along replicated ecological gradients.

BACKGROUND: Replicate population pairs that diverge in response to similar selective regimes allow for an investigation of (a) whether phenotypic traits diverge in a similar and predictable fashion, (b) whether there is gradual variation in phenotypic divergence reflecting variation in the strength of natural selection among populations, (c) whether the extent of this divergence is correlated between multiple character suites (i.e., concerted evolution), and (d) whether gradual variation in phenotypic divergence predicts the degree of reproductive isolation, pointing towards a role for adaptation as a driver of (ecological) speciation. Here, we use poeciliid fishes of the genera Gambusia and Poecilia that have repeatedly evolved extremophile lineages able to tolerate high and sustained levels of toxic hydrogen sulfide (H2S) to answer these questions. RESULTS: We investigated evolutionary divergence in response to H2S in Gambusia spp. (and to a lesser extent Poecilia spp.) using a multivariate approach considering the interplay of life history, body shape, and population genetics (nuclear miscrosatellites to infer population genetic differentiation as a proxy for reproductive isolation). We uncovered both shared and unique patterns of evolution: most extremophile Gambusia predictably evolved larger heads and offspring size, matching a priori predictions for adaptation to sulfidic waters, while variation in adult life histories was idiosyncratic. When investigating patterns for both genera (Gambusia and Poecilia), we found that divergence in offspring-related life histories and body shape were positively correlated across populations, but evidence for individual-level associations between the two character suites was limited, suggesting that genetic linkage, developmental interdependencies, or pleiotropic effects do not explain patterns of concerted evolution. We further found that phenotypic divergence was positively correlated with both environmental H2S-concentration and neutral genetic differentiation (a proxy for gene flow). CONCLUSIONS: Our results suggest that higher toxicity exerts stronger selection, and that divergent selection appears to constrain gene flow, supporting a scenario of ecological speciation. Nonetheless, progress toward ecological speciation was variable, partially reflecting variation in the strength of divergent selection, highlighting the complexity of selective regimes even in natural systems that are seemingly governed by a single, strong selective agent.

Correlated evolution of personality, morphology and performance.

Evolutionary change in one trait can elicit evolutionary changes in other traits due to genetic correlations. This constrains the independent evolution of traits and can lead to unpredicted ecological and evolutionary outcomes. Animals might frequently exhibit genetic associations among behavioural and morphological-physiological traits, because the physiological mechanisms behind animal personality can have broad multitrait effects and because many selective agents influence the evolution of multiple types of traits. However, we currently know little about genetic correlations between animal personalities and nonbehavioural traits. We tested for associations between personality, morphology and locomotor performance by comparing zebrafish (Danio rerio) collected from the wild and then selectively bred for either a proactive or reactive stress coping style ('bold' or 'shy' phenotypes). Based on adaptive hypotheses of correlational selection in the wild, we predicted that artificial selection for boldness would produce correlated evolutionary responses of larger caudal regions and higher fast-start escape performance (and the opposite for shyness). After four to seven generations, morphology and locomotor performance differed between personality lines: bold zebrafish exhibited a larger caudal region and higher fast-start performance than fish in the shy line, matching predictions. Individual-level phenotypic correlations suggested that pleiotropy or physical gene linkage likely explained the correlated response of locomotor performance, while the correlated response of body shape may have reflected linkage disequilibrium, which is breaking down each generation in the laboratory. Our results indicate that evolution of personality can result in concomitant changes in morphology and whole-organism performance, and vice versa.

Anthropogenic ecosystem fragmentation drives shared and unique patterns of sexual signal divergence among three species of Bahamian mosquitofish.

When confronted with similar environmental challenges, different organisms can exhibit dissimilar phenotypic responses. Therefore, understanding patterns of phenotypic divergence for closely related species requires considering distinct evolutionary histories. Here, we investigated how a common form of human-induced environmental alteration, habitat fragmentation, may drive phenotypic divergence among three closely related species of Bahamian mosquitofish (Gambusia spp.). Focusing on one phenotypic trait (male coloration), having a priori predictions of divergence, we tested whether populations persisting in fragmented habitats differed from those inhabiting unfragmented habitats and examined the consistency of the pattern across species. Species exhibited both shared and unique patterns of phenotypic divergence between the two types of habitats, with shared patterns representing the stronger effect. For all species, populations in fragmented habitats had fewer dorsal-fin spots. In contrast, the magnitude and trajectory of divergence in dorsal-fin color, a sexually selected trait, differed among species. We identified fragmentation-mediated increased turbidity as a possible driver of these trait shifts. These results suggest that even closely related species can exhibit diverse phenotypic responses when encountering similar human-mediated selection regimes. This element of unpredictability complicates forecasting the phenotypic responses of wild organisms faced with anthropogenic change - an important component of biological conservation and ecosystem management.

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 nontrivial diversity. Here, we identify four nonmutually 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/conflict 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.

Ecological opportunity and the adaptive diversification of lineages.

The tenet that ecological opportunity drives adaptive diversification has been central to theories of speciation since Darwin, yet no widely accepted definition or mechanistic framework for the concept currently exists. We propose a definition for ecological opportunity that provides an explicit mechanism for its action. In our formulation, ecological opportunity refers to environmental conditions that both permit the persistence of a lineage within a community, as well as generate divergent natural selection within that lineage. Thus, ecological opportunity arises from two fundamental elements: (1) niche availability, the ability of a population with a phenotype previously absent from a community to persist within that community and (2) niche discordance, the diversifying selection generated by the adaptive mismatch between a population's niche-related traits and the newly encountered ecological conditions. Evolutionary response to ecological opportunity is primarily governed by (1) spatiotemporal structure of ecological opportunity, which influences dynamics of selection and development of reproductive isolation and (2) diversification potential, the biological properties of a lineage that determine its capacity to diversify. Diversification under ecological opportunity proceeds as an increase in niche breadth, development of intraspecific ecotypes, speciation, and additional cycles of diversification that may themselves be triggered by speciation. Extensive ecological opportunity may exist in depauperate communities, but it is unclear whether ecological opportunity abates in species-rich communities. Because ecological opportunity should generally increase during times of rapid and multifarious environmental change, human activities may currently be generating elevated ecological opportunity - but so far little work has directly addressed this topic. Our framework highlights the need for greater synthesis of community ecology and evolutionary biology, unifying the four major components of the concept of ecological opportunity.

Ecosystem fragmentation drives increased diet variation in an endemic livebearing fish of the Bahamas.

One consequence of human-driven habitat degradation in general, and habitat fragmentation in particular, is loss of biodiversity. An often-underappreciated aspect of habitat fragmentation relates to changes in the ecology of species that persist in altered habitats. In Bahamian wetlands, ecosystem fragmentation causes disruption of hydrological connectivity between inland fragmented wetlands and adjacent marine areas, with the consequent loss of marine piscivores from fragmented sections. We took advantage of this environmental gradient to investigate effects of ecosystem fragmentation on patterns of resource use in the livebearing fish Gambusia hubbsi (Family Poeciliidae), using both population- and individual-level perspectives. We show that fragmentation-induced release from predation led to increased G. hubbsi population densities, which consequently led to lower mean growth rates, likely as a result of higher intraspecific competition for food. This was accompanied by a broadening of dietary niches via increased interindividual diet variation, suggesting a negative effect of predation and a positive effect of intraspecific competition on the degree of diet variation in natural populations. Our results therefore indicate that habitat fragmentation can greatly impact the ecology of resilient populations, with potentially important ecological and evolutionary implications.

The oestrogen pathway underlies the evolution of exaggerated male cranial shapes in Anolis lizards.

Sexual dimorphisms vary widely among species. This variation must arise through sex-specific evolutionary modifications to developmental processes. Anolis lizards vary extensively in their expression of cranial dimorphism. Compared with other Anolis species, members of the carolinensis clade have evolved relatively high levels of cranial dimorphism; males of this clade have exceptionally long faces relative to conspecific females. Developmentally, this facial length dimorphism arises through an evolutionarily novel, clade-specific strategy. Our analyses herein reveal that sex-specific regulation of the oestrogen pathway underlies evolution of this exaggerated male phenotype, rather than the androgen or insulin growth factor pathways that have long been considered the primary regulators of male-biased dimorphism among vertebrates. Our results suggest greater intricacy in the genetic mechanisms that underlie sexual dimorphisms than previously appreciated.

Evolution of male coloration during a post-Pleistocene radiation of Bahamas mosquitofish (Gambusia hubbsi).

Sexual signal evolution can be complex because multiple factors influence the production, transmission, and reception of sexual signals, as well as receivers' responses to them. To grasp the relative importance of these factors in generating signal diversity, we must simultaneously investigate multiple selective agents and signaling traits within a natural system. We use the model system of the radiation of Bahamas mosquitofish (Gambusia hubbsi) inhabiting blue holes to test the effects of resource availability, male body size and other life-history traits, key aspects of the transmission environment, sex ratio, and predation risk on variation in multiple male color traits. Consistent with previous work examining other traits in this system, several color traits have repeatedly diverged between predation regimes, exhibiting greater elaboration in the absence of predators. However, other factors proved influential as well, with variation in resource levels, body size, relative testes size, and background water color being especially important for several color traits. For one prominent signaling trait, orange dorsal fins, we further confirmed a genetic basis underlying population differences using a laboratory common-garden experiment. We illustrate a promising approach for gaining a detailed understanding of the many contributing factors in the evolution of multivariate sexual signals.