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Among the parasites of insects, endoparasitoids impose a costly challenge to host defenses because they use their host’s body for the development and maturation of their eggs or larvae, and ultimately kill the host. Tachinid flies are highly specialized acoustically orienting parasitoids, with first instar mobile larvae that burrow into the host’s body to feed. We investigated the possibility that Teleogryllus oceanicus field crickets employ postinfestation strategies to maximize survival when infested with the larvae of the parasitoid fly Ormia ochracea. Using crickets from the Hawaiian Islands of Kauai, where the parasitoid is present, and crickets from the Cook Islands (Mangaia), where the parasitoid is absent, we evaluated fitness consequences of infestation by comparing feeding behavior, reproductive capacity, and survival of males experimentally infested with O. ochracea larvae. We also evaluated mechanisms underlying host responses by comparing gene expression in crickets infested with fly larvae for different lengths of time with that of uninfested control crickets. We observed weak population differences in fitness (spermatophore production) and survival (total survival time postinfestation). These responses generally did not show an interaction between population and the number of larva hosts carried or by host body condition. Gene expression patterns also revealed population differences in response to infestation, but we did not find evidence for consistent differences in genes associated with immunity or stress response. One possibility is that any postinfestation evolved resistance does not involve genes associated with these particular functional categories. More likely, these results suggest that coevolution with the fly does not strongly select for either postinfestation resistance or tolerance of parasitoid larvae in male crickets., Experimental infestation of field crickets with Ormia ochracea larvae strongly impacted gene expression profiles of their hosts, and these varied over the time course of infestation. Coevolving crickets from Kauai showed a larger magnitude and extent of differential gene expression in response to infestation than did crickets from a non‐coevolving population (Mangaia). Host immune and stress response genes, however, responded similarly to infestation with O. ochracea larvae, regardless of population coevolutionary history. We found little evidence for population‐level differences in immunity, tolerance, or fitness measures in response to infestation, suggesting that evolved pre‐infestation avoidance measures are under stronger selection in the Kauai population.

Behavioural traits are often noted to persist after relaxation or removal of associated selection pressure, whereas it has been observed that morphological traits under similar conditions appear to decay more rapidly. Despite this, persistent non-adaptive, 'vestigial' behavioural variation has received little research scrutiny. Here we review published examples of vestigial behavioural traits, highlighting their surprising prevalence, and argue that their further study can reveal insights about the widely debated role of behaviour in evolution. Some vestigial behaviours incur fitness costs, so may act as a drag on adaptive evolution when that adaptation occurs via trait loss or reversal. In other cases, vestigial behaviours can contribute to future evolutionary trajectories, for example by preserving genetic and phenotypic variation which is later co-opted by selection during adaptive evolution or diversification, or through re-emergence after ancestral selection pressures are restored. We explore why vestigial behaviours appear prone to persistence. Behavioural lag may be a general phenomenon arising from relatively high levels of non-genetic variation in behavioural expression, and pleiotropic constraint. Long-term persistence of non-adaptive behavioural traits could also result when their expression is associated with morphological features which might be more rapidly lost or reduced. We propose that vestigial behaviours could provide a substrate for co-option by novel selective forces, and advocate further study of the fate of behavioural traits following relaxed and reversed selection. Vestigial behaviours have been relatively well studied in the context of antipredator behaviours, but they are far from restricted to this ecological context, and so deserve broader consideration. They also have practical importance, with mixed evidence, for example, as to whether predator/parasite-avoidance behaviours are rapidly lost in wildlife refuges and captivity. We identify important areas for future research to help determine whether vestigial behaviours essentially represent a form of evolutionary lag, or whether they have more meaningful evolutionary consequences distinct from those of other vestigial and behavioural traits.

Funding: This study was supported by JSPS Research Fellowships for Young Scientists CPD Grant 20J00660 (to N.M.), Grant-in-Aid for Early-Career Scientists 21K15168 (to N.M.), and Okanawa Institute of Science and Technology core funding. N.W.B. gratefully acknowledges funding from the UK Natural Environment Research Council (NE/T000619/1). Recent attempts to explain the evolutionary prevalence of same-sex sexual behavior (SSB) have focused on the role of indiscriminate mating. However, in many cases, SSB may be more complex than simple mistaken identity, instead involving mutual interactions and successful pairing between partners who can detect each other’s sex. Behavioral plasticity is essential for the expression of SSB in such circumstances. To test behavioral plasticity’s role in the evolution of SSB, we used termites to study how females and males modify their behavior in same-sex versus heterosexual pairs. Male termites follow females in paired “tandems” before mating, and movement patterns are sexually dimorphic. Previous studies observed that adaptive same-sex tandems also occur in both sexes. Here we found that stable same-sex tandems are achieved by behavioral plasticity when one partner adopts the other sex’s movements, resulting in behavioral dimorphism. Simulations based on empirically obtained parameters indicated that this socially cued plasticity contributes to pair maintenance, because dimorphic movements improve reunion success upon accidental separation. A systematic literature survey and phylogenetic comparative analysis suggest that the ancestors of modern termites lack consistent sex roles during pairing, indicating that plasticity is inherited from the ancestor. Socioenvironmental induction of ancestral behavioral potential may be of widespread importance to the expression of SSB. Our findings challenge recent arguments for a prominent role of indiscriminate mating behavior in the evolutionary origin and maintenance of SSB across diverse taxa. Publisher PDF

The role of within-generation phenotypic plasticity (WGP) versus transgenerational plasticity (TGP) during evolutionary adaptation are not well understood, particularly for socially-cued TGP.We tested how genetics, WGP, and TGP jointly influence expression of fitness traits facilitating adaptive evolution in the field cricket Teleogryllus oceanicus. A male-silencing mutation (“flatwing”) spread to fixation in ca. 50 generations in a Hawaiian cricket population attacked by acoustically-orienting parasitoids. This rapid loss of song caused the social environment to dramatically change.Juveniles carrying the flatwing (fw) genotype exhibited greater locomotive activity than those carrying the normal-wing (nw) allele, consistent with genetic coupling of increased locomotion with fw.Consistent with adaptive WGP, homozygous fw females developing in the absence of song showed reduced body condition and reproductive investment at adulthood.Adult but not juvenile offspring exhibited TGP in response to maternal social environment for structural size, somatic condition, and reproductive investment, whereas adult locomotion and flight was only influenced by WGP. WGP and TGP interacted to shape multiple traits at adulthood, though effect sizes were modest.Interactions between genetic effects and social plasticity within and across generations are likely to have influenced the evolutionary spread of flatwing crickets. However, interactions among these effects can be complex, and it is notable that TGP manifested most strongly later in development. Our findings stress the importance of evaluating trait plasticity at different developmental stages and across generations when studying phenotypic plasticity’s role in evolution.

Our quest to bring a child into our family led us to confront academic working practices, say Tony Ly and Nathan W. Bailey. Our quest to bring a child into our family led us to confront academic working practices, say Tony Ly and Nathan W. Bailey.

Funding: Natural Environmental ResearchCouncil for funding (NE/L011255/1) (N.W.B.). Evolutionary loss of sexual signals is widespread. Examining the consequences for behaviours associated with such signals can provide insight into factors promoting or inhibiting trait loss. We tested whether a behavioural component of a sexual trait, male calling effort, has been evolutionary reduced in silent populations of Hawaiian field crickets (Teleogryllus oceanicus). Cricket song requires energetically costly wing movements, but ‘flatwing’ males have feminized wings that preclude song and protect against a lethal, eavesdropping parasitoid. Flatwing males express wing movement patterns associated with singing but, in contrast with normal-wing males, sustained periods of wing movement cannot confer sexual selection benefits and should be subject to strong negative selection. We developed an automated technique to quantify how long males spend expressing wing movements associated with song. We compared calling effort among populations of Hawaiian crickets with differing proportions of silent males and between male morphs. Contrary to expectation, silent populations invested as much in calling effort as non-silent populations. Additionally, flatwing and normal-wing males from the same population did not differ in calling effort. The lack of evolved behavioural adjustment following morphological change in silent Hawaiian crickets illustrates how behaviour might sometimes impede, rather than facilitate, evolution. Postprint

Funding: Orthopterists' Society, Natural Environment Research Council (Grant Number(s): NE/G00949X/1, NE/G014906/1, NE/L011255/1), ARC (Grant Number(s): DP180101708). A major challenge for studying the role of sexual selection in divergence and speciation is understanding the relative influence of different sexually selected signals on those processes in both intra‐ and interspecific contexts. Different signals may be more or less susceptible to co‐option for species identification depending on the balance of sexual and ecological selection acting upon them. To examine this, we tested three predictions to explain geographic variation in long‐ versus short‐range sexual signals across a 3,500 + km transect of two related Australian field cricket species (Teleogryllus spp.): (a) selection for species recognition, (b) environmental adaptation and (c) stochastic divergence. We measured male calling song and male and female cuticular hydrocarbons (CHCs) in offspring derived from wild populations, reared under common garden conditions. Song clearly differentiated the species, and no hybrids were observed suggesting that hybridization is rare or absent. Spatial variation in song was not predicted by geography, genetics or climatic factors in either species. In contrast, CHC divergence was strongly associated with an environmental gradient supporting the idea that the climatic environment selects more directly upon these chemical signals. In light of recently advocated models of diversification via ecological selection on secondary sexual traits, the different environmental associations we found for song and CHCs suggest that the impact of ecological selection on population divergence, and how that influences speciation, might be different for acoustic versus chemical signals. Publisher PDF

Significance The evolution of sibling rivalry is a classic problem in behavioral ecology. Our approach of observing the experimental evolution of sibling interactions in real time reveals three key insights. First, when parents provide parental care, siblings evolve to compete. Parental care compensates for the costs of sibling rivalry. Second, when parents do not supply care, siblings evolve to cooperate. Sibling cooperation compensates for the loss of parental care. Third, rapid evolutionary switching between sibling rivalry and sibling cooperation is possible because siblings induce greater levels of rivalry (or cooperation) in each other. This generates positive evolutionary feedback, rapidly locking larvae into evolving greater levels of competition (or cooperation) in the presence (or absence) of parental care., Sibling rivalry is commonplace within animal families, yet offspring can also work together to promote each other’s fitness. Here we show that the extent of parental care can determine whether siblings evolve to compete or to cooperate. Our experiments focus on the burying beetle Nicrophorus vespilloides, which naturally provides variable levels of care to its larvae. We evolved replicate populations of burying beetles under two different regimes of parental care: Some populations were allowed to supply posthatching care to their young (Full Care), while others were not (No Care). After 22 generations of experimental evolution, we found that No Care larvae had evolved to be more cooperative, whereas Full Care larvae were more competitive. Greater levels of cooperation among larvae compensated for the fitness costs caused by parental absence, whereas parental care fully compensated for the fitness costs of sibling rivalry. We dissected the evolutionary mechanisms underlying these responses by measuring indirect genetic effects (IGEs) that occur when different sibling social environments induce the expression of more cooperative (or more competitive) behavior in focal larvae. We found that indirect genetic effects create a tipping point in the evolution of larval social behavior. Once the majority of offspring in a brood start to express cooperative (or competitive) behavior, they induce greater levels of cooperation (or competition) in their siblings. The resulting positive feedback loops rapidly lock larvae into evolving greater levels of cooperation in the absence of parental care and greater levels of rivalry when parents provide care.

Funding support was provided by NERC grants to N.W.B. (NE/G014906/1, NE/L011255/1), NERC (NE/G00949X/1) and ARC grants to J.H (DP180101708), and an Orthopterists’ Society grant to P.A.M. Speciation research dissects the genetics and evolution of reproductive barriers between parental species. Hybrids are the ‘gatekeepers’ of gene flow, so it is also important to understand the behavioural mechanisms and genetics of any potential isolation from their parental species. We tested the role of multiple behavioural barriers in reproductive isolation among closely related field crickets and their hybrids (Teleogryllus oceanicus and T. commodus). These species hybridize in the laboratory, but the behaviour of hybrids is unusual and there is little evidence for gene flow in the wild. We found that heterospecific pairs exhibited reduced rates of courtship behaviour due to discrimination by both sexes, and that this behavioural isolation was symmetrical. However, hybrids were not sexually selected against and exhibited high rates of courtship behaviour even though hybrid females are sterile. Using reciprocal hybrid crosses, we characterized patterns of interspecific divergence and inheritance in key sexual traits that might underlie the mating patterns we found: calling song, courtship song and cuticular hydrocarbons (CHCs). Song traits exhibited both sex linkage and transgressive segregation, whereas CHCs exhibited only the latter. Calculations of the strength of isolation exerted by these sexual traits suggest that close‐range signals are as important as long‐distance signals in contributing to interspecific sexual isolation. The surprisingly weak mating barriers observed between hybrids and parental species highlight the need to examine reproductive isolating mechanisms and their genetic bases across different potential stages of introgressive hybridization. Postprint

Social isolation has profound impacts. Most animal research focuses on negative phenotypic consequences of social isolation within individual lifetimes. Less is known about how it affects genetics, selection, and evolution over longer timescales, though ample indirect evidence suggests that it might. We advocate that evolutionary consequences of social isolation be tested more directly. We suggest that the 'index of social isolation', the mismatch between actual and optimal social interaction experienced by individuals within a population, may play a key role in releasing cryptic genetic variation, adaptation rates, diversification patterns, and ecosystem-level processes. Evolutionary dynamics arising from social isolation could have significant impacts in applied settings such as conservation, animal breeding, control of biological invasions, and evolutionary resilience to anthropogenic change.

Funding: Natural Environment Research Council grants to N.W.B., Grant/Award numbers: NE/G014906/1, NE/L011255/1; Orthopterists’ Society grant to P.A.M. Linking intraspecific and interspecific divergence is an important challenge in speciation research. X chromosomes are expected to evolve faster than autosomes and disproportionately contribute to reproductive barriers, and comparing genetic variation on X and autosomal markers within and between species can elucidate evolutionary processes that shape genome variation. We performed RADseq on a 16‐population transect of two closely‐related Australian cricket species, Teleogryllus commodus and T. oceanicus, covering allopatry and sympatry. This classic study system for sexual selection provides a rare exception to Haldane's rule, as hybrid females are sterile. We found no evidence of recent introgression, despite the fact that the species co‐exist in overlapping habitats in the wild and interbreed in the laboratory. Putative X‐linked loci showed greater differentiation between species compared to autosomal loci. However, population differentiation within species was unexpectedly lower on X‐linked markers than autosomal markers, and relative X‐to‐autosomal genetic diversity was inflated above neutral expectations. Populations of both species showed genomic signatures of recent population expansions, but these were not strong enough to account for the inflated X/A diversity. Instead, most of the excess polymorphism on the X could better be explained by sex‐biased processes that increase the relative effective population size of the X, such as interspecific variation in the strength of sexual selection among males. Taken together, the opposing patterns of diversity and differentiation at X versus autosomal loci implicate a greater role for sex‐linked genes in maintaining species boundaries in this system. Postprint

Behaviour is highly flexible, but does this make it special compared to other types of traits? We review how considering indirect genetic effects—the influence of genes expressed by social partners—can inform behavioural ecology research by improving predictions of behavioural optima in different social, evolutionary and ecological contexts. We argue that this framework is ideal for empirically testing behaviour’s proposed, yet heavily debated, unique role in shaping evolutionary patterns and processes.

Sexual selection can target many different types of traits. However, the relative influence of different sexually selected traits during evolutionary divergence is poorly understood. We used the field cricket Teleogryllus oceanicus to quantify and compare how five traits from each of three sexual signal modalities and components diverge among allopatric populations: male advertisement song, cuticular hydrocarbon (CHC) profiles and forewing morphology. Population divergence was unexpectedly consistent: we estimated the among-population (genetic) variance-covariance matrix, D, for all 15 traits, and Dmax explained nearly two-thirds of its variation. CHC and wing traits were most tightly integrated, whereas song varied more independently. We modeled the dependence of among-population trait divergence on genetic distance estimated from neutral markers to test for signatures of selection versus neutral divergence. For all three sexual trait types, phenotypic variation among populations was largely explained by a neutral model of divergence. Our findings illustrate how phenotypic integration across different types of sexual traits might impose constraints on the evolution of mating isolation and divergence via sexual selection.

International audience; The evolutionary consequences of phenotypic plasticity are debated. For example, reproductive barriers between incipient species can depend on the social environment, but most evidence for this comes from studies focusing on the effects of experiencing heterospecific individuals of the opposite sex. In Drosophila melanogaster, males are well known to invest strategically in ejaculate components and show different courtship behavior when reared in the presence of male competitors. It is unknown whether such plasticity in response to same-sex social experience influences sexual isolation, so we tested this using African and cosmopolitan lines, which show partial sexual isolation. Males were housed in social isolation, with homopopulation, or with heteropopulation male partners. We then measured their mating success, latency, and duration, their paternity share, and female remating success. Isolated males copulated for a shorter duration than males housed with any male partners. However, we found no difference in any measure between homopopulation or heteropopulation treatments. Our findings suggest that the male intrasexual competitive social environment does not strongly influence sexual isolation in D. melanogaster, and that plastic effects on reproductive isolation may be influenced more strongly by the experience of social isolation than by the composition of individuals within different social environments. Lay Summary The strength of reproductive isolation between diverging populations may depend on the social interactions experienced by individuals. We used partially isolated populations of fruit flies, Drosophila melanogaster, and showed that whether males had previously interacted with homopopulation or heteropopulation male partners did not affect the strength of premating or postmating sexual isolation. Thus, although male sexual traits are highly labile, this flexibility does not seem to affect the strength of sexual isolation in this system.

NWB is grateful to the Natural Environmental Research Council for funding that supported this work (NE/L011255/1). Male same-sex sexual behaviour (SSB), where males court or attempt to mate with other males, is common among animal taxa. Recent studies have examined its fitness costs and benefits in attempts to understand its evolutionary maintenance, but the evolutionary consequences of SSB are less commonly considered. One potential impact of SSB might be to facilitate the evolution of traits associated with less sexually dimorphic males, such as alternative reproductive tactics, by diverting costly aggression from other males. To test this, we capitalized on the recent rapid spread of a silent male morph of the field cricket, Teleogryllus oceanicus, which is unable to produce characteristic male acoustic signals, benefits from satellite mating behaviour and has feminized appearance and cuticular hydrocarbon profiles. We tested the prediction that interactions involving these nonsignalling, less sexually dimorphic male morphs would show heightened rates of SSB, which could reduce the strength of male–male competition and permit greater access to females. We found no evidence that SSB was more common in trials involving silent males. Instead, SSB was predicted by courtship of females presented during a pretrial treatment. Our results provide evidence supporting the view that SSB represents a spillover of sexually selected courtship behaviour in a nonadaptive context, but do not support a strong role for SSB in the evolution of less ornamented males in this system. Postprint

Funding: UK Natural Environment Research Council Grants NE/I027800/1, NE/G014906/1, and NE/L011255/1 (to N.W.B.) and Leverhulme Trust Grant RPG-2014-284 (to F.M.-Z.) The mechanisms underlying rapid macroevolution are controversial. One largely untested hypothesis that could inform this debate is that evolutionary reversals might release variation in vestigial traits, which then facilitates subsequent diversification. We evaluated this idea by testing key predictions about vestigial traits arising from sexual trait reversal in wild field crickets. In Hawaiian Teleogryllus oceanicus, the recent genetic loss of sound-producing and -amplifying structures on male wings eliminates their acoustic signals. Silence protects these “flatwing” males from an acoustically orienting parasitoid and appears to have evolved independently more than once. Here, we report that flatwing males show enhanced variation in vestigial resonator morphology under varied genetic backgrounds. Using laser Doppler vibrometry, we found that these vestigial sound-producing wing features resonate at highly variable acoustic frequencies well outside the normal range for this species. These results satisfy two important criteria for a mechanism driving rapid evolutionary diversification: Sexual signal loss was accompanied by a release of vestigial morphological variants, and these could facilitate the rapid evolution of novel signal values. Widespread secondary trait losses have been inferred from fossil and phylogenetic evidence across numerous taxa, and our results suggest that such reversals could play a role in shaping historical patterns of diversification. Postprint

Funding: Bioinformatic analyses were supported by the University of St Andrew Bioinformatics Unit (Wellcome Trust ISSF award 105621/Z/14/Z). This work was supported by funding to N.W.B. from the UK Natural Environment Research Council which is gratefully acknowledged (NE/I027800/1, NE/G014906/1, NE/L011255/1). The loss of sexual ornaments is observed across taxa, and pleiotropic effects of such losses provide an opportunity to gain insight into underlying dynamics of sex-biased gene expression and intralocus sexual conflict (IASC). We investigated this in a Hawaiian field cricket, Teleogryllus oceanicus, in which an X-linked genotype (flatwing) feminises males’ wings and eliminates their ability to produce sexually selected songs. We profiled adult gene expression across somatic and reproductive tissues of both sexes. Despite the feminising effect of flatwing on male wings, we found no evidence of feminised gene expression in males. Instead, female transcriptomes were more strongly affected by flatwing than males’, and exhibited demasculinised gene expression. These findings are consistent with a relaxation of IASC constraining female gene expression through loss of a male sexual ornament. In a follow-up experiment we found reduced testes mass in flatwing males, whereas female carriers showed no reduction in egg production. In contrast, female carriers exhibited greater measures of body condition. Our results suggest sex-limited phenotypic expression offers only partial resolution to intralocus sexual conflict, owing to pleiotropic effects of the loci involved. Benefits conferred by release from intralocus conflict could help explain widespread loss of sexual ornaments across taxa. Postprint

Secondary trait loss is widespread and has profound consequences, from generating diversity to driving adaptation. Sexual trait loss is particularly common. Its genomic impact is challenging to reconstruct because most reversals occurred in the distant evolutionary past and must be inferred indirectly, and questions remain about the extent of disruption caused by pleiotropy, altered gene expression and loss of homeostasis. We tested the genomic signature of recent sexual signal loss in Hawaiian field crickets, Teleogryllus oceanicus. Song loss is controlled by a sex-linked Mendelian locus, flatwing, which feminises male wings by erasing sound-producing veins. This variant spread rapidly under pressure from an eavesdropping parasitoid fly. We sequenced, assembled and annotated the T. oceanicus genome, produced a high-density linkage map, and localised flatwing on the X chromosome. We characterised pleiotropic effects of flatwing, including changes in embryonic gene expression and alteration of another sexual signal, chemical pheromones. Song loss is associated with pleiotropy, hitchhiking and genome-wide regulatory disruption which feminises flatwing male pheromones. The footprint of recent adaptive trait loss illustrates R. A. Fisher's influential prediction that variants with large mutational effect sizes can invade genomes during the earliest stages of adaptation to extreme pressures, despite having severely disruptive genomic consequences.

NWB was funded by fellowships from the UK Natural Environment Research Council [NE/G014906/1 and NE/L011255/1]. Our understanding of the evolutionary stability of socially‐selected traits is dominated by sexual selection models originating with R. A. Fisher, in which genetic covariance arising through assortative mating can trigger exponential, runaway trait evolution. To examine whether non‐reproductive, socially‐selected traits experience similar dynamics—social runaway—when assortative mating does not automatically generate a covariance, we modelled the evolution of socially‐selected badge and donation phenotypes incorporating indirect genetic effects (IGEs) arising from the social environment. We establish a social runaway criterion based on the interaction coefficient, ψ, which describes social effects on badge and donation traits. Our models make several predictions. (1) IGEs can drive the original evolution of altruistic interactions that depend on receiver badges. (2) Donation traits are more likely to be susceptible to IGEs than badge traits. (3) Runaway dynamics in non‐sexual, social contexts can occur in the absence of a genetic covariance. (4) Traits elaborated by social runaway are more likely to involve reciprocal, but non‐symmetrical, social plasticity. Models incorporating plasticity to the social environment via IGEs illustrate conditions favouring social runaway, describe a mechanism underlying the origins of costly traits such as altruism, and support a fundamental role for phenotypic plasticity in rapid social evolution. Postprint

This work was funded by Natural 524 Environment Research Council grants (NE/I027800/1, NE/G014906/1, NE/L011255/1). Recent theory predicts that increased phenotypic plasticity can facilitate adaptation as traits respond to selection. When genetic adaptation alters the social environment, socially mediated plasticity could cause co-evolutionary feedback dynamics that increase adaptive potential. We tested this by asking whether neural gene expression in a recently arisen, adaptive morph of the field cricket Teleogryllus oceanicus is more responsive to the social environment than the ancestral morph. Silent males (flatwings) rapidly spread in a Hawaiian population subject to acoustically orienting parasitoids, changing the population's acoustic environment. Experimental altering crickets’ acoustic environments during rearing revealed broad, plastic changes in gene expression. However, flatwing genotypes showed increased socially mediated plasticity, whereas normal-wing genotypes exhibited negligible expression plasticity. Increased plasticity in flatwing crickets suggests a coevolutionary process coupling socially flexible gene expression with the abrupt spread of flatwing. Our results support predictions that phenotypic plasticity should rapidly evolve to be more pronounced during early phases of adaptation. Postprint

This researchwas supported by Natural Environment Research Council grants to N.W.B. (NE/L011255/1 and NE/I027800/1). The evolutionary loss of sexual traits is widely predicted. Because sexual signals can arise from the coupling of specialized motor activity with morphological structures, disruption to a single component could lead to overall loss of function. Opportunities to observe this process and characterize any remaining signal components are rare, but could provide insight into the mechanisms, indirect costs and evolutionary consequences of signal loss. We investigated the recent evolutionary loss of a long-range acoustic sexual signal in the Hawaiian field cricket Teleogryllus oceanicus. Flatwing males carry mutations that remove sound-producing wing structures, eliminating all acoustic signalling and affording protection against an acoustically-orientating parasitoid fly. We show that flatwing males produce wing movement patterns indistinguishable from those that generate sonorous calling song in normal-wing males. Evolutionary song loss caused by the disappearance of structural components of the sound-producing apparatus has left behind the energetically costly motor behaviour underlying normal singing. These results provide a rare example of a vestigial behaviour and raise the possibility that such traits could be co-opted for novel functions. Postprint

International audience

N.W.B. received funding from Natural Environment Research Council fellowships (NE/G014906/1 and NE/L011255/1). M.Z. is supported by grants from the US National Science Foundation and by the University of Minnesota. Data used in these analyses (counts of crickets in survey plots and distances from playback speakers) have been placed in the Dryad Digital Repository and are accessible at https://doi.org/10.5061/dryad.bb384 (Zuk et al., 2018). 1. Sexual signals may be acquired or lost over evolutionary time, and are tempered in their exaggeration by natural selection. 2. In the Pacific field cricket, Teleogryllus oceanicus, a mutation (“flatwing”) causing loss of the sexual signal, the song, spread in

Funding support to N.W.B. from the Natural Environment Research Council (NE/G014906/1, NE/L011255/1, NE/I027800/1) Effective recognition of conspecific mating signals reduces the risk of maladaptive hybridization. Dissecting the signal recognition algorithms that underlie preferences is a useful approach for testing whether closely related taxa evaluate the same or different signal features to achieve mate recognition. Such data provide information about potential constraints and targets of selection during evolutionary divergence. Using a series of mate choice trials, we tested whether closely related, but genetically and phenotypically divergent, field cricket species (Teleogryllus oceanicus and Teleogryllus commodus) use shared or distinct recognition algorithms when evaluating acoustic male calling songs. These species overlap in sympatry, show premating isolation based on female discrimination of male calling songs, yet are capable of producing hybrid offspring. Unexpectedly, female selectivity for features of male song differed between the two species. We found that the two species use a combination of shared and unique signal filtering mechanisms, and we characterized how information about male carrier frequency, pulse rate and temporal patterning is integrated to achieve song recognition in each species. These results illustrate how comparatively few, simple modifications in key components of signal recognition algorithms can lead to striking interspecific discrimination between closely related taxa, despite apparent signal complexity. The finding that some steps during signal recognition and filtering are shared between the species, while others differ, can help to identify behavioural traits targeted by selection during evolutionary divergence. Postprint

Fisher's mechanism of sexual selection is a fundamental element of evolutionary theory. In it nonrandom mate choice causes a genetic covariance between a male trait and female preference for that trait and thereby generates a positive feedback process sustaining accelerated coevolution of the trait and preference. Numerous theoretical models of Fisher's mechanism have confirmed its mathematical underpinnings, yet biologists have often failed to find evidence for trait-preference genetic correlation in populations in which the mechanism was expected to function. We undertook a survey of the literature to conduct a formal meta-analysis probing the incidence and strength of trait-preference correlation among animal species. Our meta-analysis found significant positive genetic correlations in fewer than 20% of the species studied and an overall weighted correlation that is slightly positive. Importantly, a significant positive correlation was not found in any thorough study that included multiple subgroups. We discuss several ways in which the dynamic, multivariate nature of mate choice may reduce the trait-preference genetic correlation predicted by Fisher's mechanism. We then entertain the possibilities that Fisherian-like processes sometimes function without genetic correlation, and that mate choice may persist in a population as long as genetic correlation, and therefore Fisher's mechanism, occurs intermittently.

SummaryThe earliest stages of convergent evolution are difficult to observe in the wild, limiting our understanding of the incipient genomic architecture underlying convergent phenotypes [1, 2]. To address this, we capitalized on a novel trait, flatwing, that arose and proliferated at the start of the 21st century in a population of field crickets (Teleogryllus oceanicus) on the Hawaiian island of Kauai [3]. Flatwing erases sound-producing structures on male forewings. Mutant males cannot sing to attract females, but they are protected from fatal attack by an acoustically orienting parasitoid fly (Ormia ochracea). Two years later, the silent morph appeared on the neighboring island of Oahu. We tested two hypotheses for the evolutionary origin of flatwings in Hawaii: (1) that the silent morph originated on Kauai and subsequently introgressed into Oahu and (2) that flatwing originated independently on each island. Morphometric analysis of male wings revealed that Kauai flatwings almost completely lack typical derived structures, whereas Oahu flatwings retain noticeably more wild-type wing venation. Using standard genetic crosses, we confirmed that the mutation segregates as a single-locus, sex-linked Mendelian trait on both islands. However, genome-wide scans using RAD-seq recovered almost completely distinct markers linked with flatwing on each island. The patterns of allelic association with flatwing on either island reveal different genomic architectures consistent with the timing of two mutational events on the X chromosome. Divergent wing morphologies linked to different loci thus cause identical behavioral outcomes—silence—illustrating the power of selection to rapidly shape convergent adaptations from distinct genomic starting points.

Indirect genetic effects (IGEs) occur when genes expressed in one individual alter the phenotype of an interacting partner. IGEs can dramatically affect the expression and evolution of social traits. However, the interacting phenotype(s) through which they are transmitted are often unknown, or cryptic, and their detection would enhance our ability to accurately predict evolutionary change. To illustrate this challenge and possible solutions to it, we assayed male leg-tapping behavior using inbred lines of Drosophila melanogaster paired with a common focal male strain. The expression of tapping in focal males was dependent on the genotype of their interacting partner, but this strong IGE was cryptic. Using a multiple-regression approach, we identified male startle response as a candidate interacting phenotype: the longer it took interacting males to settle after being startled, the less focal males tapped them. A genome-wide association analysis identified approximately a dozen candidate protein-coding genes potentially underlying the IGE, of which the most significant was slowpoke. Our methodological framework provides information about candidate phenotypes and candidate single-nucleotide polymorphisms that underpin a strong yet cryptic IGE. We discuss how this approach can facilitate the detection of cryptic IGEs contributing to unusual evolutionary dynamics in other study systems.

A study of tropical crickets suggests that a twitchy response to ultrasonic bat calls has been co-opted for mate location. The neuroethological approach picks apart some surprising evolutionary steps that could inform the widespread occurrence of complex duetting behaviour.

Social influences on mate choice are predicted to influence evolutionary divergence of closely related taxa, because of the key role mate choice plays in reproductive isolation. However, it is unclear whether females choosing between heterospecific and conspecific male signals use previously experienced social information in the same manner or to the same extent that they do when discriminating among conspecific mates only. We tested this using two field cricket sister species (Teleogryllus oceanicus and Teleogryllus commodus), in which considerable information is known about the role of male calling song in premating isolation, in addition to the influence of acoustic experience on the development of reproductive traits. We manipulated the acoustic experience of replicate populations of both species and found, unexpectedly, that experience of male calling song during rearing did not change how accurate females were in choosing a conspecific over a heterospecific male song during playback trials. However, females with acoustic experience were considerably less responsive to male song compared with naïve females. Our results suggest that variation in the acoustic environment affects mate choice in both species, but that it may have a limited impact on premating isolation. The fact that social flexibility during interspecific mate discrimination does not appear to operate identically to that which occurs during conspecific mate discrimination highlights the importance of considering the context in which animals exercise socially flexible mating behaviours. We suggest an explanation for why social flexibility might be context dependent and discuss the consequences of such flexibility for the evolution of reproductive isolation.

This work was funded by NERC (NE/G014906/1, NE/L011255/1, NE/I027800/1). Additional funding from the Orthopterists’ Society to PM is also gratefully acknowledged. The prevalence of Haldane’s rule suggests that sex chromosomes commonly have a key role in reproductive barriers and speciation. However, the majority of research on Haldane’s rule has been conducted in species with conventional sex determination systems (XY and ZW) and exceptions to the rule have been understudied. Here we test the role of X-linked incompatibilities in a rare exception to Haldane’s rule for female sterility in field cricket sister species (Teleogryllus oceanicus and T. commodus). Both have an XO sex determination system. Using three generations of crosses, we introgressed X chromosomes from each species onto different, mixed genomic backgrounds to test predictions about the fertility and viability of each cross type. We predicted that females with two different species X chromosomes would suffer reduced fertility and viability compared with females with two parental X chromosomes. However, we found no strong support for such X-linked incompatibilities. Our results preclude X–X incompatibilities and instead support an interchromosomal epistatic basis to hybrid female sterility. We discuss the broader implications of these findings, principally whether deviations from Haldane’s rule might be more prevalent in species without dimorphic sex chromosomes. Postprint

Sexual selection can target many different types of traits. However, the relative influence of different sexually selected traits during evolutionary divergence is poorly understood. We used the field cricket Teleogryllus oceanicus to quantify and compare how five traits from each of three sexual signal modalities and components diverge among allopatric populations: male advertisement song, cuticular hydrocarbon (CHC) profiles and forewing morphology. Population divergence was unexpectedly consistent: we estimated the among-population (genetic) variance-covariance matrix, D, for all 15 traits, and D

There exist several high-order sandwich panel theories, most notably, the first to be introduced high-order sandwich panel theory (HSAPT) assumes a constant shear stress in the core. Recently, the extended high-order sandwich panel theory (EHSAPT) was introduced, its novelty being that it allows for three generalized coordinates in the core (the axial and transverse displacements at the centroid of the core, and the rotation at the centroid of the core) instead of just one (shear stress in the core) of the earlier theory. In this paper, the EHSAPT formulation for predicting the critical wrinkling load is presented for a simply supported sandwich of general asymmetric construction. The cases of (i) applying the loading just on the face sheets with a linear core assumption and (ii) applying uniform strain loading throughout the thickness of the panel and a nonlinear core assumption are examined. The results are compared with a benchmark elasticity solution. In addition, edgewise compression experiments were conducted on glass face/Nomex honeycomb core and the ensuing wrinkling point is compared with the theoretical predictions. A comparison is also made with earlier edgewise compression experiments on aluminum face/granulated-cork core reported in literature. Other wrinkling formulas that are included in the comparison are: Hoff–Mautner and the HSAPT.

Female mating preferences are often flexible, reflecting the social environment in which they are expressed. Associated indirect genetic effects (IGEs) can affect the rate and direction of evolutionary change, but sexual selection models do not capture these dynamics. We incorporate IGEs into quantitative genetic models to explore how variation in social environments and mate choice flexibility influence Fisherian sexual selection. The importance of IGEs is that runaway sexual selection can occur in the absence of a genetic correlation between male traits and female preferences. Social influences can facilitate the initiation of the runaway process and increase the rate of trait elaboration. Incorporating costs to choice do not alter the main findings. Our model provides testable predictions: (1) genetic covariances between male traits and female preferences may not exist, (2) social flexibility in female choice will be common in populations experiencing strong sexual selection, (3) variation in social environments should be associated with rapid sexual trait divergence, and (4) secondary sexual traits will be more elaborate than previously predicted. Allowing feedback from the social environment resolves discrepancies between theoretical predictions and empirical data, such as why indirect selection on female preferences, theoretically weak, might be sufficient for preferences to become elaborated.

Social experience can elicit phenotypically plastic changes in mate choice, but little is known about the degree to which social information from one modality can influence mating decisions based on information from a different modality. I used the field cricket Teleogryllus oceanicus to test whether experience of chemical cues mimicking a high density of sexually mature males causes changes in mate choice based on acoustic signals. T. oceanicus males produce long-range calling songs to attract females for mating, but they also produce waxy, non-volatile hydrocarbons on their cuticle (CHCs) which, when deposited on a substrate, can be detected by females and may provide demographic information. I manipulated female experience of substrate-bound male CHCs and then performed acoustic mate choice trials. When CHCs were present on the substrate during trials, females showed greater motivation to respond to male calling song. This effect diminished with repeated exposure to male songs, demonstrating that the importance of olfactory cues in altering acoustic mate choice decreased with increasing exposure to acoustic signals. However, the temporal nature of CHC experience mattered: previous experience of CHCs did not alter subsequent female choice for male calling song traits. Exposure to male song increased the threshold of mate acceptance over time, and individuals varied considerably in overall levels of responsiveness. Taken together, the results demonstrate that mate choice is dependent on social context mediated by multiple modalities in T. oceanicus, but they do not support the idea that prior experience of social cues in one modality necessarily influences later mating decisions based on other signalling modalities.

Modifications in female mate choice resulting from social experience can affect male reproductive success, thereby influencing the evolution of male secondary sexual characters. However, there is little information about how social experience affects different stages of female choice, for example, pre- versus postcopulatory choice, and whether social experience exerts parallel or divergent effects. Using field crickets, we tested 1) how prior experience with males of varying attractiveness modifies females' precopulatory and postcopulatory mate choice during subsequent mating encounters and 2) whether socially mediated changes in precopulatory choice reinforce or oppose changes in postcopulatory choice. We manipulated the attractiveness of males that females experienced by surgically silencing them and playing back artificially constructed courtship songs during preliminary mating trials. This experience, mediated solely by acoustic signals, had long-term effects on both pre- and postcopulatory choice during subsequent mating trials. Experience with an attractive male 24 h earlier caused females to mount subsequent males more slowly and retain their spermatophore for less time, whereas experience with an unattractive male caused females to mount subsequent males faster and retain their spermatophores for longer. Prior experience had a parallel effect on pre- and postcopulatory choice. The perceived attractiveness of previously encountered males, mediated by their courtship song, appears to strongly influence the reproductive success of subsequent males via alterations in pre- and postcopulatory female choice, confirming key predictions of theoretical models of sexual selection and mate choice that incorporate social effects. Copyright 2011, Oxford University Press.

Summary Developmental plasticity allows juvenile animals to assess environmental cues and adaptively shape behavioral and morphological traits to maximize fitness in their adult environment [1]. Sexual signals are particularly conspicuous cues, making them likely candidates for mediating such responses. Plasticity in male reproductive traits is a common phenomenon, but empirical evidence for signal-mediated plasticity in males is lacking. We tested whether experience of acoustic sexual signals during juvenile stages influences the development of three adult traits in the continuously breeding field cricket Teleogryllus oceanicus : male mating tactics, reproductive investment, and condition. All three traits were affected by juvenile acoustic experience. Males of this species produce a long-range calling song to attract receptive females, but they can also behave as satellites by parasitizing other males' calls [2]. Males reared in an environment mimicking a population with many calling males were less likely to exhibit satellite behavior, invested more in reproductive tissues, and attained higher condition than males reared in a silent environment. These results contrast with other studies [3] and demonstrate how the effects of juvenile social experience on adult male morphology, reproductive investment, and behavior may subsequently influence sexual selection and phenotypic evolution.

Prevailing models of animal communication assume that signalling during aggressive conflict mitigates the costs of fighting. We tested this assumption by staging dyadic encounters between male field crickets, Teleogryllus oceanicus , under three conditions: (i) both males could sing aggressive songs, (ii) neither male could sing, and (iii) one male could sing but the other could not. We conducted experiments on males from a Hawaiian population from Kauai that has recently evolved signal loss, and males from a Hawaiian population from the Big Island that has not. Among both populations, interactions between two silent males were characterized by higher levels of aggression than interactions involving one or two singing males. Because the level of aggression is strongly related to the cost of fighting, these data demonstrate that signalling mitigates the cost of fighting. In mixed trials, we found no statistically significant differences between the behaviour of calling and non-calling males in either population. We conclude that there is no evidence that the Kauai population exhibits special adaptations to alleviate the costs of signal loss. Finally, we found that males were much more likely to signal after their opponent's retreat than after their own retreat. Aggressive song therefore meets the definition of a ‘victory display’.

Same-sex sexual behavior has been extensively documented in non-human animals. Here we review the contexts in which it has been studied, focusing on case studies that have tested both adaptive and non-adaptive explanations for the persistence of same-sex sexual behavior. Researchers have begun to make headway unraveling possible evolutionary origins of these behaviors and reasons for their maintenance in populations, and we advocate expanding these approaches to examine their role as agents of evolutionary change. Future research employing theoretical, comparative and experimental approaches could provide a greater understanding not only of how selection might have driven the evolution of same-sex sexual behaviors but also ways in which such behaviors act as selective forces that shape social, morphological and behavioral evolution.

Sexual signals consist of multiple components, each of which can contribute to mating decisions. Male field crickets use 2 acoustic signals in the context of mating: a calling song that attracts females from a distance and a courtship song that follows once a female makes physical contact with a male. The function of courtship is unclear because females have already chosen and approached a particular male based on his calling song. Using the field cricket Teleogryllus oceanicus, we tested whether females evaluate the attractiveness of males based on their courtship song irrespective of other male qualities. In a tournament-style assay, females chose males based on elements of their courtship song and preferred males with longer courtship songs that had a higher duty cycle (more sound per unit time). Courtship song was also highly repeatable not only within a bout but also between days in the presence of different females. Additionally, we manipulated the attractiveness of males to females by surgically silencing males and broadcasting playbacks of artificially constructed courtship songs. When we broadcast a preferred song model during courtship by previously nonpreferred males, females showed greater attraction, and vice versa. Courtship song may be particularly important in systems with satellite males that do not produce long-range signals because it gives females their only opportunity to evaluate potential mates. Key words: courtship song, mate choice, multiple signals, repeatability, Teleogryllus oceanicus. [Behav Ecol]

Female choice can drive the evolution of extravagant male traits. In invertebrates, the influence of prior social experience on female choice has only recently been considered. To better understand the evolutionary implications of experience-mediated plasticity in female choice, we investigated the effect of acoustic experience during rearing on female responsiveness to male song in the field cricket Teleogryllus oceanicus . Acoustic experience has unique biological relevance in this species: a morphological mutation has rendered over 90 per cent of males on the Hawaiian island of Kauai silent in fewer than 20 generations, impeding females' abilities to locate potential mates. Females reared in silent conditions mimicking Kauai were less discriminating of male calling song and more responsive to playbacks, compared with females that experienced song during rearing. Our results to our knowledge, are the first demonstration of long-term effects of acoustic experience in an arthropod, and suggest that female T. oceanicus may be able to compensate for the reduced availability of long-range male sexual signals by increasing their responsiveness to the few remaining signallers. Understanding the adaptive significance of experience-mediated plasticity in female choice provides insight into processes that facilitate rapid evolutionary change and shape sexual selection pressure in natural populations.

Female mate choice is a driving force in the evolution of male secondary sexual characters. It can be dissected into several components: discrimination describes the degree to which females distinguish male trait variation, responsiveness indicates the speed or likelihood of females’ reactions to a mate, and preference functions illustrate how the probability of mating relates to male trait variation. Relatively little is known about how these components interact to produce final mating decisions and influence the strength and direction of sexual selection, so I used female field crickets (Teleogryllus oceanicus) to measure interactions between individual preference functions, discrimination, and 2 measures of responsiveness (number of responses and response effort). Preference function shape varied considerably between individual females. Highly discriminating females showed greater numbers of responses to playbacks and were more likely to have stabilizing preference functions. When I constructed 2 population-level preference functions using either response number or response effort, the first yielded a linear, directional function, whereas the second implied a stabilizing function. The clear differences between the 2 imply that different components of female choice can exert contrasting selection pressure on a single male trait. Overall, both response number and discrimination were mutually reinforcing and likely govern the strength of sexual selection in this population. The direction of selection in a wild setting ultimately depends on the relative importance of response number versus response effort, where exogenous factors such as predation risk or density will determine which component of female choice predominates mating decisions. Key words: choosiness, discrimination, mate choice, preference function, sexual selection, Teleogryllus oceanicus. [Behav Ecol]

Behavioral preadaptations can provide an accommodating environment in which novel morphological characters may be selected. A very recent morphological mutation, flatwing, has caused the loss of male song in field crickets (Teleogryllus oceanicus) from the Hawaiian island of Kauai. Previous studies in this and related species have shown that females require male courtship song to mount males, but flatwing T. oceanicus males still achieve matings. Females from Kauai may have a relaxed requirement for male courtship song, or flatwing males may compensate for their inability to sing by altering other courtship behaviors. We tested whether male courtship and female responses to male courtship were preadapted in a way that facilitated the spread of the male wing mutation or if parallel changes in male courtship and female responses accompanied the mutation. We performed mating trials in 2 captive-bred populations to assess how mating behavior varied depending on the presence or absence of courtship song playback. The first was an ancestral population from Kauai established prior to the emergence of the flatwing mutation, and the second was derived from Kauai after the mutation became prevalent. Mating behaviors did not differ qualitatively or quantitatively between the ancestral and current populations, and females from both accepted males for mating in the absence of courtship song. Our results provide direct evidence that a mechanism allowing flatwing males to mate with females was in place before the mutation actually arose on Kauai and demonstrate how preexisting behavior facilitated the rapid spread of a novel morphological mutation. Copyright 2008, Oxford University Press.

A major advance in modern evolutionary biology is the ability to start linking phenotypic evolution in the wild with genomic changes that underlie that evolution. We capitalised on a rapidly-evolving Hawaiian population of crickets (Teleogryllus oceanicus) to test hypotheses about the genomic consequences of a recent Mendelian mutation of large effect which disrupts the development of sound-producing structures on male forewings. The resulting silent phenotype, flatwing, persists because of natural selection imposed by an acoustically-orienting parasitoid, but it interferes with mate attraction. We examined gene expression differences in developing wing buds of wild-type and flatwing male crickets using RNA-seq and quantitative proteomics. Most differentially expressed (DE) transcripts were down-regulated in flatwing males (625 up vs. 1716 down), whereas up and down-regulated proteins were equally represented (30 up and 34 down). Differences between morphs were clearly not restricted to a single pathway, and we recovered annotations associated with a broad array of functions that would not be predicted a priori. Using a candidate gene detection test based on homology we identified 30% of putative Drosophila wing development genes in the cricket transcriptome, but only 10% were DE. In addition to wing related annotations, endocrine pathways and several biological processes such as reproduction, immunity and locomotion were DE in the mutant crickets at both biological levels. Our results illuminate the breadth of genetic pathways that are potentially affected in the early stages of adaptation. Postprint

Debates about how coevolution of sexual traits and preferences might promote evolutionary diversification have permeated speciation research for over a century. Recent work demonstrates that the expression of such traits can be sensitive to variation in the social environment. Here, we examined social flexibility in a sexually selected male trait-cuticular hydrocarbon (CHC) profiles-in the field cricket Teleogryllus oceanicus and tested whether population genetic divergence predicts the extent or direction of social flexibility in allopatric populations. We manipulated male crickets' social environments during rearing and then characterized CHC profiles. CHC signatures varied considerably across populations and also in response to the social environment, but our prediction that increased social flexibility would be selected in more recently founded populations exposed to fluctuating demographic environments was unsupported. Furthermore, models examining the influence of drift and selection failed to support a role of sexual selection in driving population divergence in CHC profiles. Variation in social environments might alter the dynamics of sexual selection, but our results align with theoretical predictions that the role social flexibility plays in modulating evolutionary divergence depends critically on whether responses to variation in the social environment are homogeneous across populations, or whether gene by social environment interactions occur.