Laurel B. Symes

Contributions of natural and sexual selection to the evolution of premating reproductive isolation: a research agenda.

Speciation by divergent natural selection is well supported. However, the role of sexual selection in speciation is less well understood due to disagreement about whether sexual selection is a mechanism of evolution separate from natural selection, as well as confusion about various models and tests of sexual selection. Here, we outline how sexual selection and natural selection are different mechanisms of evolutionary change, and suggest that this distinction is critical when analyzing the role of sexual selection in speciation. Furthermore, we clarify models of sexual selection with respect to their interaction with ecology and natural selection. In doing so, we outline a research agenda for testing hypotheses about the relative significance of divergent sexual and natural selection in the evolution of reproductive isolation.

Diversification under sexual selection: the relative roles of mate preference strength and the degree of divergence in mate preferences

The contribution of sexual selection to diversification remains poorly understood after decades of research. This may be in part because studies have focused predominantly on the strength of sexual selection, which offers an incomplete view of selection regimes. By contrast, students of natural selection focus on environmental differences that help compare selection regimes across populations. To ask how this disparity in focus may affect the conclusions of evolutionary research, we relate the amount of diversification in mating displays to quantitative descriptions of the strength and the amount of divergence in mate preferences across a diverse set of case studies of mate choice. We find that display diversification is better explained by preference divergence rather than preference strength; the effect of the latter is more subtle, and is best revealed as an interaction with the former. Our findings cast the action of sexual selection (and selection in general) in a novel light: the strength of selection influences the rate of evolution, and how divergent selection is determines how much diversification can occur. Adopting this view will enhance tests of the relative role of natural and sexual selection in processes such as speciation.

SPECIES RECOGNITION AND PATTERNS OF POPULATION VARIATION IN THE REPRODUCTIVE STRUCTURES OF A DAMSELFLY GENUS

The selection pressures imposed by mate choice for species identity should impose strong stabilizing selection on traits that confer species identity to mates. Thus, we expect that such traits should show nonoverlapping distributions among closely related species, but show little to no variance among populations within a species. We tested these predictions by comparing levels of population differentiation in the sizes and shapes of male cerci (i.e., the clasper structures used for species identity during mating) of six Enallagma damselfly species. Cerci shapes were nonoverlapping among Enallagma species, and five of six Enallagma species showed no population variation across their entire species ranges. In contrast, cerci sizes overlapped among species and varied substantially among populations within species. These results, taken with previous studies, suggest that cerci shape is a primary feature used in species recognition used to discriminate conspecific from heterospecifics during mating.

The Role of Ecology in Speciation by Sexual Selection: A Systematic Empirical Review

Theoretical and empirical research indicates that sexual selection interacts with the ecological context in which mate choice occurs, suggesting that sexual and natural selection act together during the evolution of premating reproductive isolation. However, the relative importance of natural and sexual selection to speciation remains poorly understood. Here, we applied a recent conceptual framework for examining interactions between mate choice divergence and ecological context to a review of the empirical literature on speciation by sexual selection. This framework defines two types of interactions between mate choice and ecology: internal interactions, wherein natural and sexual selection jointly influence divergence in sexual signal traits and preferences, and external interactions, wherein sexual selection alone acts on traits and preferences but ecological context shapes the transmission efficacy of sexual signals. The objectives of this synthesis were 3-fold: to summarize the traits, ecological factors, taxa, and geographic contexts involved in studies of mate choice divergence; to analyze patterns of association between these variables; and to identify the most common types of interactions between mate choice and ecological factors. Our analysis revealed that certain traits are consistently associated with certain ecological factors. Moreover, among studies that examined a divergent sexually selected trait and an ecological factor, internal interactions were more common than external interactions. Trait–preference associations may thus frequently be subject to both sexual and natural selection in cases of divergent mate choice. Our results highlight the importance of interactions between sexual selection and ecology in mate choice divergence and suggest areas for future research. Subject areas: Reproductive strategies and kinship analysisTheoretical and empirical research indicates that sexual selection interacts with the ecological context in which mate choice occurs, suggesting that sexual and natural selection act together during the evolution of premating reproductive isolation. However, the relative importance of natural and sexual selection to speciation remains poorly understood. Here, we applied a recent conceptual framework for examining interactions between mate choice divergence and ecological context to a review of the empirical literature on speciation by sexual selection. This framework defines two types of interactions between mate choice and ecology: internal interactions, wherein natural and sexual selection jointly influence divergence in sexual signal traits and preferences, and external interactions, wherein sexual selection alone acts on traits and preferences but ecological context shapes the transmission efficacy of sexual signals. The objectives of this synthesis were 3-fold: to summarize the traits, ecological factors, taxa, and geographic contexts involved in studies of mate choice divergence; to analyze patterns of association between these variables; and to identify the most common types of interactions between mate choice and ecological factors. Our analysis revealed that certain traits are consistently associated with certain ecological factors. Moreover, among studies that examined a divergent sexually selected trait and an ecological factor, internal interactions were more common than external interactions. Trait-preference associations may thus frequently be subject to both sexual and natural selection in cases of divergent mate choice. Our results highlight the importance of interactions between sexual selection and ecology in mate choice divergence and suggest areas for future research.

Mechanisms of Assortative Mating in Speciation with Gene Flow: Connecting Theory and Empirical Research

The large body of theory on speciation with gene flow has brought to light fundamental differences in the effects of two types of mating rules on speciation: preference/trait rules, in which divergence in both (female) preferences and (male) mating traits is necessary for assortment, and matching rules, in which individuals mate with like individuals on the basis of the presence of traits or alleles that they have in common. These rules can emerge from a variety of behavioral or other mechanisms in ways that are not always obvious. We discuss the theoretical properties of both types of rules and explain why speciation is generally thought to be more likely under matching rather than preference/trait rules. We furthermore discuss whether specific assortative mating mechanisms fall under a preference/trait or matching rule, present empirical evidence for these mechanisms, and propose empirical tests that could distinguish between them. The synthesis of the theoretical literature on these assortative mating rules with empirical studies of the mechanisms by which they act can provide important insights into the occurrence of speciation with gene flow. Finally, by providing a clear framework we hope to inspire greater alignment in the ways that both theoreticians and empiricists study mating rules and how these rules affect speciation through maintaining or eroding barriers to gene flow among closely related species or populations.

COMMUNITY COMPOSITION AFFECTS THE SHAPE OF MATE RESPONSE FUNCTIONS

The evolution of mate preferences can be critical for the evolution of reproductive isolation and speciation. Heterospecific interference may carry substantial fitness costs and result in preferences where females are most responsive to the mean conspecific trait with low response to traits that differ from this value. However, when male traits are unbounded by heterospecifics, there may not be selection against females that respond to extreme trait values in the unbounded direction. To test how heterospecifics affected the shape of female response functions, I presented female Oecanthus tree crickets with synthetic calls representing a range of male calls, then measured female phonotaxis to construct response functions. The species with the fastest pulse rates in the community consistently responded to pulse rates faster than those produced by their males, whereas in the intermediate and slowest pulse rate species there was no significant difference between the male trait and the female response. This work suggests that species with the most extreme signal in the community respond to a greater range of signals, potentially resulting in a higher probability of hybridization during secondary contact, and revealing interactions between mate recognition and other aspects of sexual selection.

Signal diversification in Oecanthus tree crickets is shaped by energetic, morphometric, and acoustic trade‐offs

Physiology, physics, and ecological interactions can generate trade‐offs within species, but may also shape divergence among species. We tested whether signal divergence in Oecanthus tree crickets is shaped by acoustic, energetic, and behavioral trade‐offs. We found that species with faster pulse rates, produced by opening and closing wings up to twice as many times per second, did not have higher metabolic costs of calling. The relatively constant energetic cost across species is explained by trade‐offs between the duration and repetition rate of acoustic signals—species with fewer stridulatory teeth closed their wings more frequently such that the number of teeth struck per second of calling and the resulting duty cycle were relatively constant across species. Further trade‐offs were evident in relationships between signals and body size. Calling was relatively inexpensive for small males, permitting them to call for much of the night, but at low amplitude. Large males produced much louder calls, reaching up to four times more area, but the energetic costs increased substantially with increasing size and the time spent calling dropped to only 20% of the night. These trade‐offs indicate that the trait combinations that arise in these species represent a limited subset of conceivable trait combinations.

Beyond temperature coupling: Effects of temperature on ectotherm signaling and mate choice and the implications for communication in multispecies assemblages

Abstract Many organisms share communication channels, generating complex signaling environments that increase the risk of signal interference. Variation in abiotic conditions, such as temperature, may further exacerbate signal interference, particularly in ectotherms. We tested the effects of temperature on the pulse rate of male signals in a community of Oecanthus tree crickets, and for one focal species we also assessed its effect on female pulse rate preferences and motivation to seek mates. We confirm prior findings of temperature‐dependent signals that result in increasing signal similarity at lower temperatures. Temperature also affected several aspects of female preferences: The preferred pulse rate value was temperature dependent, and nearly perfectly coupled with signal pulse rate; the range of pulse rate values that females found attractive also increased with temperature. By contrast, the motivation of females to perform phonotaxis was unaffected by temperature. Thus, at lower temperatures the signals of closely related species were more similar and females more discriminating. However, because signal similarity increased more strongly than female discrimination, signal interference and the likelihood of mismating may increase as temperatures drop. We suggest that a community approach will be useful for understanding the role of environmental variability in the evolution of communication systems.

Theory Meets Empiry: A Citation Network Analysis

According to a recent survey, ecologists and evolutionary biologists feel that theoretical and empirical research should coexist in a tight feedback loop but believe that the two domains actually interact very little. We evaluate this perception using a citation network analysis for two data sets, representing the literature on sexual selection and speciation. Overall, 54%-60% of citations come from a papers own category, whereas 17%-23% are citations across categories. These cross-citations tend to focus on highly cited papers, and we observe a positive correlation between the numbers of citations a study receives within and across categories. We find evidence that reviews can function as integrators between the two literatures, argue that theoretical models are analogous to specific empirical study systems, and complement our analyses by studying a cocitation network. We conclude that theoretical and empirical research are more tightly connected than generally thought but that avenues exist to further increase this integration.

Spatial and temporal variation in three call traits and preferences of the tree cricket Oecanthus forbesi

Multiple selective forces act on the evolution of mating preferences. While mating preferences are central to pre-zygotic isolation, certain preferences and traits may make greater contributions. For some traits, females may exhibit preferences, but accept heterospecifics trait values when preferred values are scarce. For other traits, females may fail to reproduce before accepting heterospecifics trait values. Understanding patterns of variation and divergence in this later class of traits is particularly relevant to understanding divergence and speciation. Here, I focus on three call traits of Forbes’ Tree Cricket (Oecanthus forbesi) to quantify their capacity to produce reproductive isolation and to compare patterns of variation and divergence in these traits. By generating female preference functions and measuring male call parameters, I test two hypotheses: (1) traits and preferences vary in their capacity to contribute to reproductive isolation and (2) traits that are important to reproductive isolation have lower intrapopulation, interpopulation, and interannual variation and weaker correlation with male body size. I find that female response to one trait (pulse rate) decreased sharply when trait values fell within the heterospecific range. This trait had low variation and no correlation with male morphology. For two other traits (pulse duration and dominant frequency), females responded to many values, including values characteristics of co-occurring heterospecifics. Trait variation was higher and pulse duration correlated with male leg length. These results indicate that the evolutionary dynamics of a low-variation trait (pulse rate) may be more important to speciation than changes in more conspicuously variable sexually selected traits.Significance statementAnimals often attract and assess mates using complex signals. This paper tests whether some signal components contribute more to preventing mating between species. The data show that changes in a single trait [pulse rate of cricket calls] can eliminate female response to males, while other traits [dominant frequency (pitch) and pulse duration] can be changed to match the values produced by other species without reducing female response. Consequently, some traits may diverge without contributing to reproductive isolation between species. The paper then tests for correlations between trait function and patterns of trait variation within and between populations and species. Pulse rate has low variation within and between populations, but differs substantially between species. Dominant frequency and pulse rate are more variable within and between populations. Pulse duration also correlates with male body size, indicating that pulse duration could reflect male condition even if it is relatively unimportant for reproductive isolation.