Competing adaptations maintain nonadaptive variation in a wild cricket population.

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.

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.

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.

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.

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.

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.

Testing the role of trait reversal in evolutionary diversification using song loss in wild crickets.

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.

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.

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.

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.