Darren Rebar

The evolution and evolutionary consequences of social plasticity in mate preferences

In many animals, experience modifies behaviour in a variety of ways and contexts. Here we focus on experience of social environments and phenotypic plasticity in mate preferences. We first review adaptive hypotheses about the evolution of social plasticity in mate preferences, finding support for all of them across different species. We suggest that future work should assess which patterns of variation in social environments select for which forms of plasticity in mate preferences. We then highlight that social plasticity in mate preferences creates feedback loops between the role of social environments as causes of variation in phenotypes and the role of social environments as causes of selection on phenotypes. Fully understanding the consequences of these feedbacks will involve assessing both how selection shapes the plastic response to variation in social environments and how individuals in social environments are selected to influence the mate preferences of others. This task is just beginning, but we review evidence of genetic variation in both of these aspects of social plasticity in mate preferences.

Genetic variation in social influence on mate preferences

Patterns of phenotypic variation arise in part from plasticity owing to social interactions, and these patterns contribute, in turn, to the form of selection that shapes the variation we observe in natural populations. This proximate–ultimate dynamic brings genetic variation in social environments to the forefront of evolutionary theory. However, the extent of this variation remains largely unknown. Here, we use a member of the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae) to assess how mate preferences are influenced by genetic variation in the social environment. We used full-sibling split-families as ‘treatment’ social environments, and reared focal females alongside each treatment family, describing the mate preferences of the focal females. With this method, we detected substantial genetic variation in social influence on mate preferences. The mate preferences of focal females varied according to the treatment families along with which they grew up. We discuss the evolutionary implications of the presence of such genetic variation in social influence on mate preferences, including potential contributions to the maintenance of genetic variation, the promotion of divergence, and the adaptive evolution of social effects on fitness-related traits.

Insect mating signal and mate preference phenotypes covary among host plant genotypes

Sexual selection acting on small initial differences in mating signals and mate preferences can enhance signal–preference codivergence and reproductive isolation during speciation. However, the origin of initial differences in sexual traits remains unclear. We asked whether biotic environments, a source of variation in sexual traits, may provide a general solution to this problem. Specifically, we asked whether genetic variation in biotic environments provided by host plants can result in signal–preference phenotypic covariance in a host‐specific, plant‐feeding insect. We used a member of the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae) to assess patterns of variation in male mating signals and female mate preferences induced by genetic variation in host plants. We employed a novel implementation of a quantitative genetics method, rearing field‐collected treehoppers on a sample of naturally occurring replicated host plant clone lines. We found remarkably high signal–preference covariance among host plant genotypes. Thus, genetic variation in biotic environments influences the sexual phenotypes of organisms living on those environments in a way that promotes assortative mating among environments. This consequence arises from conditions likely to be common in nature (phenotypic plasticity and variation in biotic environments). It therefore offers a general answer to how divergent sexual selection may begin.

Cooperative interactions within the family enhance the capacity for evolutionary change in body size

Classical models of evolution seldom predict the rate at which populations evolve in the wild. One explanation is that the social environment affects how traits change in response to natural selection. Here, we determine how social interactions between parents and offspring, and among larvae, influence the response to experimental selection on adult size. Our experiments focus on burying beetles (Nicrophorus vespilloides), whose larvae develop within a carrion nest. Some broods exclusively self-feed on the carrion while others are also fed by their parents. We found populations responded to selection for larger adults but only when parents cared for their offspring. We also found populations responded to selection for smaller adults too, but only by removing parents and causing larval interactions to exert more influence on eventual adult size. Comparative analyses revealed a similar pattern: evolutionary increases in species size within the genus Nicrophorus are associated with the obligate provision of care. Synthesising our results with previous studies, we suggest that cooperative social environments enhance the response to selection whereas excessive conflict can prevent further directional selection.

Female preference functions drive interpopulation divergence in male signalling: call diversity in the bushcricket Ephippiger diurnus

Female preferences play a major role in the elaboration and diversification of male traits: as a selective pressure on males, variation in female preferences can generate population divergence and ultimately, speciation. We studied how interpopulation differences in the shape of female mate preference functions may have shaped male advertisement signals in the bushcricket Ephippiger diurnus. This species is distributed as geographically isolated populations with striking interpopulation variation in male acoustic signals, most notably in the number of syllables per call. Here, we asked whether differences in the shape of preference functions exist among populations and whether those differences may have driven male signal evolution resulting in the observed differences in syllable numbers. Our results reveal fundamental differences in female preferences among populations, with differences in the overall preference function shape corresponding to differences in male signals. These differences in female preferences best explain the major differences in male signals among populations. The interpopulation variation in signals and preferences potentially reflects the evolutionary history of the species and may contribute to further divergence among populations and subsequent speciation.

Genetic Variation in Host Plants Influences the Mate Preferences of a Plant-Feeding Insect

Many species spend their lives in close association with other organisms, and the environments provided by those organisms can play an important role as causes of variation in phenotypes. When this is the case, the genotypes of the individuals constituting the environment may influence the phenotypes of individuals living in that environment. When these effects are between heterospecifics, interspecific indirect genetic effects (IIGEs) occur. Several studies have detected IIGEs, but whether IIGEs contribute to variation in sexually selected traits remains virtually unexplored. We assessed how mate preferences in a plant-feeding insect are influenced by the genotype of their host plant. We established clone lines of a sample of host plant genotypes constituting the background biotic environment for a random sample of insects that we reared on them. We found that the insects’ mate preferences varied according to the clone line on which they developed. These results demonstrate that genetic variation in host plants has cross-trophic consequences on a trait that has strong effects on fitness and interpopulation dynamics such as diversification in communication systems. We discuss how IIGEs on mate preferences may influence the way in which selection acts, including the maintenance of variation and the promotion of evolutionary divergence.

Describing mate preference functions and other function-valued traits

Mate preferences are important causes of sexual selection. They shape the evolution of sexual ornaments and displays, sometimes maintaining genetic diversity and sometimes promoting speciation. Mate preferences can be challenging to study because they are expressed in animal brains and because they are a function of the features of potential mates that are encountered. Describing them requires taking this into account. We present a method for describing and analysing mate preference functions, and introduce a freely available computer program that implements the method. We give an overview of how the program works, and we discuss how it can be used to visualize and quantitatively analyse preference functions. In addition, we provide an informal review of different methods of testing mate preferences, with recommendations for how best to set up experiments on mate preferences. Although the program was written with mate preferences in mind, it can be used to study any function‐valued trait, and we hope researchers will take advantage of it across a broad range of traits.

Vibrational playback by means of airborne stimuli.

SUMMARY Substrate-borne vibrational communication is a common form of communication in animals. Current contact-based playback methods limit the number of substrates that can be stimulated simultaneously and potentially change the transmission properties of the substrate. Here, we explore a solution to these limitations by broadcasting airborne stimuli onto plant substrates to impart vibrational playbacks. We demonstrate that one can effectively compensate for the filtering properties of any individual plant across a range of frequencies. We then address how well both compensated broad-band and pure-tone stimuli for one plant individual apply to other individuals across days. Variation within and between plants was similar across the range tested but was quite variable at certain frequencies. Focusing on a subset of this range, at low frequencies, responses were flat across days and pure-tone frequency stimuli in this range were consistently transmitted despite repositioning of plants relative to the loudspeaker. Our results present a potential solution to researchers interested in exposing large samples of individuals to vibrational signals but also highlight the importance of validating the use of airborne stimuli as vibrational playbacks to the particular substrate type and frequency range of interest.

Adaptive evolution of synchronous egg-hatching in compensation for the loss of parental care

Interactions among siblings are finely balanced between rivalry and cooperation, but the factors that tip the balance towards cooperation are incompletely understood. Previous observations of insect species suggest that (i) sibling cooperation is more likely when siblings hatch at the same time, and (ii) this is more common when parents provide little to no care. In this paper, we tested these ideas experimentally with the burying beetle, Nicrophorus vespilloides. Burying beetles convert the body of a small dead vertebrate into an edible nest for their larvae, and provision and guard their young after hatching. In our first experiment, we simulated synchronous or asynchronous hatching by adding larvae at different intervals to the carrion-breeding resource. We found that ‘synchronously’ hatched broods survived better than ‘asynchronously’ hatched broods, probably because ‘synchronous hatching’ generated larger teams of larvae, that together worked more effectively to penetrate the carrion nest and feed upon it. In our second experiment, we measured the synchronicity of hatching in experimental populations that had evolved for 22 generations without any post-hatching care, and control populations that had evolved in parallel with post-hatching care. We found that larvae were more likely to hatch earlier, and at the same time as their broodmates, in the experimental populations that evolved without post-hatching care. We suggest that synchronous hatching enables offspring to help each other when parents are not present to provide care. However, we also suggest that greater levels of cooperation among siblings cannot compensate fully for the loss of parental care.

A sustained change in the supply of parental care causes adaptive evolution of offspring morphology

Although cooperative social interactions within species are considered an important driver of evolutionary change, few studies have experimentally demonstrated that they cause adaptive evolution. Here we address this problem by studying the burying beetle Nicrophorus vespilloides. In this species, parents and larvae work together to obtain nourishment for larvae from the carrion breeding resource: parents feed larvae and larvae also self-feed. We established experimentally evolving populations in which we varied the assistance that parents provided for their offspring and investigated how offspring evolved in response. We show that in populations where parents predictably supplied more care, larval mandibles evolved to be smaller in relation to larval mass, and larvae were correspondingly less self-sufficient. Previous work has shown that antagonistic social interactions can generate escalating evolutionary arms races. Our study shows that cooperative interactions can yield the opposite evolutionary outcome: when one party invests more, the other evolves to invest less.The amount and predictability of parental care may influence the evolution of offspring traits. Here, the authors experimentally evolve burying beetles at different levels of parental care and find smaller mandibles and lower self-sufficiency in populations with more care.