G. Sander van Doorn

Life-history trade-offs favour the evolution of animal personalities

In recent years evidence has been accumulating that personalities are not only found in humans but also in a wide range of other animal species. Individuals differ consistently in their behavioural tendencies and the behaviour in one context is correlated with the behaviour in multiple other contexts. From an adaptive perspective, the evolution of animal personalities is still a mystery, because a more flexible structure of behaviour should provide a selective advantage. Accordingly, many researchers view personalities as resulting from constraints imposed by the architecture of behaviour (but see ref. 12). In contrast, we show here that animal personalities can be given an adaptive explanation. Our argument is based on the insight that the trade-off between current and future reproduction often results in polymorphic populations in which some individuals put more emphasis on future fitness returns than others. Life-history theory predicts that such differences in fitness expectations should result in systematic differences in risk-taking behaviour. Individuals with high future expectations (who have much to lose) should be more risk-averse than individuals with low expectations. This applies to all kinds of risky situations, so individuals should consistently differ in their behaviour. By means of an evolutionary model we demonstrate that this basic principle results in the evolution of animal personalities. It simultaneously explains the coexistence of behavioural types, the consistency of behaviour through time and the structure of behavioural correlations across contexts. Moreover, it explains the common finding that explorative behaviour and risk-related traits like boldness and aggressiveness are common characteristics of animal personalities.

Evolutionary emergence of responsive and unresponsive personalities

In many animal species, individuals differ consistently in suites of correlated behaviors, comparable with human personalities. Increasing evidence suggests that one of the fundamental factors structuring personality differences is the responsiveness of individuals to environmental stimuli. Whereas some individuals tend to be highly responsive to such stimuli, others are unresponsive and show routine-like behaviors. Much research has focused on the proximate causes of these differences but little is known about their evolutionary origin. Here, we provide an evolutionary explanation. We develop a simple but general evolutionary model that is based on two key ingredients. First, the benefits of responsiveness are frequency-dependent; that is, being responsive is advantageous when rare but disadvantageous when common. This explains why responsive and unresponsive individuals can coexist within a population. Second, positive-feedback mechanisms reduce the costs of responsiveness; that is, responsiveness is less costly for individuals that have been responsive before. This explains why individuals differ consistently in their responsiveness, across contexts and over time. As a result, natural selection gives rise to stable individual differences in responsiveness. Whereas some individuals respond to environmental stimuli in all kinds of contexts, others consistently neglect such stimuli. Interestingly, such differences induce correlations among all kinds of other traits (e.g., boldness and aggressiveness), thus providing an explanation for environment-specific behavioral syndromes.

On the Origin of Species by Natural and Sexual Selection

Local Selection of Magic Traits Ecological interactions can favor specialization, and sexual selection can induce reproductive isolation; however, these processes are insufficient by themselves to create new species. They must act in concert and on the same set of genes. Van Doorn et al. (p. 1704, published online 26 November; see the Perspective by Mank) present a theoretical model that shows that within a larger population the evolution of mating preferences will favor sexual ornaments that indicate the degree of adaptation to the local ecological conditions, for example, the abundant song of a male bird that can obtain food easily because it has the right bill size for the seeds in that locale. Once mate choice evolves on the basis of a signal of local adaptation, natural and sexual selection will mutually enforce each other, ultimately leading to speciation. Modeling demonstrates how speciation occurs due to sexual selection. Ecological speciation is considered an adaptive response to selection for local adaptation. However, besides suitable ecological conditions, the process requires assortative mating to protect the nascent species from homogenization by gene flow. By means of a simple model, we demonstrate that disruptive ecological selection favors the evolution of sexual preferences for ornaments that signal local adaptation. Such preferences induce assortative mating with respect to ecological characters and enhance the strength of disruptive selection. Natural and sexual selection thus work in concert to achieve local adaptation and reproductive isolation, even in the presence of substantial gene flow. The resulting speciation process ensues without the divergence of mating preferences, avoiding problems that have plagued previous models of speciation by sexual selection.

Sympatric speciation by sexual selection: A critical reevaluation

Several empirical studies put forward sexual selection as an important driving force of sympatric speciation. This idea agrees with recent models suggesting that speciation may proceed by means of divergent Fisherian runaway processes within a single population. Notwithstanding this, the models so far have not been able to demonstrate that sympatric speciation can unfold as a fully adaptive process driven by sexual selection alone. Implicitly or explicitly, most models rely on nonselective factors to initiate speciation. In fact, they do not provide a selective explanation for the considerable variation in female preferences required to trigger divergent runaway processes. We argue that such variation can arise by disruptive selection but only when selection on female preferences is frequency dependent. Adaptive speciation is therefore unattainable in traditional female choice models, which assume selection on female preferences to be frequency independent. However, when frequency‐dependent sexual selection processes act alongside mate choice, truly adaptive sympatric speciation becomes feasible. Speciation is then initiated independently of nonadaptive processes and does not suffer from the theoretical weaknesses associated with the current Fisherian runaway model of speciation. However, adaptive speciation requires the simultaneous action of multiple mechanisms, and therefore it occurs under conditions far more restrictive than earlier models of sympatric speciation by sexual selection appear to suggest.

Intralocus Sexual Conflict

Intralocus sexual conflict arises when there are sex‐specific optima for a trait that is expressed in both sexes and when the constraint of a shared gene pool prevents males and females from reaching their optima independently. This situation may result in a negative intersexual correlation for fitness. Here I first discuss key differences between intra‐ and interlocus conflict, the type of sexual conflict that arises in mating interactions between males and females. I then review the experimental evidence for the existence of genomewide sexually antagonistic variation and discuss how intralocus conflict can be resolved. Substantial genomewide sexually antagonistic variation exists in Drosophila melanogaster lab populations. Yet, in the same species, sex‐specific gene regulation appears to evolve rapidly, suggesting that the obstacles to the resolution of intralocus conflict are minor. The fact that negative intersexual correlations for fitness are observed even if sexual dimorphism can evolve rapidly suggests that intralocus conflict is highly dynamic. The final part of this review examines the evolutionary consequences of intralocus sexual conflict for the evolution of the sex chromosomes, sexual selection, and sex determination. Intralocus conflict helps to explain many of the peculiar features of the sex chromosomes and has shaped the functional bias and expression biases of sex‐linked genes. The genomic distribution of sexually selected genes, in particular, affects sexual selection in various ways. The presence of sexually antagonistic variation can strongly interfere with the good genes’ process of sexual selection and erode the genetic benefits of mate choice. Regarding sex determination, this review concentrates on evolutionary transitions between different sex determination mechanisms. Such transitions have occurred frequently in several taxa. Theory and empirical data suggest an important role for intralocus conflict in triggering switches between sex determination systems.

On the coevolution of social responsiveness and behavioural consistency

Recent research focuses on animal personalities, that is individual differences in behaviour that are consistent across contexts and over time. From an adaptive perspective, such limited behavioural plasticity is surprising, since a more flexible structure of behaviour should provide a selective advantage. Here, we argue that consistency can be advantageous because it makes individuals predictable. Predictability, however, can only be advantageous if at least some individuals in the population respond to individual differences. Consequently, the evolution of consistency and responsiveness are mutually dependent. We present a general analysis of this coevolutionary feedback for scenarios that can be represented as matrix games with two pure strategies (e.g. hawk-dove game, snowdrift game). We first show that responsive strategies are favoured whenever some individual differences are present in the population (e.g. due to mutation and drift). We then show that the presence of responsive individuals can trigger a coevolutionary process between responsiveness and consistency that gives rise to populations in which responsive individuals coexist with unresponsive individuals who show high levels of adaptive consistency in their behaviour. Next to providing an adaptive explanation for consistency, our results also link two key features associated with personalities, individual differences in responsiveness and behavioural consistency.

Adaptive speciation theory: a conceptual review

Speciation—the origin of new species—is the source of the diversity of life. A theory of speciation is essential to link poorly understood macro-evolutionary processes, such as the origin of biodiversity and adaptive radiation, to well understood micro-evolutionary processes, such as allele frequency change due to natural or sexual selection. An important question is whether, and to what extent, the process of speciation is ‘adaptive’, i.e., driven by natural and/or sexual selection. Here, we discuss two main modelling approaches in adaptive speciation theory. Ecological models of speciation focus on the evolution of ecological differentiation through divergent natural selection. These models can explain the stable coexistence of the resulting daughter species in the face of interspecific competition, but they are often vague about the evolution of reproductive isolation. Most sexual selection models of speciation focus on the diversification of mating strategies through divergent sexual selection. These models can explain the evolution of prezygotic reproductive isolation, but they are typically vague on questions like ecological coexistence. By means of an integrated model, incorporating both ecological interactions and sexual selection, we demonstrate that disruptive selection on both ecological and mating strategies is necessary, but not sufficient, for speciation to occur. To achieve speciation, mating must at least partly reflect ecological characteristics. The interaction of natural and sexual selection is also pivotal in a model where sexual selection facilitates ecological speciation even in the absence of diverging female preferences. In view of these results, it is counterproductive to consider ecological and sexual selection models as contrasting and incompatible views on speciation, one being dominant over the other. Instead, an integrative perspective is needed to achieve a thorough and coherent understanding of adaptive speciation.

Transitions Between Male and Female Heterogamety Caused by Sex-Antagonistic Selection

Many animal taxa show frequent and rapid transitions between male heterogamety (XY) and female heterogamety (ZW). We develop a model showing how these transitions can be driven by sex-antagonistic selection. Sex-antagonistic selection acting on loci linked to a new sex-determination mutation can cause it to invade, but when acting on loci linked to the ancestral sex-determination gene will inhibit an invasion. The strengths of the consequent indirect selection on the old and new sex-determination loci are mediated by the strengths of sex-antagonistic selection, linkage between the sex-antagonistic and sex-determination genes, and the amount of genetic variation. Sex-antagonistic loci that are tightly linked to a sex-determining gene have a vastly stronger influence on the balance of selection than more distant loci. As a result, changes in linkage, caused, for example, by an inversion that captures a sex-determination mutation and a gene under sex-antagonistic selection, can trigger transitions between XY and ZW systems. Sex-antagonistic alleles can become more strongly associated with pleiotropically dominant sex-determining factors, which may help to explain biases in the rates of transitions between male and female heterogamety. Deleterious recessive mutations completely linked to the ancestral Y chromosome can prevent invasion of a neo-W chromosome or result in a stable equilibrium at which XY and ZW systems segregate simultaneously at two linkage groups.

The evolution of female preferences for multiple indicators of quality.

In a variety of species, females exhibit preferences for multiple male ornaments. Several hypotheses have been proposed to explain this phenomenon. Which, if any, of these hypotheses is the most plausible in general remains largely unresolved based on the available empirical data. Yet theoretical studies conclude that the evolution of preferences for multiple signals of male quality is unlikely, especially when the use of an additional cue in mate choice strongly increases the overall cost of choice. This would imply that most male courtship characters do not reflect the male’s genetic quality but instead evolved through Fisherian sexual selection. However, the existing models focus on ornaments that signal overall genetic quality and do not address the possibility that different ornaments provide information about different aspects of quality. Therefore, we develop a model in which the ornaments act as signals for distinct quality components. When the ornaments provide overlapping information about these quality components, we retrieve the results of earlier models. However, when the ornaments provide independent information, preferences for multiple ornaments may evolve, even when exhibiting multiple preferences is costly. We discuss our results in relation to the multiple‐message and redundant‐signal hypotheses for ornament diversity and identify parallels between Fisherian and good‐genes mechanisms for the evolution of multiple ornaments.

The evolution of age-dependent plasticity.

When organisms encounter environments that are heterogeneous in time, phenotypic plasticity is often favored by selection. The degree of such plasticity can vary during an organism’s lifetime, but the factors promoting differential plastic responses at different ages or life stages remain poorly understood. Here we develop and analyze an evolutionary model to investigate how environmental information is optimally collected and translated into phenotypic adjustments at different ages. We demonstrate that plasticity must often be expected to vary with age in a nonmonotonic fashion. Early in life, it is generally optimal to delay phenotypic adjustments until sufficient information has been collected about the state of the environment to warrant a costly phenotypic adjustment. Toward the end of life, phenotypic adjustments are disfavored as well because their beneficial effects can no longer be fully reaped before death. Our analysis clarifies how patterns of age-dependent plasticity are shaped by the interplay of environmental uncertainty, the accuracy of perceived information, and the costs of phenotypic adjustments with life-history determinants such as the relative strengths of fecundity and viability selection experienced by the organism over its lifetime. We conclude by comparing our results with expectations for alternative mechanisms, including developmental constraints, that promote age-dependent plasticity.