Ulrika Candolin

The use of multiple cues in mate choice

An increasing number of studies find females to base their mate choice on several cues. Why this occurs is debated and many different hypotheses have been proposed. Here I review the hypotheses and the evidence in favour of them. At the same time I provide a new categorisation based on the adaptiveness of the preferences and the information content of the cues. A few comparative and empirical studies suggest that most multiple cues are Fisherian attractiveness cues or uninformative cues that occur alongside a viability indicator and facilitate detection, improve signal reception, or are remnants from past selection pressures. However, much evidence exists for multiple cues providing additional information and serving as multiple messages that either indicate general mate quality or enable females that differ in mate preferences to choose the most suitable male. Less evidence exists for multiple cues serving as back‐up signals. The importance of receiver psychology, multiple sensory environments and signal interaction in the evolution of multiple cues and preferences has received surprisingly little attention but may be of crucial importance. Similarly, sexual conflict has been proposed to result in maladaptive preferences for manipulative cues, and in neutral preferences for threshold cues, but no reliable evidence exists so far. An important factor in the evolution of multiple preferences is the cost of using additional cues. Most theoretical work assumes that the cost of choice increases with the number of cues used, which restricts the conditions under which preferences for multiple cues are expected to evolve. I suggest that in contrast to this expectation, the use of multiple cues can reduce mate choice costs by decreasing the number of mates inspected more closely or the time and energy spent inspecting a set of mates. This may be one explanation for why multiple cues are more common than usually expected. Finally I discuss the consequences that the use of multiple cues may have for the process of sexual selection, the maintenance of genetic variation, and speciation.

How is female mate choice affected by male competition

The plethora of studies devoted to the topics of male competition and female mate choice belie the fact that their interaction remains poorly understood. Indeed, on the question of whether competition should help or hinder the choice process, opinions scattered throughout the sexual selection literature seem unnecessarily polarised. We argue, in the light of recent theoretical and empirical advances, that the effect of competition on mate choice depends on whether it results in the choosy sex attaining high breeding value for total fitness, considering both direct and indirect fitness benefits. Specifically, trade‐offs may occur between different fitness benefits if some are correlated with male competitive ability whilst others are not. Moreover, the costs and benefits of mating with competitive males may vary in time and/or space. These considerations highlight the importance of injecting a life‐history perspective into sexual selection studies. Within this context, we turn to the sexual selection literature to try to offer insights into the circumstances when competition might be expected to have positive or negative implications for pre‐copulatory female choice. In this regard, we elaborate on three stages where competition might impact upon the choice process: (i) during mate detection, (ii) mate evaluation, and (iii) in dictating actual mating outcomes. We conclude by offering researchers several potentially rewarding avenues for future research.

Behavioural responses to human-induced environmental change

The initial response of individuals to human‐induced environmental change is often behavioural. This can improve the performance of individuals under sudden, large‐scale perturbations and maintain viable populations. The response can also give additional time for genetic changes to arise and, hence, facilitate adaptation to new conditions. On the other hand, maladaptive responses, which reduce individual fitness, may occur when individuals encounter conditions that the population has not experienced during its evolutionary history, which can decrease population viability. A growing number of studies find human disturbances to induce behavioural responses, both directly and by altering factors that influence fitness. Common causes of behavioural responses are changes in the transmission of information, the concentration of endocrine disrupters, the availability of resources, the possibility of dispersal, and the abundance of interacting species. Frequent responses are alterations in habitat choice, movements, foraging, social behaviour and reproductive behaviour. Behavioural responses depend on the genetically determined reaction norm of the individuals, which evolves over generations. Populations first respond with individual behavioural plasticity, whereafter changes may arise through innovations and the social transmission of behavioural patterns within and across generations, and, finally, by evolution of the behavioural response over generations. Only a restricted number of species show behavioural adaptations that make them thrive in severely disturbed environments. Hence, rapid human‐induced disturbances often decrease the diversity of native species, while facilitating the spread of invasive species with highly plastic behaviours. Consequently, behavioural responses to human‐induced environmental change can have profound effects on the distribution, adaptation, speciation and extinction of populations and, hence, on biodiversity. A better understanding of the mechanisms of behavioural responses and their causes and consequences could improve our ability to predict the effects of human‐induced environmental change on individual species and on biodiversity.

Changed environmental conditions weaken sexual selection in sticklebacks

Environmental heterogeneity can cause the intensity and direction of selection to vary in time and space. Yet, the effects of human‐induced environmental changes on sexual selection and the expression of mating traits of native species are poorly known. Currently, the breeding habitats of the three‐spined sticklebackGasterosteus aculeatus are changing in the Baltic Sea because of eutrophication and increased growth of algae. Here we show that enhanced growth of filamentous algae increases the costs of mating by inducing an increase in the time and energy spent on courtship and mate choice. This is not followed by a concomitant increase in mate attraction, but instead the strength of selection on male red nuptial coloration and courtship activity is relaxed. Thus, the high investment into the costly sexually selected traits is maladaptive under the new conditions, and the mating system mediates a negative effect of the environmental change on the population. We attribute these environmentally induced changes in the benefit of the mating traits and in the strength of sexual selection to reduced visibility in dense vegetation. Anthropogenic disturbances hence affect the selection pressures that mould the species, which could have long‐term effects on the viability and evolution of the populations.

Is sexual selection beneficial during adaptation to environmental change

The role of sexual selection in adaptation is disputed. A balance between sexual and viability selection can be achieved in stable environments, but environmental perturbations could change the costs and benefits arising from sexual selection and influence the rate of adaptation. Here we synthesise theoretical and empirical work on the role of sexual selection in adaptation to changed conditions. Contrasting results have been gained, but the majority of studies suggest that sexual selection has no significant effect or a negative effect on the rate of adaptation. However, once sexually selected traits start to evolve, sexual selection can accelerate adaptation. The role of sexual selection in extinction appears to be minor, but the results could be skewed.

Environmental deterioration compromises socially enforced signals of male quality in three-spined sticklebacks.

Social costs are often important in promoting the honesty of sexually selected traits. What happens, then, when social costs are relaxed? In species that breed in shallow coastal waters, increases in the frequency and severity of phytoplankton blooms may undermine the value of visual signals by reducing visibility and, in so doing, lead to dishonest signaling by relaxing the social consequences of high signaling effort for poor‐quality individuals. Here, we experimentally test the effects of algally induced water turbidity on the role of male‐male competition in facilitating reliable sexual displays in three‐spined sticklebacks. We found that males in poor condition reduced their courtship effort in the presence of competition in turbid water. This reduction, however, was to a much lesser extent than that observed in clear water. Thus, courtship under conditions of algal turbidity did not reflect male condition as honestly as courtship in clear water. Algal turbidity also influenced breeding coloration, with males in poor condition reducing their area of red nuptial coloration in turbid conditions. Our findings suggest that anthropogenic disturbance to the signaling environment can potentially reduce the evolutionary potential of sexual selection by diminishing the efficacy of visual displays and weakening socially enforced signals of male quality.

Communication in troubled waters: responses of fish communication systems to changing environments

Fish populations are increasingly being subjected to anthropogenic changes to their sensory environments. The impact of these changes on inter- and intra-specific communication, and its evolutionary consequences, has only recently started to receive research attention. A disruption of the sensory environment is likely to impact communication, especially with respect to reproductive interactions that help to maintain species boundaries. Aquatic ecosystems around the world are being threatened by a variety of environmental stressors, causing dramatic losses of biodiversity and bringing urgency to the need to understand how fish respond to rapid environmental changes. Here, we discuss current research on different communication systems (visual, chemical, acoustic, electric) and explore the state of our knowledge of how complex systems respond to environmental stressors using fish as a model. By far the bulk of our understanding comes from research on visual communication in the context of mate selection and competition for mates, while work on other communication systems is accumulating. In particular, it is increasingly acknowledged that environmental effects on one mode of communication may trigger compensation through other modalities. The strength and direction of selection on communication traits may vary if such compensation occurs. However, we find a dearth of studies that have taken a multimodal approach to investigating the evolutionary impact of environmental change on communication in fish. Future research should focus on the interaction between different modes of communication, especially under changing environmental conditions. Further, we see an urgent need for a better understanding of the evolutionary consequences of changes in communication systems on fish diversity.

Predator-induced nest site preference: safe nests allow courtship in sticklebacks

Reproductive activities often increase the susceptibility of individuals to predators. Individuals may be able to reduce this risk of predation, however, by their choice of breeding habitat, as the structural complexity of habitats is known to affect predator foraging success. Here we show that the presence of predators induces a preference for structurally complex nest sites over open ones in male three-spined sticklebacks, Gasterosteus aculeatus. To investigate whether this predator-induced nest site preference can decrease the known negative effect of predators on courtship activity, we recorded the reduction in courtship activity during predator presentations for males in vegetated and open nest sites. Habitat structure affected the response to a predator when males were in competition. A male in a vegetated site reduced courtship activity less than a male in an open site. Habitat had no effect on courtship when males were solitary, however. This suggests that male-male competition and the possibility of losing mating opportunities to other males affect risk taking. Females, who were unaware of the predator, preferred the male in the vegetated site, which showed less reduction in courtship, when the males were exposed to a predator, but chose randomly between the males when the predator was absent. Thus, a preference for vegetated nest sites under predation risk may be beneficial not only by increasing the probability of survival, but also by reducing the negative impact of predators on courtship activity and mating probability. Copyright 1998 The Association for the Study of Animal Behaviour.

OPPOSING SELECTION ON A SEXUALLY DIMORPHIC TRAIT THROUGH FEMALE CHOICE AND MALE COMPETITION IN A WATER BOATMAN

Abstract Female choice and male‐male competition are traditionally considered to act in concert, with male competition facilitating female choice. This situation would enforce the strength of directional selection, which could reduce genetic variation and thus the benefits of choice. Here I show that in a water boatman, Sigara falleni, the direction of selection through female choice and male competition vary among traits under laboratory conditions. The two forces were mutually enforcive in acting on body size but exerted opposing selection on a sexually selected trait, male foreleg pala size. Female choice favored large palae, whereas male competition favored smaller palae, suggesting that large palae are costly in competition. This conflicting selection through female choice and male competition could be one of the forces that contribute to the maintenance of genetic variation in sexually selected traits.

Does Competition Allow Male Mate Choosiness in Threespine Sticklebacks

The theory of mate choice posits that intensified competition for mates can generate variation in either the strength or the direction of mate preferences within the competing sex. Here, we show that intensified male competition, manipulated through the operational sex ratio, induced differential mate choosiness among threespine stickleback males Gasterosteus aculeatus. In the absence of male competition, males were choosy independent of their condition when presented sequentially with a large and a small female. However, in a male‐biased social setting, males in poor condition became indiscriminate, whereas good‐condition males continued to be selective. Hence, competition induced condition‐dependent mate choosiness. This was probably due to mating opportunities decreasing more for poor‐condition than for good‐condition males when competition intensified, resulting in condition‐dependent cost of choice. Variation in condition and cost of choice could thus allow the persistence of male mate choosiness in populations experiencing intense male competition.