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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.

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. Gene flow is classically thought to impede local adaptation via parallel evolution. However, a genomic study on Hawaiian crickets from different island populations finds evidence of parallel adaptation to the same lethal parasitoid in spite of strong ongoing gene flow.

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.

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.

One of the most enduring mysteries in biology concerns the evolution of complex adaptations made up of interacting component traits. When these component traits do not enhance fitness independently of one another, their origin requires that they evolve sequentially through intermediate steps that do not produce their full adaptive value as a combined trait, or alternatively, that they arise via simultaneous, synergistic evolution. We tested these alternatives using the powerful but accessible example of leaf masquerade in katydids, where in some species, highly modified wings strikingly mimic vegetation to avoid predator recognition. Combining a field predation experiment with a phylogenetic comparative analysis of wing morphology in 58 Neotropical katydid species, we show that color and shape synergistically interact to enhance survival in the wild, and modifications in both traits evolved concurrently during diversification of this clade. Our findings identify the adaptive value of masquerade camouflage in the wild and show how concordant evolutionary change in separate traits—evolutionary synergy—can generate extraordinarily specialized, multi-component adaptations.

Theory predicts that compensatory genetic changes reduce negative indirect effects of selected variants during adaptive evolution, but evidence is scarce. Here, we test this in a wild population of Hawaiian crickets using temporal genomics and a high-quality chromosome-level cricket genome. In this population, a mutation, flatwing , silences males and rapidly spread due to an acoustically-orienting parasitoid. Our sampling spanned a social transition during which flatwing fixed and the population went silent. We find long-range linkage disequilibrium around the putative flatwing locus was maintained over time, and hitchhiking genes had functions related to negative flatwing -associated effects. We develop a combinatorial enrichment approach using transcriptome data to test for compensatory, intragenomic coevolution. Temporal changes in genomic selection were distributed genome-wide and functionally associated with the population’s transition to silence, particularly behavioural responses to silent environments. Our results demonstrate how ‘adaptation begets adaptation’; changes to the sociogenetic environment accompanying rapid trait evolution can generate selection provoking further, compensatory adaptation. Theory predicts that adaptive mutations can have indirect negative effects on fitness. This study demonstrates how ‘adaptation begets adaptation’: changes to the sociogenetic environment accompanying rapid adaptation in wild crickets provoked genome-wide compensatory adaptation.

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.

Predicting the function of a biological structure solely from its morphology can be a very powerful tool in several fields of biology, but especially in evolutionary reconstruction. In the field of invertebrate acoustic communication, reconstructing the acoustic properties of sound-producing forewings in crickets has been based on two very divergent methods, finite element modelling (FEM) and vibrometric measurements from preserved specimens. Both methods, however, make strong simplifying assumptions that have not been tested and the reliability of inferences made from either method remains in question. Here, we rigorously test and refine both reconstruction methods using the well-known Teleogryllus oceanicus model system and determine the appropriate conditions required to reconstruct the vibroacoustic behaviour of male forewings. We find that when using FEM it is not necessary to assume simplified boundary conditions if the appropriate parameters are found. When using preserved specimens, we find that the sample needs to be rehydrated for reliable reconstruction; however, it may be possible to accomplish rehydration in silico using FEM. Our findings provide a refined methodology for the reliable reconstruction of cricket songs, whether from fossils or preserved specimens from museums or field collections.

Farmed insects have gained attention as an alternative, sustainable source of protein with a lower carbon footprint than traditional livestock. We present a high‐quality reference genome for one of the most commonly farmed insects, the banded cricket Gryllodes sigillatus. In addition to its agricultural importance, G. sigillatus is also a model in behavioural and evolutionary ecology research on reproduction and mating systems. We report comparative genomic analyses that clarify the banded cricket's evolutionary history, identify gene family expansions and contractions unique to this lineage, associate these with agriculturally important traits, and identify targets for genome‐assisted breeding efforts. The high‐quality G. sigillatus genome assembly plus accompanying comparative genomic analyses serve as foundational resources for both applied and basic research on insect farming and behavioural biology, enabling researchers to pinpoint trait‐associated genetic variants, unravel functional pathways governing those phenotypes, and accelerate selective breeding efforts to increase the efficacy of large‐scale insect farming operations.

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.