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Female response to male sexual signals is context dependent and influenced by a variety of environmental factors. For instance, females often adjust mating preferences in response to predation risk. Social experiences as a juvenile, such as exposure to conspecific sexual signals, have also been shown to influence female mating preferences as adults. Experiments that examine the influence of both environmental factors and early social experiences on female preferences are needed to understand female mating behaviors in the wild. In Pacific field crickets (Teleogryllus oceanicus), males produce a calling song that females evaluate during mate choice. We examined the influence of both risk perception and juvenile exposure to calling song in shaping adult T. oceanicus female phonotaxis to either a high- or low-quality calling song. We predicted that females raised in song-less conditions would be more responsive to calling song to maximize mating opportunities, and that females would show reduced response to calling in a risky, open area. Females raised in a song-deprived environment were much more responsive to calling song compared to those reared with song. In contrast to our predictions, females raised in song-less conditions were more responsive to the high-quality song in the risky, open arena. These results suggest that juvenile acoustic rearing influences female responsiveness to male calling song, but it has less influence on strength of preference for signal quality.

Sexual signal evolution may present fitness consequences for the non-signaling sex due to shared genes and altered social conditions, but this is rarely studied in natural populations. On the Hawaiian Island of Kauai, most male Teleogryllus oceanicus (Pacific field crickets) lack the ability to sing because of a novel wing mutation (flatwing) that arose and spread in

Animals in captivity experience drastically different selective pressures than their wild counterparts. This can cause evolutionary divergence in behavior between captive and wild populations. While most research on evolution under captivity has focused on vertebrates, we expect similar behavioral changes in insects that live and breed in commercial facilities. Using the common house cricket, Acheta domesticus, we tested how crickets reared in captivity for many generations differed from wild-caught counterparts in two aspects of social behavior: male aggression and female responsiveness to male calling song. Acheta domesticus is an important model organism for behavioral research and are often reared in dense, commercial facilities with ad-libitum access to food and no risk of mortality from predators— very different conditions from the wild. We predicted that commercially-derived males would exhibit less intrasexual aggression due to selection from living in dense conditions. We predicted that commercially-derived females would be less responsive to male calling song because they are more likely to encounter many males at random. Instead, we found that commercially-derived males were more aggressive than wild ones, and that commercially-derived and wild females did not differ in responsiveness to calling song. Insects serve as model systems for a great deal of research in evolutionary and behavioral biology. If these animals are evolving in captivity, they may not provide an accurate representation of the natural phenomena we aim to understand.

Associations between heritable polymorphisms and life-history traits, such as development time or reproductive investment, may play an underappreciated role in maintaining polymorphic systems. This is because selection acting on a particular morph could be bolstered or disrupted by correlated changes in life history or vice versa. In a Hawaiian population of the Pacific field cricket (Teleogryllus oceanicus), a novel mutation (flatwing) on the X-chromosome is responsible for a heritable polymorphism in male wing structure. We used laboratory cricket colonies fixed for male wing morph to investigate whether males and females bearing the flatwing or normal-wing (wild-type) allele differed in their life-history traits. We found that flatwing males developed faster and had heavier testes than normal-wings, whereas flatwing homozygous females developed slower and had lighter reproductive tissues than normal-wing homozygous females. Our results advance our understanding of the evolution of polymorphisms by demonstrating that the genetic change responsible for a reproductive polymorphism can also have consequences for fundamental life-history traits in both males and females.

How populations adapt, or not, to rapid evolution of sexual signals has important implications for population viability, but is difficult to assess due to the paucity of examples of sexual signals evolving in real time. In Hawaiian populations of the Pacific field cricket (Teleogryllus oceanicus), selection from a deadly parasitoid fly has driven the rapid loss of a male acoustic signal, calling song, that females use to locate and evaluate potential mates. In this newly quiet environment where many males are obligately silent, how do phonotactic females find mates? Previous work has shown that the acoustic rearing environment (presence or absence of male calling song) during late juvenile stages and early adulthood exposes adaptive flexibility in locomotor behaviors of males, as well as mating behaviors in both sexes that helps facilitate the spread of silent (flatwing) males. Here, we tested whether females also show acoustically induced plasticity in walking behaviors using laboratory‐reared populations of T. oceanicus from Kauai (HI; >90% flatwings), Oahu (HI; ~50% flatwings), and Mangaia (Cook Islands; no flatwings or parasitoid fly). Though we predicted that females reared without song exposure would increase walking behaviors to facilitate mate localization when song is rare, we discovered that, unlike males, female T. oceanicus showed relatively little plasticity in exploratory behaviors in response to an acoustic rearing environment. Across all three populations, exposure to male calling song during development did not affect latency to begin walking, distance walked, or general activity of female crickets. However, females reared in the absence of song walked slower and showed a marginally non‐significant tendency to walk for longer durations of time in a novel environment than those reared in the presence of song. Overall, plasticity in female walking behaviors appears unlikely to have facilitated sexual signal loss in this species.

How sexual traits are gained and lost in the wild remains an important question in evolutionary biology. Pacific field crickets (Teleogryllus oceanicus) in Hawaii provide an unprecedented opportunity to investigate the factors facilitating evolutionary loss of a sexual signal in real time. Natural selection from an acoustically orienting parasitoid fly drove rapid evolution of a novel, silent male morph. While silent (flatwing) males enjoy protection from the fly, they face difficulty attracting mates. We tested how offspring production varies in association with three male attributes affected by the spread of flatwing: wing morph (flatwing or normal-wing), age (flatwings should survive longer than singers) and exposure to calling song during rearing (wild populations with many flatwings lack ambient calling song). Per mating event, flatwings sired more offspring than singers and older males were mounted more quickly by females when presented with standard courtship song. Despite prior work showing that male age and acoustic experience influence sperm characteristics associated with fertilization, age and song exposure had no influence on male offspring production per mating. This represents the first evidence that the silent male morph possesses a reproductive advantage that may help compensate for precopulatory barriers to mate attraction.

Pleiotropy between male signals and female preferences can facilitate evolution of sexual communication by maintaining coordination between the sexes. Alternatively, it can favor variation in the mating system, such as a reproductive polymorphism. It is unknown how common either of these scenarios is in nature. In Pacific field crickets (Teleogryllus oceanicus) on Kauai, Hawaii, a mutation (flatwing) that segregates as a single locus is responsible for the rapid loss of song production in males. We used outbred cricket colonies fixed for male wing morph to investigate whether homozygous flatwing and normal-wing (wild-type) females differ in responsiveness to male calling song and propensity to mate when paired with either a flatwing or normal-wing male in the presence or absence of courtship song. Flatwing females were less likely to mount a male than normal-wing females. Females of both genotypes showed a preference for normal-wing males and were more likely to mate in the presence of courtship song; normal-wing females were particularly likely to mate with song. Our results show that negative pleiotropy between obligate male silence and female mating behavior can constrain the evolution of sexual signal loss and contribute to the maintenance of a male reproductive polymorphism in the wild.

Evolutionary loss of traits is common over evolutionary time and occurs in diverse taxa. Sexual signals and other non-signal traits should differ in their likelihood of becoming lost because they experience different selection pressures contributing to their diminution or persistence. In particular, conspicuous sexual signals are often exploited by natural enemies; this significant cost can favor signal reduction or loss. Yet sexual signals should also experience strong selection favoring their persistence because they facilitate communication during sexual encounters and their loss would involve changes in both the signaler and receiver. Most examples of sexual signal loss come from phylogenetic studies, so it is difficult to ascertain the context and key factors responsible for their loss. Here, we describe one of the best documented examples of evolutionary sexual signal loss in real time due to signal exploitation: Teleogryllus oceanicus (the Pacific field cricket) in Hawaii where many males have lost the ability to sing due to natural selection from a deadly, acoustically-orienting parasitoid fly. Using sexual signal loss in T. oceanicus as a model, we identify environmental, social, and genetic factors that appear generally important in driving sexual signal loss due to signal exploitation. We also discuss each putative factor contributing to signal loss more broadly within the context of non-signal trait loss. Overall, the factors that facilitate evolutionary loss of signals and other traits exhibit significant parallels. In general, a significant cost from the environment, weak selection for persistence, and alternative ways of accomplishing the former function appear critical to achieving evolutionary loss of both sexual signals and non-signal traits. However, because few empirical examples of sexual signal loss over contemporary timescales exist, we need more theory and empirical work to better understand the evolutionary dynamics of sexual signal loss.

Many animals show complex behaviours that can have important ecological and evolutionary consequences. Environmental variation can lead to divergent selection that consistently favours particular behaviours in different environments; but how predictably multiple aspects of animal behaviour diverge in response to different environmental conditions remains unclear. We tested whether populations evolving under different levels of predation risk show predictable and repeatable population-level behavioural differences in all five primary components of animal personality: aggression, sociability, boldness, activity and exploration. We formulated and tested a priori predictions of divergence for each behaviour using the adaptive radiation of Bahamas mosquitofish, Gambusia hubbsi (family Poeciliidae), inhabiting vertical water-filled caves (blue holes) where they have evolved for thousands of years in either the presence or absence of predatory fish. Mosquitofish behaviours differed consistently, and largely predictably, between predation regimes: low-predation mosquitofish showed reduced sociability and greater exploration of a novel environment compared to high-predation counterparts. However, some differences were sex dependent: only females showed greater boldness and only males displayed reduced aggressiveness in low-predation populations. Activity levels did not differ between predation regimes. All populations showed a behavioural syndrome characteristic of either proactive or reactive stress-coping styles with regard to exploration. Exploration behavioural syndromes were more similar among populations that evolved in similar predation regimes, regardless of genetic relatedness. Using laboratory-born, high-predation mosquitofish, we confirmed that exploratory behaviours have a genetic basis and show significant within-individual repeatability. Our results suggest that environmental variation, such as chronic predation risk, can lead to repeatable, and often predictable, changes in multifarious animal behaviours, and that various aspects of behaviour can diversify more or less independently of one another. Considering the ecological importance of these behaviours, the ability to forecast behavioural shifts in a rapidly changing world could serve as a valuable conservation tool.

A longstanding hypothesis in evolutionary biology is that trade-offs between natural and sexual selection often underlie the diversification of sexual signals in the wild. A classic example of this "selection trade-off hypothesis" proposes that males evolve elaborate and conspicuous ornamentation in low-risk environments where female preferences dominate selection on sexual traits, but they evolve muted and relatively cryptic sexual traits in high-risk environments where selection from predators acts against conspicuous sexual traits and female preferences potentially weaken or reverse. However, little direct empirical evidence supports this notion. Using the model system of Bahamas mosquitofish (Gambusia hubbsi)—where males have recently evolved greater orange coloration in their dorsal fins in blue holes lacking predatory fish relative to populations with fish predators—we tested this hypothesis using fish replicas differing only in dorsal-fin color. Specifically, we employed plastic fish models in a combination of field and lab experiments to directly examine conspicuity to predators and female preferences for dorsal-fin color. We found that orange-shifted dorsal fins resembling the color exhibited in predator-free populations appeared more conspicuous to predatory bigmouth sleepers (Gobiomorus dormitor) that are evolutionarily naive to mosquitofish. Wild-caught female mosquitofish preferred the orange-shifted dorsal-fin model during dichotomous choice tests; evolutionary history with predators did not affect female preferences. Similar mate-choice trials with lab-born virgin females also found preferences for the orange-shifted dorsal-fin model and revealed significant genetic variation for female preferences. Our study provides direct empirical evidence documenting a trade-off between natural and sexual selection in a colorful sexual signal.

The aim of this study rests on three premises: (i) humans are altering ecosystems worldwide, (ii) environmental variation often influences the strength and nature of sexual selection, and (iii) sexual selection is largely responsible for rapid and divergent evolution of male genitalia. While each of these assertions has strong empirical support, no study has yet investigated their logical conclusion that human impacts on the environment might commonly drive rapid diversification of male genital morphology. We tested whether anthropogenic habitat fragmentation has resulted in rapid changes in the size, allometry, shape, and meristics of male genitalia in three native species of livebearing fishes (genus: Gambusia) inhabiting tidal creeks across six Bahamian islands. We found that genital shape and allometry consistently and repeatedly diverged in fragmented systems across all species and islands. Using a model selection framework, we identified three ecological consequences of fragmentation that apparently underlie observed morphological patterns: decreased predatory fish density, increased conspecific density, and reduced salinity. Our results demonstrate that human modifications to the environment can drive rapid and predictable divergence in male genitalia. Given the ubiquity of anthropogenic impacts on the environment, future research should evaluate the generality of our findings and potential consequences for reproductive isolation.

How sexual traits are gained and lost in the wild remains an important question in evolutionary biology. Pacific field crickets ( Teleogryllus oceanicus ) in Hawaii provide an unprecedented opportunity to investigate the factors facilitating evolutionary loss of a sexual signal in real time. Natural selection from an acoustically orienting parasitoid fly drove rapid evolution of a novel, silent male morph. While silent (flatwing) males enjoy protection from the fly, they face difficulty attracting mates. We tested how offspring production varies in association with three male attributes affected by the spread of flatwing: wing morph (flatwing or normal-wing), age (flatwings should survive longer than singers) and exposure to calling song during rearing (wild populations with many flatwings lack ambient calling song). Per mating event, flatwings sired more offspring than singers and older males were mounted more quickly by females when presented with standard courtship song. Despite prior work showing that male age and acoustic experience influence sperm characteristics associated with fertilization, age and song exposure had no influence on male offspring production per mating. This represents the first evidence that the silent male morph possesses a reproductive advantage that may help compensate for precopulatory barriers to mate attraction.

Male genital morphology is remarkably diverse across internally fertilizing animals, a phenomenon largely attributed to sexual selection. Ecological differences across environments can alter the context of sexual selection, yet little research has addressed how this may influence the rapid, divergent evolution of male genitalia. Using the model system of Bahamas mosquitofish (Gambusia hubbsi) undergoing ecological speciation across blue holes, we used geometric morphometric methods to test (i) whether male genital shape (the small, approximately 1 mm long, distal tip of the sperm-transfer organ, the gonopodium) has diverged between populations with and without predatory fish and (ii) whether any observed divergence has a genetic basis. We additionally examined the effects of genetic relatedness and employed model selection to investigate other environmental factors (i.e. interspecific competition, adult sex ratio and resource availability) that could potentially influence genital shape via changes in sexual selection. Predation regime comprised the most important factor associated with male genital divergence in this system, although sex ratio and some aspects of resource availability had suggestive effects. We found consistent, heritable differences in male genital morphology between predation regimes: Bahamas mosquitofish coexisting with predatory fish possessed more elongate genital tips with reduced soft tissue compared with counterparts inhabiting blue holes without predatory fish. We suggest this may reflect selection for greater efficiency of sperm transfer and fertilization during rapid and often forced copulations in high-predation populations or differences in sexual conflict between predation regimes. Our study highlights the potential importance of ecological variation, particularly predation risk, in indirectly generating genital diversity.