Wiebke Schuett

Sexual selection and animal personality

Consistent individual behavioural tendencies, termed “personalities”, have been identified in a wide range of animals. Functional explanations for personality have been proposed, but as yet, very little consideration has been given to a possible role for sexual selection in maintaining differences in personality and its stability within individuals. We provide an overview of the available literature on the role of personality traits in intrasexual competition and mate choice in both human and non‐human animals and integrate this into a framework for considering how sexual selection can generate and maintain personality. For this, we consider the evolution and maintenance of both main aspects of animal personality: inter‐individual variation and intra‐individual consistency.

Sex differences, social context and personality in zebra finches, Taeniopygia guttata

Despite burgeoning interest in consistent individual differences in behaviour (animal ‘personality’), the influence of social interactions on the performance of different behavioural types is poorly understood. Similarly, the ecological and evolutionary consequences of personality differences in social contexts remain unexplored. Moreover, the possibility that the sexes differ in the degree to which they exhibit personality in both social and nonsocial contexts has not yet received serious attention, despite the sexes usually being subject to differing selection pressures. Using a highly gregarious species, the zebra finch, we tested for consistent behavioural differences (in exploration) between individuals of both sexes in both nonsocial and social contexts, the latter considering the behavioural influence of opposite-sex companions. We then investigated how exploratory tendencies relate to behaviour in a potentially risky foraging context in mixed-sex dyads of individuals with differing personalities. Males were not more exploratory on average but were more consistent in their exploratory tendencies than females. Additionally, males behaved more consistently across the social and asocial contexts than females, even though individuals of both sexes similarly influenced each others exploratory behaviour within the social context: the more exploratory the companion, the more exploratory the focal individual (relative to its level of exploration in the asocial context). An individuals exploration also affected its performance in the social foraging context. Our results stress the importance of looking for sex differences in personality and of considering the influence of social context in animal personality studies. We discuss our findings and their implications in the light of the biology of the species and set them in a broader ecological and evolutionary context.

Pairs of zebra finches with similar 'personalities' make better parents

Although behavioural plasticity should be an advantage in a varying world, there is increasing evidence for widespread stable individual differences in the behaviour of animals: that is, ‘personality’. Here we provide evidence suggesting that sexual selection is an important factor in the evolution of personality in species with biparental care. We carried out a cross-fostering breeding experiment on zebra finches, Taeniopygia guttata, and found that parental personality traits and the combination of personalities within breeding pairs had positive effects on correlates of (foster) offspring fitness (body mass and condition). Furthermore, these nongenetic parental effects were pervasive and carried over into the next generation. Our results suggest that similarity in behavioural traits of biparental species can have important, long-lasting effects on reproductive success, probably because of reduced sexual conflict over the provision of parental investment.

Studying personality variation in invertebrates: why bother?

Research on animal personality variation has been burgeoning in the last 20 years but surprisingly few studies have investigated personalities in invertebrate species although they make up 98% of all animal species. Such lack of invertebrate studies might be due to a traditional belief that invertebrates are just ‘minirobots’. Lately, studies highlighting personality differences in a range of invertebrate species have challenged this idea. However, the number of invertebrate species investigated still contrasts markedly with the effort that has been made studying vertebrates, which represent only a single subphylum. We describe how investigating proximate, evolutionary and ecological correlates of personality variation in invertebrates may broaden our understanding of personality variation in general. In our opinion, personality studies on invertebrates are much needed, because invertebrates exhibit a range of aspects in their life histories, social and sexual behaviours that are extremely rare or absent in most studied vertebrates, but that offer new avenues for personality research. Examples are complete metamorphosis, male emasculation during copulation, asexual reproduction, eusociality and parasitism. Further invertebrate personality studies could enable a comparative approach to unravel how past selective forces have driven the evolution of personality differences. Finally, we point out the advantages of studying personality variation in many invertebrate species, such as easier access to relevant data on proximate and ultimate factors, arising from easy maintenance, fast life cycles and short generation times.

Personality variation in a clonal insect: The pea aphid, Acyrthosiphon pisum

Individuals are often consistent in their behavior but vary from each other in the level of behavior shown. Despite burgeoning interest in such animal personality variation, studies on invertebrates are scarce, and studies on clonal invertebrates nonexistent. This is surprising given the obvious advantages of using invertebrates/clones to tackle the crucial question why such consistent behavioral differences exist. Here we show that individuals of clonal pea aphids exhibit consistent behavioral differences in their escape responses to a predator attack (dropping vs. nondropping off a plant). However, behavior was not repeatable at the clonal level. Genetically identical clones expressed various phenotypes but different clones produced different proportions of each phenotype (dropper, nondropper, and inconsistent). Manipulations of early environmental conditions had little qualitative impact on such patterns. We discuss the importance of our findings for future studies of the evolutionary and ecological consequences of personality variation.

Environmental transmission of a personality trait: foster parent exploration behaviour predicts offspring exploration behaviour in zebra finches

Consistent behavioural differences among individuals are common in many species and can have important effects on offspring fitness. To understand such ‘personality’ variation, it is important to determine the mode of inheritance, but this has been quantified for only a few species. Here, we report results from a breeding experiment in captive zebra finches, Taeniopygia guttata, in which we cross-fostered offspring to disentangle the importance of genetic and non-genetic transmission of behaviour. Genetic and foster-parents’ exploratory type was measured in a novel environment pre-breeding and offspring exploratory type was assessed at adulthood. Offspring exploratory type was predicted by the exploratory behaviour of the foster but not the genetic parents, whereas offspring size was predicted by genetic but not foster-parents’ size. Other aspects of the social environment, such as rearing regime (uni- versus biparental), hatching position, brood size or an individuals sex did not influence offspring exploration. Our results therefore indicate that non-genetic transmission of behaviour can play an important role in shaping animal personality variation.

Evolution of sex-specific pace-of-life syndromes: causes and consequences

Males and females commonly differ in their life history optima and, consequently, in the optimal expression of life history, behavioral and physiological traits involved in pace-of-life syndromes (POLS). Sex differences in mean trait expression typically result if males and females exhibit different fitness optima along the same pace-of-life continuum, but the syndrome structure may also differ for the sexes. Due to sex-specific selective pressures imposed by reproductive roles and breeding strategies, the sexes may come to differ in the strength of correlation among traits, or different traits may covary in males and females. Ignorance of these selective forces operating between and within the sexes may lead to flawed conclusions about POLS manifestation in the species, and stand in the way of understanding the evolution, maintenance, and variability of POLS. We outline ways in which natural and sexual selection influence sex-specific trait evolution, and describe potential ultimate mechanisms underlying sex-specific POLS. We make predictions on how reproductive roles and the underlying sexual conflict lead to sex-specific trait covariances. These predictions lead us to conclude that sexual dimorphism in POLS is expected to be highly prevalent, allow us to assess possible consequences for POLS evolution, and provide guidelines for future studies.

Early environmental conditions shape personality types in a jumping spider

Individuals of many species across the animal kingdom are found to be less plastic than expected, even in behavioral traits. The existence of consistent behavioral differences between individuals, termed personality differences, is puzzling, since plastic behavior is considered ideal to enable animals to adaptively respond to changes in environmental conditions. In order to elucidate which mechanisms are important for the evolution of personality differences, it is crucial to understand which aspects of the environment are important for the development of personality differences. Here, we tested whether physical or social aspects of the environment during development influence individual differentiation (mean level of behavior) using the jumping spider Marpissa muscosa. Furthermore, we assessed whether those behaviors were repeatable, i.e. whether personalities existed. We applied a split-brood design and raised spider siblings in three different environments: a deprived environment with no enrichment, a socially and a physically enriched environment. We focused on exploratory behavior and repeatedly assessed individual behavior in a novel environment and a novel object test. Results show that the environment during development influenced spiders’ exploratory tendencies: spiders raised in enriched environments tended to be more exploratory. Most investigated behaviors were repeatable (i.e. personalities existed) across all individuals tested, whereas only few behaviors were also repeatable across individuals that had experienced the same environmental condition. Taken together, our results indicate that external stimuli can influence the development of one aspect of personality, the inter-individual variation (mean level of behavior), in a jumping spider. We also found family by environment interactions on behavioral traits potentially suggesting genetic variation in developmental plasticity.

Foster, but not genetic, father plumage coloration has a temperature-dependent effect on offspring quality

Secondary sexual characters have most likely evolved through sexual selection because such traits indicate the genetic or phenotypic quality of the bearer. While genetic variation in such fitness-related traits should be depleted by directional selection, there are many cases in which variation is higher than expected. One hypothesis explaining this variation is that different phenotypes within a population are adapted to different environmental conditions. We tested this hypothesis by comparing the offspring quality of male pied flycatchers, Ficedula hypoleuca, with different degrees of melanin-based dorsal plumage coloration under different environmental conditions. To create different environmental growth conditions and to be able to separate offspring genotype effects from paternal effects on offspring body mass, we used a partial cross-foster design where the brood size was reduced or enlarged by one chick. We also examined the interactive effects of temperature and male phenotype because previous correlative studies suggest such temperature-dependent effects in this species. We show that, while manipulated brood size did not interact with male phenotype to affect offspring quality, temperature during the nestling period influenced the offspring quality of dark and brown foster (but not genetic) fathers. When the temperature was relatively low during the nestling period, foster offspring of black males were lighter than those raised by brown males; the opposite was true if temperature was relatively high. These results add a new aspect to our understanding of how variation in the degree of melanin-based coloration is maintained in wild populations and how phenotypic variation may be maintained in general.

Evolution of sex-specific pace-of-life syndromes: genetic architecture and physiological mechanisms

Sex differences in life history, physiology, and behavior are nearly ubiquitous across taxa, owing to sex-specific selection that arises from different reproductive strategies of the sexes. The pace-of-life syndrome (POLS) hypothesis predicts that most variation in such traits among individuals, populations, and species falls along a slow-fast pace-of-life continuum. As a result of their different reproductive roles and environment, the sexes also commonly differ in pace-of-life, with important consequences for the evolution of POLS. Here, we outline mechanisms for how males and females can evolve differences in POLS traits and in how such traits can covary differently despite constraints resulting from a shared genome. We review the current knowledge of the genetic basis of POLS traits and suggest candidate genes and pathways for future studies. Pleiotropic effects may govern many of the genetic correlations, but little is still known about the mechanisms involved in trade-offs between current and future reproduction and their integration with behavioral variation. We highlight the importance of metabolic and hormonal pathways in mediating sex differences in POLS traits; however, there is still a shortage of studies that test for sex specificity in molecular effects and their evolutionary causes. Considering whether and how sexual dimorphism evolves in POLS traits provides a more holistic framework to understand how behavioral variation is integrated with life histories and physiology, and we call for studies that focus on examining the sex-specific genetic architecture of this integration.