Christine W. Miller

Sexual Selection in Complex Environments

Sexual selection has resulted in some of the most captivating features of insects, including flashy colors, bizarre structures, and complex pheromones. These features evolve in dynamic environments, where conditions can change rapidly over space and time. However, only recently has ecological complexity been embraced by theory and practice in sexual selection. We review replicated selection studies as well as studies on variation in the agents of selection to delineate gaps in current knowledge and clarify exciting new directions for research. Existing work suggests that fluctuations in sexual selection may be extremely common, though work on the ecological factors influencing these fluctuations is scarce. We suggest that deeper ecological perspectives on sexual selection may alter some of the fundamental assumptions of sexual selection theory and rapidly lead to new discoveries.

A potential resolution to the lek paradox through indirect genetic effects

Females often prefer males with elaborate traits, even when they receive no direct benefits from their choice. In such situations, mate discrimination presumably has genetic advantages; selective females will produce offspring of higher genetic quality. Over time, persistent female preferences for elaborate secondary-sexual traits in males should erode genetic variance in these traits, eventually eliminating any benefit to the preferences. Yet, strong female preferences persist in many taxa. This puzzle is called the lek paradox and raises two primary questions: do females obtain genetic benefits for offspring by selecting males with elaborate secondary-sexual characteristics and, if so, how is the genetic variation in these male traits maintained? We suggest that indirect genetic effects may help to resolve the lek paradox. Maternal phenotypes, such as habitat selection behaviours and offspring provisioning, often influence the condition and the expression of secondary-sexual traits in sons. These maternal influences are commonly genetic based (i.e. they are indirect genetic effects). Females choosing mates with elaborate traits may receive ‘good genes’ for daughters in the form of effective maternal characteristics. Recognizing the significance of indirect genetic effects may be important to our understanding of the process and consequences of sexual selection.

Why Sexually Selected Weapons Are Not Ornaments

The elaboration and diversification of sexually selected weapons remain poorly understood. We argue that progress in this topic has been hindered by a strong bias in sexual selection research, and a tendency for weapons to be conflated with ornaments used in mate choice. Here, we outline how male-male competition and female choice are distinct mechanisms of sexual selection, and why weapons and ornaments are fundamentally different types of traits. We call for research on the factors contributing to weapon divergence, the potential for male-male competition to drive speciation, and the specific use of weapons in the context of direct fights versus displays. Given that weapons are first and foremost fighting structures, biomechanical approaches are an especially promising direction for understanding weapon design.

The form of sexual selection arising from male–male competition depends on the presence of females in the social environment

Sexual selection arises from social interactions, and if social environments vary so too should sexual selection. For example, male–male competition often occurs either in the presence or in the absence of females, and such changes in the social environment could affect the form and strength of sexual selection. Here we examine how the presence of a female influences selection arising from male–male competition in a leaf‐footed cactus bug, Narnia femorata, which has a resource defence mating system. Males compete for territories on cacti because females lay eggs on the cactus plants. Females are not always present when this competition first occurs; however, the presence or absence of the female matters. We found that both the form and strength of selection on male traits, those traits that influenced success in intrasexual competition, depended on the social context. When a female was not present, male size and the area of the sexually dimorphic hind legs was only marginally important to winning a contest. However, males with larger overall size and leg area were more likely to win in the presence of a female. There was also positive quadratic selection on these traits when a female was present with both the largest and the smallest males winning. The implication is unexpected alternative strategies when females are present. Our results support the notion that sexual selection should be studied under all relevant social contexts.

Sexual selection is influenced by both developmental and adult environments

Sexual selection is often assumed to be strong and consistent, yet increasing research shows it can fluctuate over space and time. Few experimental studies have examined changes in sexual selection in response to natural environmental variation. Here, we use a difference in resource quality to test for the influence of past environmental conditions and current environmental conditions on male and female mate choice and resulting selection gradients for leaf‐footed cactus bugs, Narnia femorata. We raised juveniles on natural high‐ and low‐quality diets, cactus pads with and without ripe cactus fruits. New adults were again assigned a cactus pad with or without fruit, paired with a potential mate, and observed for mating behaviors. We found developmental and adult encounter environments affected mating decisions and the resulting patterns of sexual selection for both males and females. Males were not choosy in the low‐quality encounter environment, cactus without fruit, but they avoided mating with small females in the high‐quality encounter environment. Females were choosy in both encounter environments, avoiding mating with small males. However, they were the choosiest when they were in the low‐quality encounter environment. Female mate choice was also context dependent by male developmental environment. Females were more likely to mate with males that had developed on cactus with fruit when they were currently in the cactus with fruit environment. This pattern disappeared when females were in the cactus without fruit environment. Altogether, these results experimentally demonstrate context‐dependent mate choice by both males and females. Furthermore, we demonstrate that simple, seasonal changes in resources can lead to fluctuations in sexual selection.

The type and timing of social information alters offspring production

The acquisition and use of information are essential for decision-making in an uncertain world. The use of social information, or information from the behaviour of others, may be a common and efficient mechanism to improve estimates of resource quality by animals. According to theory, social information cues with higher information content should have a greater influence on decision-making, and current information should be weighed more than prior information. However, experimental tests of these hypotheses remain scarce. We exposed female cactus bugs (Chelinidea vittiger) to different types of social information (the presence of conspecific eggs or nymphs) presented at different times (current or prior to egg laying) to determine the influence of social information on offspring production. We found that social information substantially altered the number of eggs produced. The presence of conspecific eggs, regardless of timing, consistently increased egg production, whereas nymphs only increased egg production when present during egg laying. We conclude that the type and timing of social information may have an important, yet unappreciated, influence on reproductive allocation.

On the evolution of hidden leks and the implications for reproductive and habitat selection behaviours

Habitat selection affects many aspects of individual fitness, which can have strong consequences for lifehistory strategies, species interactions, population dynamics and evolutionary trajectories (e.g. Danchin & Wagner 1997; Morris 2003). A potentially important link among habitat selection, sexual selection and mating systems was recently illustrated with the description of hidden leks by Wagner (1998). Hidden leks evolve in territorial species when female receptivity to extrapair copulations (EPCs) outside the social pair bond results in aggregations of territorial males (Wagner 1998). By drawing analogy from lekking behaviour in promiscuous species, Wagner provided novel insight into habitat selection behaviour. This hypothesis sheds new light on the evolution of conspecific attraction used in habitat selection (Stamps 1988), which has been documented experimentally in many taxa (e.g. Stamps 1988; Muller 1998; Ward & Schlossberg 2004). Conspecific attraction challenges assumptions of both habitat selection theory and metapopulation theory (Stamps 1988; Ray et al. 1991), but why attraction evolves remains largely unknown. The hidden lek hypothesis could help to explain attraction; however, robust criteria for detecting hidden leks and specific predictions of how hidden leks influence habitat selection behaviours have been obscure (Wagner 1998; Tarof et al. 2005). Here, we seek to refine and clarify predictions made from the

Conspecific and Heterospecific Cues Override Resource Quality to Influence Offspring Production

Animals live in an uncertain world. To reduce uncertainty, animals use cues that can encode diverse information regarding habitat quality, including both non-social and social cues. While it is increasingly appreciated that the sources of potential information are vast, our understanding of how individuals integrate different types of cues to guide decision-making remains limited. We experimentally manipulated both resource quality (presence/absence of cactus fruit) and social cues (conspecific juveniles, heterospecific juveniles, no juveniles) for a cactus-feeding insect, Narnia femorata (Hemiptera: Coreidae), to ask how individuals responded to resource quality in the presence or absence of social cues. Cactus with fruit is a high-quality environment for juvenile development, and indeed we found that females laid 56% more eggs when cactus fruit was present versus when it was absent. However, when conspecific or heterospecific juveniles were present, the effects of resource quality on egg numbers vanished. Overall, N . femorata laid approximately twice as many eggs in the presence of heterospecifics than alone or in the presence of conspecifics. Our results suggest that the presence of both conspecific and heterospecific social cues can disrupt responses of individuals to environmental gradients in resource quality.

Dynamic effects of oviposition site on offspring sexually-selected traits and scaling relationships

The expression of sexually-selected traits such as bright plumage, exaggerated antlers, and elongated eyestalks can be highly influenced by environmental factors, including the behaviors of mothers. Many recent studies have described the ways that maternal behavior can influence the expression of sexually-selected traits in offspring, however, few studies have investigated if and how such maternal effects might change, over time, in natural populations. Here, we examine the influence of maternal oviposition site on the expression of offspring sexually-selected traits in four successive cohorts of the heliconia bug, Leptoscelis tricolor (Hemiptera: Coreidae). Female heliconia bugs lay eggs on multiple host plant species, and offspring remain on these plants for the entirety of growth and development. We found that natal plant species had significant effects on the expression of male sexually-selected traits and the degree of sexual dimorphism. Moreover, these effects changed over time for later cohorts, concurrent with changes in host plant resources. Our results suggest that maternal effects can be a significant and dynamic influence on the sexually-selected traits of offspring. Such environmental effects on sexually-selected traits could have broad implications for the processes and outcomes of sexual selection.

The tale of the shrinking weapon: seasonal changes in nutrition affect weapon size and sexual dimorphism, but not contemporary evolution

Sexually selected traits are often highly variable in size within populations due to their close link with the physical condition of individuals. Nutrition has a large impact on physical condition, and thus, any seasonal changes in nutritional quality are predicted to alter the average size of sexually selected traits as well as the degree of sexual dimorphism in populations. However, although traits affected by mate choice are well studied, we have a surprising lack of knowledge of how natural variation in nutrition affects the expression of sexually selected weapons and sexual dimorphism. Further, few studies explicitly test for differences in the heritability and mean‐scaled evolvability of sexually selected traits across conditions. We studied Narnia femorata (Hemiptera: Coreidae), an insect where males use their hind legs as weapons and the femurs are enlarged, to understand the extent to which weapon expression, sexual dimorphism and evolvability change across the actual range of nutrition available in the wild. We found that insects raised on a poor diet (cactus without fruit) are nearly monomorphic, whereas those raised on a high‐quality diet (cactus with ripe fruit) are distinctly sexually dimorphic via the expression of large hind leg weapons in males. Contrary to our expectations, we found little evidence of a potential for evolutionary change for any trait measured. Thus, although we show weapons are highly condition dependent, and changes in weapon expression and dimorphism could alter evolutionary dynamics, our populations are unlikely to experience further evolutionary changes under current conditions.