Behavioural plasticity compensates for adaptive loss of cricket song.

Behavioural flexibility might help animals cope with costs of genetic variants under selection, promoting genetic adaptation. However, it has proven challenging to experimentally link behavioural flexibility to the predicted compensation of population-level fitness. We tested this prediction using the field cricket Teleogryllus oceanicus. In Hawaiian populations, a mutation silences males and protects against eavesdropping parasitoids. To examine how the loss of this critical acoustic communication signal impacts offspring production and mate location, we developed a high-resolution, individual-based tracking system for low-light, naturalistic conditions. Offspring production did not differ significantly in replicate silent versus singing populations, and fitness compensation in silent conditions was associated with significantly increased locomotion in both sexes. Our results provide evidence that flexible behaviour can promote genetic adaptation via compensation in reproductive output and suggest that rapid evolution of animal communication systems may be less constrained than previously appreciated.

Machine learning reveals singing rhythms of male Pacific field crickets are clock controlled.

Circadian rhythms are ubiquitous in nature and endogenous circadian clocks drive the daily expression of many fitness-related behaviors. However, little is known about whether such traits are targets of selection imposed by natural enemies. In Hawaiian populations of the nocturnally active Pacific field cricket (Teleogryllus oceanicus), males sing to attract mates, yet sexually selected singing rhythms are also subject to natural selection from the acoustically orienting and deadly parasitoid fly, Ormia ochracea. Here, we use T. oceanicus to test whether singing rhythms are endogenous and scheduled by circadian clocks, making them possible targets of selection imposed by flies. We also develop a novel audio-to-circadian analysis pipeline, capable of extracting useful parameters from which to train machine learning algorithms and process large quantities of audio data. Singing rhythms fulfilled all criteria for endogenous circadian clock control, including being driven by photoschedule, self-sustained periodicity of approximately 24 h, and being robust to variation in temperature. Furthermore, singing rhythms varied across individuals, which might suggest genetic variation on which natural and sexual selection pressures can act. Sexual signals and ornaments are well-known targets of selection by natural enemies, but our findings indicate that the circadian timing of those traits' expression may also determine fitness.

Rapid sexual signal diversification is facilitated by permissive females.

The initial process by which novel sexual signals evolve remains unclear, because rare new variants are susceptible to loss by drift or counterselection imposed by prevailing female preferences.1,2,3,4 We describe the diversification of an acoustic male courtship signal in Hawaiian populations of the field cricket Teleogryllus oceanicus, which was brought about by the evolution of a brachypterous wing morph ("small-wing") only 6 years ago.5 Small-wing has a genetic basis and causes silence or reduced-amplitude signaling by miniaturizing male forewings, conferring protection against an eavesdropping parasitoid, Ormia ochracea.5 We found that wing reduction notably increases the fundamental frequency of courtship song from an average of 5.1 kHz to 6.4 kHz. It also de-canalizes male song, broadening the range of peak signal frequencies well outside normal song character space. As courtship song prompts female mounting and is sexually selected,6,7,8,9 we evaluated two scenarios to test the fate of these new signal values. Females might show reduced acceptance of small-wing males, imposing counterselection via prevailing preferences. Alternatively, females might accept small-wing males as readily as long-wing males if their window of preference is sufficiently wide. Our results support the latter. Females preferred males who produced some signal over none, but they mounted sound-producing small-wing males as often as sound-producing long-wing males. Indiscriminate mating can facilitate the persistence of rare, novel signal values. If female permissiveness is a general characteristic of the earliest stages of sexual signal evolution, then taxa with low female mate acceptance thresholds should be more prone to diversification via sexual selection.

Social Plasticity Enhances Signal-Preference Codivergence.

AbstractThe social environment is often the most dynamic and fitness-relevant environment animals experience. Here we tested whether plasticity arising from variation in social environments can promote signal-preference divergence-a key prediction of recent speciation theory but one that has proven difficult to test in natural systems. Interactions in mixed social aggregations could reduce, create, or enhance signal-preference differences. In the latter case, social plasticity could establish or increase assortative mating. We tested this by rearing two recently diverged species of Enchenopa treehoppers-sap-feeding insects that communicate with plant-borne vibrational signals-in treatments consisting of mixed-species versus own-species aggregations. Social experience with heterospecifics (in the mixed-species treatment) resulted in enhanced signal-preference species differences. For one of the two species, we tested but found no differences in the plastic response between sympatric and allopatric sites, suggesting the absence of reinforcement in the signals and preferences and their plastic response. Our results support the hypothesis that social plasticity can create or enhance signal-preference differences and that this might occur in the absence of long-term selection against hybridization on plastic responses themselves. Such social plasticity may facilitate rapid bursts of diversification.

Intrasexual aggression reduces mating success in field crickets.

Aggressive behaviour is thought to have significant consequences for fitness, sexual selection and the evolution of social interactions, but studies measuring its expression across successive encounters-both intra- and intersexual-are limited. We used the field cricket Teleogryllus oceanicus to evaluate factors affecting repeatability of male aggression and its association with mating success. We quantified focal male aggression expressed towards partners and received from partners in three successive, paired trials, each involving a different male partner. We then measured a proxy of focal male fitness in mating trials with females. The likelihood and extent of aggressive behaviour varied across trials, but repeatability was negligible, and we found no evidence that patterns of focal aggression resulted from interacting partner identity or prior experience. Males who consistently experienced aggression in previous trials showed decreased male mating 'efficiency'-determined by the number of females a male encountered before successfully mating, but the effect was weak and we found no other evidence that intrasexual aggression was associated with later mating success. During mating trials, however, we observed unexpected male aggression towards females, and this was associated with markedly decreased male mating efficiency and success. Our findings suggest that nonadaptive aggressive spillover in intersexual mating contexts could be an important but underappreciated factor influencing the evolution of intrasexual aggression.

Within-generation and transgenerational social plasticity interact during rapid adaptive evolution.

The effects of within-generation plasticity vs. transgenerational plasticity on trait expression are poorly understood, but important for evaluating plasticity's evolutionary consequences. We tested how genetics, within-generation plasticity, and transgenerational plasticity jointly shape traits influencing rapid evolution in the field cricket Teleogryllus oceanicus. In Hawaiian populations attacked by acoustically orienting parasitoid flies, a protective, X-linked variant ("flatwing") eliminates male acoustic sexual signals. Silent males rapidly spread to fixation, dramatically changing the acoustic environment. First, we found evidence supporting flatwing-associated pleiotropy in juveniles: pure-breeding flatwing males and females exhibit greater locomotion than those with normal-wing genotypes. Second, within-generation plasticity caused homozygous-flatwing females developing in silence, which mimics all-flatwing populations, to attain lower adult body condition and reproductive investment than those experimentally exposed to song. Third, maternal song exposure caused transgenerational plasticity in offspring, affecting adult, but not juvenile, size, condition, and reproductive investment. This contrasted with behavioral traits, which were only influenced by within-generation plasticity. Fourth, we matched and mismatched maternal and offspring social environments and found that transgenerational plasticity sometimes interacted with within-generation plasticity and sometimes opposed it. Our findings stress the importance of evaluating plasticity of different traits and stages across generations when evaluating its fitness consequences and role in adaptation.

Ancestral sex-role plasticity facilitates the evolution of same-sex sexual behavior.

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.

Freshwater Salinization Syndrome Alters Retention and Release of 'Chemical Cocktails' along Flowpaths: from Stormwater Management to Urban Streams.

We investigate impacts of Freshwater Salinization Syndrome (FSS) on mobilization of salts, nutrients, and metals in urban streams and stormwater BMPs by analyzing original data on concentrations and fluxes of salts, nutrients, and metals from 7 urban watersheds in the Mid-Atlantic U.S. and synthesizing literature data. We also explore future critical research needs through a survey of practitioners and scientists. Our original data show: (1) sharp pulses in concentrations of salt ions and metals in urban streams directly following both road salt events and stream restoration construction (e.g., similar to the way concentrations increase during other soil disturbance activities); (2) sharp declines in pH (acidification) in response to road salt applications due to mobilization of H+ from soil exchange sites by Na+; (3) sharp increases in organic matter from microbial and algal sources (based on fluorescence spectroscopy) in response to road salt applications likely due to lysing cells and/or changes in solubility; (4) significant retention (~30-40%) of Na+ in stormwater BMP sediments and floodplains in response to salinization; (5) increased ion exchange and mobilization of diverse salt ions (Na+, Ca2+, K+, Mg2+), nutrients (N, P), and trace metals (Cu, Sr) from stormwater BMPs and restored streams in response to FSS; (6) downstream increasing loads of Cl-, SO4 2-, Br-, F-, and I- along flowpaths through urban streams, and P release from urban stormwater BMPs in response to salinization, and (7) a significant annual reduction (> 50%) in Na+ concentrations in an urban stream when road salt applications were dramatically reduced, which suggests potential for ecosystem recovery. We compared our original results to published metrics of contaminant retention and release across a broad range of stormwater management BMPs from North America and Europe. Overall, urban streams and stormwater management BMPs consistently retain Na+ and Cl- but mobilize multiple contaminants based on salt types and salinity levels. Finally, we present our top 10 research questions regarding FSS impacts on urban streams and stormwater management BMPs. Reducing diverse 'chemical cocktails' of contaminants mobilized by freshwater salinization is now a priority for effectively and holistically restoring urban waters.

The persistence and evolutionary consequences of vestigial behaviours.

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.

The Indirect Genetic Effect Interaction Coefficient ψ: Theoretically Essential and Empirically Neglected.

The interaction effect coefficient ψ has been a much-discussed, fundamental parameter of indirect genetic effect (IGE) models since its formal mathematical description in 1997. The coefficient simultaneously describes the form of changes in trait expression caused by genes in the social environment and predicts the evolutionary consequences of those IGEs. Here, we report a striking mismatch between theoretical emphasis on ψ and its usage in empirical studies. Surveying all IGE research, we find that the coefficient ψ has not been equivalently conceptualized across studies. Several issues related to its proper empirical measurement have recently been raised, and these may severely distort interpretations about the evolutionary consequences of IGEs. We provide practical advice on avoiding such pitfalls. The majority of empirical IGE studies use an alternative variance-partitioning approach rooted in well-established statistical quantitative genetics, but several hundred estimates of ψ (from 15 studies) have been published. A significant majority are positive. In addition, IGEs with feedback, that is, involving the same trait in both interacting partners, are far more likely to be positive and of greater magnitude. Although potentially challenging to measure without bias, ψ has critically-developed theoretical underpinnings that provide unique advantages for empirical work. We advocate for a shift in perspective for empirical work, from ψ as a description of IGEs, to ψ as a robust predictor of evolutionary change. Approaches that "run evolution forward" can take advantage of ψ to provide falsifiable predictions about specific trait interactions, providing much-needed insight into the evolutionary consequences of IGEs.

A neglected conceptual problem regarding phenotypic plasticity's role in adaptive evolution: The importance of genetic covariance and social drive.

There is tantalizing evidence that phenotypic plasticity can buffer novel, adaptive genetic variants long enough to permit their evolutionary spread, and this process is often invoked in explanations for rapid adaptive evolution. However, the strength and generality of evidence for it is controversial. We identify a conceptual problem affecting this debate: recombination, segregation, and independent assortment are expected to quickly sever associations between genes controlling novel adaptations and genes contributing to trait plasticity that facilitates the novel adaptations by reducing their indirect fitness costs. To make clearer predictions about this role of plasticity in facilitating genetic adaptation, we describe a testable genetic mechanism that resolves the problem: genetic covariance between new adaptive variants and trait plasticity that facilitates their persistence within populations. We identify genetic architectures that might lead to such a covariance, including genetic coupling via physical linkage and pleiotropy, and illustrate the consequences for adaptation rates using numerical simulations. Such genetic covariances may also arise from the social environment, and we suggest the indirect genetic effects that result could further accentuate the process of adaptation. We call the latter mechanism of adaptation social drive, and identify methods to test it. We suggest that genetic coupling of plasticity and adaptations could promote unusually rapid 'runaway' evolution of novel adaptations. The resultant dynamics could facilitate evolutionary rescue, adaptive radiations, the origin of novelties, and other commonly studied processes.

Variable dosage compensation is associated with female consequences of an X-linked, male-beneficial mutation.

Recent theory has suggested that dosage compensation mediates sexual antagonism over X-linked genes. This process relies on the assumption that dosage compensation scales phenotypic effects between the sexes, which is largely untested. We evaluated this by quantifying transcriptome variation associated with a recently arisen, male-beneficial, X-linked mutation across tissues of the field cricket Teleogryllus oceanicus, and testing the relationship between the completeness of dosage compensation and female phenotypic effects at the level of gene expression. Dosage compensation in T. oceanicus was variable across tissues but usually incomplete, such that relative expression of X-linked genes was typically greater in females. Supporting the assumption that dosage compensation scales phenotypic effects between the sexes, we found tissues with incomplete dosage compensation tended to show female-skewed effects of the X-linked allele. In gonads, where expression of X-linked genes was most strongly female-biased, ovaries-limited genes were much more likely to be X-linked than were testes-limited genes, supporting the view that incomplete dosage compensation favours feminization of the X. Our results support the expectation that sex chromosome dosage compensation scales phenotypic effects of X-linked genes between sexes, substantiating a key assumption underlying the theoretical role of dosage compensation in determining the dynamics of sexual antagonism on the X.

Rapid parallel adaptation despite gene flow in silent crickets.

Gene flow is predicted to impede parallel adaptation via de novo mutation, because it can introduce pre-existing adaptive alleles from population to population. We test this using Hawaiian crickets (Teleogryllus oceanicus) in which 'flatwing' males that lack sound-producing wing structures recently arose and spread under selection from an acoustically-orienting parasitoid. Morphometric and genetic comparisons identify distinct flatwing phenotypes in populations on three islands, localized to different loci. Nevertheless, we detect strong, recent and ongoing gene flow among the populations. Using genome scans and gene expression analysis we find that parallel evolution of flatwing on different islands is associated with shared genomic hotspots of adaptation that contain the gene doublesex, but the form of selection differs among islands and corresponds to known flatwing demographics in the wild. We thus show how parallel adaptation can occur on contemporary timescales despite gene flow, indicating that it could be less constrained than previously appreciated.

Immunogenetic and tolerance strategies against a novel parasitoid of wild field crickets.

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.

Can behaviour impede evolution? Persistence of singing effort after morphological song loss in crickets.

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.

Sexual selection and population divergence III: Interspecific and intraspecific variation in mating signals.

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.

Field cricket genome reveals the footprint of recent, abrupt adaptation in the wild.

Evolutionary adaptation is generally thought to occur through incremental mutational steps, but large mutational leaps can occur during its early stages. These are challenging to study in nature due to the difficulty of observing new genetic variants as they arise and spread, but characterizing their genomic dynamics is important for understanding factors favoring rapid adaptation. Here, we report genomic consequences of recent, adaptive song loss in a Hawaiian population of field crickets (Teleogryllus oceanicus). A discrete genetic variant, flatwing, appeared and spread approximately 15 years ago. Flatwing erases sound-producing veins on male wings. These silent flatwing males are protected from a lethal, eavesdropping parasitoid fly. We sequenced, assembled and annotated the cricket genome, produced a linkage map, and identified a flatwing quantitative trait locus covering a large region of the X chromosome. Gene expression profiling showed that flatwing is associated with extensive genome-wide effects on embryonic gene expression. We found that flatwing male crickets express feminized chemical pheromones. This male feminizing effect, on a different sexual signaling modality, is genetically associated with the flatwing genotype. Our findings suggest that the early stages of evolutionary adaptation to extreme pressures can be accompanied by greater genomic and phenotypic disruption than previously appreciated, and highlight how abrupt adaptation might involve suites of traits that arise through pleiotropy or genomic hitchhiking.

An evolutionary switch from sibling rivalry to sibling cooperation, caused by a sustained loss 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.

Social runaway: Fisherian elaboration (or reduction) of socially selected traits via indirect genetic effects.

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 nonreproductive, socially selected traits experience similar dynamics-social runaway-when assortative mating does not automatically generate a covariance, we modeled 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 nonsexual, social contexts can occur in the absence of a genetic covariance. (4) Traits elaborated by social runaway are more likely to involve reciprocal, but nonsymmetrical, social plasticity. Models incorporating plasticity to the social environment via IGEs illustrate conditions favoring 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.