Developmental temperature alters the thermal sensitivity of courtship activity and signal-preference relationships, but not mating rates.

Mating behaviors are sensitive to novel or stressful thermal conditions, particularly for ectothermic organisms. An organism's sensitivity to temperature, which may manifest in altered mating outcomes, can be shaped in part by temperatures experienced during development. Here, we tested how developmental temperature shapes the expression of adult mating-related behaviors across different ambient conditions, with a focus on courtship behavior, mating rates, and mating signals and preferences. To do so, we reared treehoppers under two temperature regimes and then tested the expression of male and female mating behaviors across a range of ambient temperatures. We found that developmental temperature affects the thermal sensitivity of courtship behavior and mating signals for males. However, developmental temperature did not affect the thermal sensitivity of courtship or mate preferences in females. This sex-specific plasticity did not alter the likelihood of mating across ambient temperatures, but it did disrupt how closely mating signals and preferences matched each other at higher ambient temperatures. As a result, developmental temperature could alter sexual selection through signal-preference de-coupling. We further discuss how adult age may drive sex-specific results, and the potential for mismatches between developmental and mating thermal environments under future climate change predictions.

Evolutionary interactions between thermal ecology and sexual selection.

Thermal ecology and mate competition are both pervasive features of ecological adaptation. A surge of recent work has uncovered the diversity of ways in which temperature affects mating interactions and sexual selection. However, the potential for thermal biology and reproductive ecology to evolve together as organisms adapt to their thermal environment has been underappreciated. Here, we develop a series of hypotheses regarding (1) not only how thermal ecology affects mating system dynamics, but also how mating dynamics can generate selection on thermal traits; and (2) how the thermal consequences of mate competition favour the reciprocal co-adaptation of thermal biology and sexual traits. We discuss our hypotheses in the context of both pre-copulatory and post-copulatory processes. We also call for future work integrating experimental and phylogenetic comparative approaches to understand evolutionary feedbacks between thermal ecology and sexual selection. Overall, studying reciprocal feedbacks between thermal ecology and sexual selection may be necessary to understand how organisms have adapted to the environments of the past and could persist in the environments of the future.

Sex-specific ornament evolution is a consistent feature of climatic adaptation across space and time in dragonflies.

Adaptation to different climates fuels the origins and maintenance of biodiversity. Detailing how organisms optimize fitness for their local climates is therefore an essential goal in biology. Although we increasingly understand how survival-related traits evolve as organisms adapt to climatic conditions, it is unclear whether organisms also optimize traits that coordinate mating between the sexes. Here, we show that dragonflies consistently adapt to warmer climates across space and time by evolving less male melanin ornamentation-a mating-related trait that also absorbs solar radiation and heats individuals above ambient temperatures. Continent-wide macroevolutionary analyses reveal that species inhabiting warmer climates evolve less male ornamentation. Community-science observations across 10 species indicate that populations adapt to warmer parts of species' ranges through microevolution of smaller male ornaments. Observations from 2005 to 2019 detail that contemporary selective pressures oppose male ornaments in warmer years; and our climate-warming projections predict further decreases by 2070. Conversely, our analyses show that female ornamentation responds idiosyncratically to temperature across space and time, indicating the sexes evolve in different ways to meet the demands of the local climate. Overall, these macro- and microevolutionary findings demonstrate that organisms predictably optimize their mating-related traits for the climate just as they do their survival-related traits.

Temperature impacts all behavioral interactions during insect and arachnid reproduction.

Temperature shapes the processes and outcomes of behaviors that occur throughout the progression of insect and arachnid mating interactions and reproduction. Here, we highlight how temperature impacts precopulatory activity levels, competition among rivals, communication with potential mates, and the relative costs and benefits of mating. We review how both the prevailing temperature conditions during reproductive activity and the temperatures experienced early in life influence mating-related behavior. To effectively predict the consequences of global warming for insect and arachnid mating behavior, we advocate for future work that universally integrates a function-valued approach to measuring thermal sensitivity. A function-valued approach will be especially useful for understanding how fine-scale temperature variation shapes current and future selection on mating interactions.

Temperature coupling of mate attraction signals and female mate preferences in four populations of Enchenopa treehopper (Hemiptera: Membracidae).

Variation in temperature can affect the expression of a variety of important fitness-related behaviours, including those involved with mate attraction and selection, with consequences for the coordination of mating across variable environments. We examined how temperature influences the expression of male mating signals and female mate preferences-as well as the relationship between how male signals and female mate preferences change across temperatures (signal-preference temperature coupling)-in Enchenopa binotata treehoppers. These small plant-feeding insects communicate using plantborne vibrations, and our field surveys indicate they experience significant natural variation in temperature during the mating season. We tested for signal-preference temperature coupling in four populations of E. binotata by manipulating temperature in a controlled laboratory environment. We measured the frequency of male signals-the trait for which females show strongest preference-and female peak preference-the signal frequency most preferred by females-across a range of biologically relevant temperatures (18°C-36°C). We found a strong effect of temperature on both male signals and female preferences, which generated signal-preference temperature coupling within each population. Even in a population in which male signals mismatched female preferences, the temperature coupling reinforces predicted directional selection across all temperatures. Additionally, we found similar thermal sensitivity in signals and preferences across populations even though populations varied in the mean frequency of male signals and female peak preference. Together, these results suggest that temperature variation should not affect the action of sexual selection via female choice, but rather should reinforce stabilizing selection in populations with signal-preference matches, and directional selection in those with signal-preference mismatches. Finally, we do not predict that thermal variation will disrupt the coordination of mating in this species by generating signal-preference mismatches at thermal extremes.

Using Variation in Heritability Estimates as a Test of G × E in Behavioral Research: A Brief Research Note.

Better characterization of the sources of phenotypic variation in human behavioural traits-stemming from genetic and environmental influences-will allow for more informed decisions about how to approach a range of challenges arising from variation, ranging from societal issues to the treatment of diseases. In particular, understanding how the environment moderates genetic influence on phenotypes (i.e., genotype-environment interactions, or G × E) is a central component of the behavioral sciences. Yet, understanding of this phenomenon is lagging somewhat, due in part to the difficulties of detecting G × E. We discuss the logic behind one of the primary ways to detect G × E: comparing heritability estimates across environments. Then, we highlight some pitfalls, with an emphasis on how very strong G × E can sometimes be undetectable using this method when high heritability is present in multiple environments. We conclude by forwarding some initial, yet tentative, suggestions for how best to address to the problem.

Variation in Mating Dynamics across Five Species of Leiobunine Harvestmen (Arachnida: Opliones).

The study of mating choices often focuses on correlates of traits to the overall outcome of a mating interaction. However, mating interactions can proceed through a series of stages, with opportunities for assessment at each stage. We compared whether male or female size predicted mating interaction outcome across several stages of mating in five species of North American leiobunine harvestmen (commonly known as daddy longlegs). Leiobunine harvestmen have been previously shown to exhibit incredible morphological diversity consistent with a spectrum of male⁻female antagonism. Across all of the species, we found a general progression of female size predicting the outcome (success and timing) of early stages of interactions, and male size or male size relative to female size predicting the outcome and timing of later stages of interactions. We also found that size was not a strong predictor of outcome in the two species on the lower end of the antagonism spectrum. The variation in how female and male size predicted outcomes across species and stages of mating suggests that multiple mechanisms may operate to shape mating dynamics within and across species. Given the close relatedness of the species studied, the patterns we uncovered suggest a rapid evolution of the traits and processes predicting the outcome of mating interactions.

Female mate choice of male signals is unlikely to promote ecological adaptation in Enchenopa treehoppers (Hemiptera: Membracidae).

A key question in speciation research is how ecological and sexual divergence arise and interact. We tested the hypothesis that mate choice causes local adaptation and ecological divergence using the rationale that the performance~signal trait relationship should parallel the attractiveness~signal trait relationship. We used female fecundity as a measure of ecological performance. We used a species in the Enchenopa binotata treehopper complex, wherein speciation involves adaptation to novel environments and divergence in sexual communication. We used a full-sibling, split-family rearing design to estimate genetic correlations (rG) between fecundity and signal traits, and compared those relationships against population-level mate preferences for the signal traits. Animal model estimates for rG between female fecundity and male signal traits overlapped zero-rejecting the hypothesis-but could reflect sample size limitations. The magnitude of rG correlated with the strength of the mate preferences for the corresponding signal traits, especially for signal frequency, which has the strongest mate preference and the most divergence in the complex. However, signal frequencies favored by the population-level mate preference are not associated with high fecundity. Therefore, mate preferences do not appear to have been selected to favor high-performance genotypes. Our findings suggest that ecological and sexual divergence may arise separately, but reinforce each other, during speciation.

The causes of variation in the presence of genetic covariance between sexual traits and preferences.

Mating traits and mate preferences often show patterns of tight correspondence across populations and species. These patterns of apparent coevolution may result from a genetic association between traits and preferences (i.e. trait-preference genetic covariance). We review the literature on trait-preference covariance to determine its prevalence and potential biological relevance. Of the 43 studies we identified, a surprising 63% detected covariance. We test multiple hypotheses for factors that may influence the likelihood of detecting this covariance. The main predictor was the presence of genetic variation in mate preferences, which is one of the three main conditions required for the establishment of covariance. In fact, 89% of the nine studies where heritability of preference was high detected covariance. Variables pertaining to the experimental methods and type of traits involved in different studies did not greatly influence the detection of trait-preference covariance. Trait-preference genetic covariance appears to be widespread and therefore represents an important and currently underappreciated factor in the coevolution of traits and preferences.

Variation in signal-preference genetic correlations in Enchenopa treehoppers (Hemiptera: Membracidae).

Fisherian selection is a within-population process that promotes signal-preference coevolution and speciation due to signal-preference genetic correlations. The importance of the contribution of Fisherian selection to speciation depends in part on the answer to two outstanding questions: What explains differences in the strength of signal-preference genetic correlations? And, how does the magnitude of within-species signal-preference covariation compare to species differences in signals and preferences? To address these questions, we tested for signal-preference genetic correlations in two members of the Enchenopa binotata complex, a clade of plant-feeding insects wherein speciation involves the colonization of novel host plants and signal-preference divergence. We used a full-sibling, split-family rearing experiment to estimate genetic correlations and to analyze the underlying patterns of variation in signals and preferences. Genetic correlations were weak or zero, but exploration of the underlying patterns of variation in signals and preferences revealed some full-sib families that varied by as much as 50% of the distance between similar species in the E. binotata complex. This result was stronger in the species that showed greater amounts of genetic variation in signals and preferences. We argue that some forms of weak signal-preference genetic correlation may have important evolutionary consequences.

The complexities of female mate choice and male polymorphisms: Elucidating the role of genetics, age, and mate-choice copying.

Genetic, life history, and environmental factors dictate patterns of variation in sexual traits within and across populations, and thus the action and outcome of sexual selection. This study explores patterns of inheritance, diet, age, and mate-choice copying on the expression of male sexual signals and associated female mate choice in a phenotypically diverse group of Schizocosa wolf spiders. Focal spiders exhibit one of two male phenotypes: 'ornamented' males possess large black brushes on their forelegs, and 'non-ornamented' males possess no brushes. Using a quantitative genetics breeding design in a mixed population of ornamented/non-ornamented males, we found a strong genetic basis to male phenotype and female choice. We also found that some ornamented males produced some sons with large brushes and others with barely visible brushes. Results of diet manipulations and behavioral mating trials showed no influence of diet on male phenotype or female mate choice. Age post maturation, however, influenced mate choice, with younger females being more likely to mate with ornamented males. A mate-choice copying experiment found that, following observations of another female's mate choice/copulation, virgin mature females tended to match the mate choice (ornamented vs. non-ornamented males) of the females they observed. Finally, analyses of genetic variation across phenotypically pure (only one male phenotype present) vs. mixed (both phenotypes present) populations revealed genetic distinction between phenotypes in phenotypically-pure populations, but no distinctionin phenotypically-mixed populations. The difference in patterns of genetic differentiation and mating across geographic locations suggests a complex network of factors contributing to the outcome of sexual selection.

Male Enchenopa treehoppers (Hemiptera: Membracidae) vary mate-searching behavior but not signaling behavior in response to spider silk.

Finding and attracting mates can impose costs on males in terms of increased encounters with, and attraction of, predators. To decrease the likelihood of predation, males may modify mate-acquisition efforts in two main ways: they may reduce mate-searching efforts or they may reduce mate-attraction efforts. The specific behavior that males change in the presence of predator cues should depend upon the nature of risk imposed by the type of predator present in the environment. For example, sit-and-wait predators impose greater costs to males moving in search of mates. Here, we test whether cues of the presence of a sit-and-wait predator lead to a reduction in mate-searching but not mate-acquisition behavior. We used a member of the Enchenopa binotata complex of treehoppers-a clade of vibrationally communicating insects in which males fly in search of mates and produce mate-attraction signals when they land on plant stems. We tested for changes in mate-searching and signaling behaviors when silk from a web-building spider was present or absent. We found that males delayed flight when spider silk was present but only if they were actively searching for mates. These results suggest that males have been selected to reduce predation risk by adjusting how they move about their environment according to the cues of sit-and-wait predators.

Experience-mediated plasticity in mate preferences: mating assurance in a variable environment.

An individual's prior experience of sexual signals can result in variation in mate preferences, with important consequences for the course of sexual selection. We test two hypotheses about the evolution of experience-mediated plasticity in mate preferences: mating assurance and mismating avoidance. We exposed female Enchenopa binotata treehoppers (Hemiptera: Membracidae) to treatments that varied their experience of signal frequency, the most divergent sexual signal trait in the E. binotata species complex. Treatments consisted of (1) signals matching the preferred frequency, (2-3) signals deviating either 100 Hz above or 100 Hz below the preferred frequency, and (4) no signals. Females experiencing preferred signals showed the greatest selectivity. However, experience had no effect on peak preference. These results support the hypothesis that selection has favored plasticity in mate preferences that ensures that mating takes place when preferred mates are rare or absent, while ensuring choice of preferred types when those are present. We consider how experience-mediated plasticity may influence selection on sexual advertisement signals, patterns of reproductive isolation, and the maintenance of genetic variation. We suggest that the plasticity we describe may increase the likelihood of successful colonization of a novel environment, where preferred mating types may be rare.