Kasey D. Fowler-Finn

EXPERIENCE-MEDIATED PLASTICITY IN MATE PREFERENCES: MATING ASSURANCE IN A VARIABLE ENVIRONMENT

An individuals 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.

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.

The evolution of experience‐mediated plasticity in mate preferences

Experience of sexual signals can alter mate preferences and influence the course of sexual selection. Here, we examine the patterns of experience‐mediated plasticity in mate preferences that can arise in response to variation in the composition of mates in the environment. We use these patterns to test hypotheses about potential sources of selection favouring experience‐mediated plasticity. We manipulated signal experience of female Enchenopa treehoppers (Hemiptera: Membracidae) in a vibrational playback experiment with the following treatments: silence; two types of non‐preferred signals; preferred signals; and a mixture of preferred and non‐preferred signals. This experiment revealed plasticity in mate preference selectivity, with greatest selectivity in the mixed signal treatment, followed by the preferred signal treatment. We found no plasticity in peak preference. These results suggest that females have been selected to adjust preference selectivity according to the variability of potential mates in their social environment, as well as to the presence/absence of preferred mates. We discuss how experience‐mediated plasticity in mate preferences can influence the strength of selection on male signals and can result in evolutionary dynamics between variation in preferences and signals that either promote the maintenance of variation or facilitate rapid trait fixation.

Curves as traits: genetic and environmental variation in mate preference functions

Study of the genetic and developmental architecture of mate preferences lags behind the study of sexual ornaments. This is in part because of the challenges involved in describing mate preferences, which are expressed as a function of variation in ornaments. We used the function‐valued approach to test for genetic and environmental components of variation in female mate preferences in Enchenopa treehoppers (Hemiptera: Membracidae). These insects communicate with plant‐borne vibrational signals, and offer a case study of speciation involving sexual selection and environmental change. We focused on female preferences for male signal frequency, the most divergent signal trait in Enchenopa. Obtaining complete, individual‐level descriptions of mate preferences in a full‐sib, split‐family rearing experiment, we document substantial genetic variation in mate preference functions. Focusing on traits describing variation in the shape of the preference functions, we further document considerable broad‐sense heritability and evidence of weak genotype × environment interaction in most traits. Against the background of recent and rapid divergence in Enchenopa, these results indicate potent mechanisms that maintain variation and sustain the involvement of mate preferences in sexual selection.

AN EXAMINATION OF AGONISTIC INTERACTIONS IN THE WHIP SPIDER PHRYNUS MARGINEMACULATUS (ARACHNIDA, AMBLYPYGI)

Abstract Intraspecific interactions in adult whip spiders (Phrynus marginemaculatus) were investigated in a laboratory setting to quantify agonistic interactions and to determine predictors of contest outcome. Males were initially paired with size-symmetric or size-asymmetric opponents to assess the effect of size symmetry on contests. Three weeks later, the same males were paired with either the same opponent, or a different opponent to determine whether or not individuals remember earlier encounters. Finally, we quantified aspects of female-female contests. Agonistic encounters between males are characterized by varying degrees of pedipalpal opening, elevation displays, and rapid flicking (∼ 29 Hz) of the antenniform leg. Duration of elevation displays was a predictor of contest outcome, with individuals being more likely to win if they held an elevated posture for longer than their opponent during the contest. Relative size influenced both contest duration and weight loss, with contests between size-symmetric males lasting longer and resulting in greater weight loss than size-asymmetric contests. In second contests, familiar encounters were both shorter in duration and involved fewer aggressive displays than unfamiliar second contests, suggesting that males were able to remember previous opponents. Females were less likely to exhibit aggressive displays than males, and female contests were shorter in duration than male contests. Overall, the results of our study suggest that agonistic interactions in P. marginemaculatus are extremely complex, varying with the sex and size-symmetry of individuals and involving elaborate signaling, and that there may be a large role for learning and memory.

Repeatability of mate preference functions in Enchenopa treehoppers (Hemiptera: Membracidae)

Patterns of variation in mate preferences provide information about the processes influencing the evolution of mate choice behaviour. We measured variation in female mate preferences using preference functions, which are curves that describe female responses across variation in male signals. Over 3 weeks of testing, we repeatedly measured female Enchenopa binotata ‘Ptelea’ treehoppers (Hemiptera: Membracidae) for their preference for male signal frequency (Hz). We then calculated the consistency of differences in mate preference functions among females (i.e. repeatability) and variability across females for the preference functions. We then measured traits describing different aspects of variation in mate preferences, including peak preference and selectivity. We found repeatability in the overall preference functions, indicating a potential for preference functions to respond to selection. Furthermore, we found substantial repeatability and variability in selectivity traits and low repeatability and variability in peak preference. Finally, we found only weak covariation between peak preference and selectivity. We discuss the implications of our results within the framework of the evolution of mate preferences, both in terms of past selection shaping mate preferences, and the potential for preferences to respond to current selection.

Mating in the harvestman Leiobunum vittatum (Arachnida: Opiliones): from premating struggles to solicitous tactile engagement

When mating interactions are influenced by multiple sources of selection, they may involve multiple stages of mate assessment. At each stage, a different set of morphological and behavioural traits may be important in determining the outcome of the interaction. Here, we test the potential for multiple sources of selection to shape mating interactions in Leiobunum vittatum harvestmen, commonly known as ‘daddy longlegs’. We provide a qualitative and quantitative study of mating interactions, and investigate the influence of multiple morphological traits on each of several distinct stages of their mating interactions. Mating interactions start with a struggle between males and females during which the male attempts to secure the females in a mating embrace. Success at this stage depends on the length of the male’s clasping pedipalps: those with shorter pedipalps (and thus greater mechanical advantage) were more successful. Male size relative to the female determines how quickly males achieve this embrace. Mating interactions then proceed to tactile exchanges between males and females, indicating the potential for mutual mate choice and/or peri- and post-copulatory selection. We found no morphological predictors of the timing of these later stages of the mating interactions, and suggest that the exchange of a nuptial gift is important for the dynamics of these stages. Overall, our results highlight L. vittatum as a potentially highly informative group for studying how traits involved in mating are shaped by the interaction of selection across multiple stages in mating interactions.

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.

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.

Local population density and group composition influence the signal‐preference relationship in Enchenopa treehoppers (Hemiptera: Membracidae)

Many animals exhibit social plasticity – changes in phenotype or behaviour in response to experience with conspecifics that change how evolutionary processes like sexual selection play out. Here, we asked whether social plasticity arising from variation in local population density in male advertisement signals and female mate preferences influences the form of sexual selection. We manipulated local density and determined whether this changed how the distribution of male signals overlapped with female preferences – the signal preference relationship. We specifically look at the shape of female mate preference functions, which, when compared to signal distributions, provide hypotheses about the form of sexual selection. We used Enchenopa binotata treehoppers, a group of plant‐feeding insects that exhibit natural variation in local densities across individual host plants, populations, species and years. We measured male signal frequency and female preference functions across the density treatments. We found that male signals varied across local social groups, but not according to local density. By contrast, female preferences varied with local density – favouring higher signal frequencies in denser environments. Thus, local density changes the signal–preference relationship and, consequently, the expected form of sexual selection. We found no influence of sex ratio on the signal–preference relationship. Our findings suggest that plasticity arising from variation in local group density and composition can alter the form of sexual selection with potentially important consequences both for the maintenance of variation and for speciation.