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How emerging adaptive variants interact is an important factor in the evolution of wild populations, but the opportunity to empirically study this interaction is rare. We recently documented the emergence of an adaptive phenotype "curly-wing" in Hawaiian populations of field crickets (Teleogryllus oceanicus). Curly-wing inhibits males' ability to sing, protecting them from eavesdropping parasitoid flies (Ormia ochracea). Surprisingly, curly-wing co-occurs with similarly protective silent "flatwing" phenotypes in multiple populations, in which neither phenotype has spread to fixation. These two phenotypes are frequently coexpressed, but since either sufficiently reduces song amplitude to evade the fly, their coexpression confers no additional fitness benefit. Numerous "off-target" phenotypic changes are known to accompany flatwing, and we find that curly-wing, too, negatively impacts male courtship ability and affects mass and survival of females under lab conditions. We show through crosses and genomic and mRNA sequencing that curly-wing expression is associated with variation on a single autosome. In parallel analyses of flatwing, our results reinforce previous findings of X-linked single-locus inheritance. By combining insights into the genetic architecture of these alternative phenotypes with simulations and field observations, we show that the co-occurrence of these two adaptations impedes either from fixing, despite extreme fitness benefits, due to fitness epistasis. This co-occurrence of similar adaptive forms in the same populations might be more common than is generally considered and could be an important force inhibiting adaptive evolution in wild populations of sexually reproducing organisms. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]