COGNITIVE PERFORMANCE AND THE EVOLUTION OF MULTIPLE BEHAVIORAL DISPLAY TRAITS

Males of many species have complex behavioral sexual displays and it is possible that these displays indicate aspects about male quality because of their relationship with cognitive ability. However, the relationship between behavioral display traits, cognitive ability, and reproductive success has received little attention. Satin bowerbirds, Ptilonorhynchus violaceus, are an excellent species for studying this relationship because their complex male courtship suggests a selective advantage to individuals with superior cognitive abilities. Here I show that cognitive performance can have important effects on mating success and the quality of behavioral displays. First, I present males with two novel problem solving tests and find that males who are better at solving these problems have higher mating success, establishing a link between male cognitive ability and sexual attractiveness. Second, I add four additional cognitive tests to expand the diversity of cognitive abilities tested and construct two measures of general cognitive ability using these data: the scores from an analysis that best explains covariation among performance on the different cognitive tests (g), and the average rank score on these cognitive tests ("IQ"). I show that these measures of general cognitive ability, as well as the majority of the independent cognitive tests, are positively associated with mating success. Third, I construct a different composite measure of male cognitive ability using an analysis that determines the combination of cognitive traits that make males most successful in attracting females (f). I show that this measure is significantly associated with my measures of general cognitive ability, suggesting that evolution of cognitive ability in bowerbirds is possible if there is sufficient heritability. I construct three different aggregate measures of male display quality (produced from four behavioral display traits) and find that they are all associated with f and with mating success. Finally, I show some support for the hypothesis that separate display traits may indicate different aspects of male cognitive ability. These results suggest that behavioral display traits may have a special role in sexual selection because of their connection to cognitive ability. Overall, this research highlights the importance of considering the interrelationship between cognitive ability and sexual selection

The effect of relatedness on mating behavior in the satin bowerbird (Ptilonorhynchus violaceus)

Behavior is a main component of sexual selection theory in which male competition and female mate choice influence the evolution of a species. Relatedness commonly affects behavioral interactions, but the potential for relatedness to influence sexual selection is often overlooked. Here I show that relatedness affects mating behaviors in satin bowerbirds. Bowerbirds are a model species for non-resource based mating systems in which males provide only sperm to females, and females are free to mate with their preferred males, typically resulting in high skews in male mating success. Males build stick structures (bowers) on the ground to attract, and copulate with, females. Males compete, in part, by destroying neighboring males' bowers. Females search among multiple adjacent bowers and then select subsets of these males for courtship and then copulation. Automated video monitoring of bowers allows identification of males that destroy bowers and females that visit bowers for courtship or copulation. Using microsatellite genetic markers to estimate relatedness, I show that paternity assignments based on observed copulations match the genetic sires of offspring, supporting the hypotheses that copulations occur only at bowers and that male reproductive success can be reliably estimated from observed copulations. Next, I report that competing males are less aggressive, in the form of bower destructions, towards relatives than non-relatives and that this restraining effect of relatedness on aggression favors the close spatial association of relatives' bowers. These results support the hypothesis that relatedness affects male competition and ability to maintain attractive displays for females. Lastly, I investigate the influence of relatedness on female mate choice. I show that females do not actively prefer or avoid relatives in mate choice. However, females bias the areas in which they search for mates to be inclusive of relatives and then mate randomly with respect to relatedness within their search areas, resulting in tendencies to mate with relatives in some years. This effect of relatedness on female mate searching may be due in part to the spatial association of related males, and highlights the influence of mate searching rather than active mate preferences on overall mate choice patterns

Why Can't all Males be Attractive? Inter-individual Variation in Male Spotted Bowerbird Display

One of the greatest conundrums facing evolutionary biologists is how variation between individuals is maintained in situations where there is expected to be strong directional selection on an elaborate male trait. Sexual selection via female choice leads to the evolution of elaborate male traits, and consensus among females in their mate choice decisions can result in high reproductive skew. Such strong directional selection pressure may be expected to reduce genetic variation over time, yet high levels of inter-individual variation sustain such preferences. In this thesis I explored potential mechanisms that may maintain variation between individuals in one of the most unusual and exaggerated avian male traits; the bowers displayed by male spotted bowerbirds, Ptilonorhynchus maculatus. Choosy females exert strong selection pressure on males, yet males vary widely in their ability to exhibit a high quality display. My results showed that male bower owners were remarkably consistent in their display of decorations, a trait expected to experience a high level of fluctuation due to variation in the ecological and social environment. Given the range of factors that may introduce inconsistency, my results suggest that males actively maintain consistent displays, although I found no evidence for the adaptive benefits of doing so. I then explored three mechanisms that may be expected to maintain variation in bowerbird display. I found that attending the bower imposed physical costs on males, but these costs were only apparent in seasons of environmental stress. Males varied in their cognitive and problem-solving abilities, but I found no impact of higher cognitive performance on a male’s reproductive fitness. The final mechanism I tested was the impact of the social environment on male mating success. I found that males actively engage in marauding, a form of intrasexual competition targeting the bowers of rival males. Marauding was highly targeted and non-random within the population, and predominantly occurred between neighbouring bower owners. However, I was unable to determine what factors predicted these non-random interactions, and found no impact of the marauding rates experienced on male mating success. In the final part of this study, I looked at the novel occurrence of collaborative display between male bower owners and other non-bower-owning males. I found that these auxiliary males may gain delayed benefits from attending the bowers of experienced males, but was unable to determine what impact contributions from auxiliaries had on bower owning males and females attempting to assess them. I conclude by discussing the implications of my results for models of sexual selection

Great bowerbirds create theaters with forced perspective when seen by their audience

Birds in the infraorder Corvida [1] (ravens, jays, bowerbirds) are renowned for their cognitive abilities [2–4], which include advanced problem solving with spatial inference [4–8], tool use and complex constructions [7–10], and bowerbird cognitive ability is associated with mating success [11]. Great bowerbird males construct bowers with a long avenue from within which females view the male displaying over his bower court [10]. This predictable audience viewpoint is a prerequisite for forced (altered) visual perspective [12–14]. Males make courts with gray and white objects that increase in size with distance from the avenue entrance. This gradient creates forced visual perspective for the audience; court object visual angles subtended on the female viewer’s eye are more uniform than if the objects were placed at random. Forced perspective can yield false perception of size and distance [12, 15]. After experimental reversal of their size-distance gradient, males recovered their gradients within 3 days, and there was little difference from the original after 2 wks. Variation among males in their forced-perspective quality as seen by their female audience indicates that visual perspective is available for use in mate choice, perhaps as an indicator of cognitive ability. Regardless of function, the creation and maintenance of forced visual perspective is clearly important to great bowerbirds and suggests the possibility of a previously unknown dimension of bird cognition

Ownership conflicts and their resolution

Game theory has been used to investigate a wide range of evolutionary questions, and has been important in explaining apparently selfish patterns in animal behaviour, and behaviours that do not appear to benefit the individual. The modelling chapters in this thesis develop new game theory approaches to modelling animal conflict, investigating the acquisition of territories and the trade-offs that occur between behaviours. Many game theory models of conflicts between individuals make predictions regarding the duration of fights in relation to asymmetries in resource holding potential (RHP). Duration is often interpreted as a result of mutual assessment of RHP, allowing the weaker individual to avoid costly interactions. However, the duration of a contest may also be the result of each individual persisting to a threshold determined by its own RHP, in fiddler crabs, Uca mjoebergi, I show that duration of contests increases with increasing size of the loser, and decreases, but to a lesser extent, with increasing size of the winter, suggesting that neither the mutual assessment or individual threshold hypothesis can explain fight duration in this species. Instead, individual cost thresholds may determine duration, but larger opponents may inflict costs more rapidly, consistent with the cumulative assessment game of animal conflict. In animal contests, the larger opponent is often victorious, but contests are often initiated by individuals that have little chance of winning (generally smaller individuals). A number of hypotheses may explain this behaviour, including a lack of alternative options (the ‘desperado effect’). Recent work has suggested that likely losers attack first due to an error in perception: they mistakenly perceive their chances of winning as being greater than they are. Using a game theoretical model, I show that if smaller individuals can accurately assess their chance of winning, if this chance is relatively high, and if they have few alternative options, they are predicted to be as aggressive as their larger opponents. In addition, when resources are abundant, and small individuals have some change of winning, they may be more aggressive than their larger opponents. Using a game theory model, I show that avoidance of a single fight location can be adaptive if the benefits of access to the area are low compared to the costs of fighting. Low fight costs and high population densities lead to the break down of territoriality and the formation of large, overlapping home ranges

Toward wild psychometrics: Linking individual cognitive differences to fitness

Journal ArticleCopyright © The Author 2014. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology.Our understanding of the processes underlying animal cognition has improved dramatically in recent years, but we still know little about how cognitive traits evolve. Following Darwinian logic, to understand how selection acts on such traits we must determine whether they vary between individuals, influence fitness, and are heritable. A handful of recent studies have begun to explore the relationship between variation in individual cognitive performance and fitness under natural conditions. Such work holds great promise, but its success is contingent on accurate characterization and quantification of the cognitive differences between individuals. Existing research has typically adopted a "problem-solving" approach, assuming that individuals that complete novel tasks have greater cognitive prowess than those that do not. We argue that this approach is incapable of determining that individual differences are due to cognitive factors. We propose the adoption of psychologically grounded psychometric testing and discuss the criteria necessary to examine the fitness consequences of cognitive variation in the wild.BBSRCUniversity of Exete

The Role of Cognition in Sexual Signals and Mate Choice Decisions

Cognitive ability varies dramatically among individuals, yet the manner in which this variation affects reproduction has rarely been investigated. Here, we asked 1) whether male sexual signals reflect cognitive ability and whether females prefer males with superior cognitive abilities, and 2) whether female cognition affects male and female mating decisions? We addressed these questions in a mutual mate choice system, threespine sticklebacks (Gasterosteus aculeatus). We tested cognitive performance by presenting the males and females with a novel task (a barrier to food) to evaluate problem-solving abilities and learning. We found that males that problem solve have elaborate sexual signals and are preferred by females. However, contrary to our expectations, female cognitive abilities did not influence male courtship vigor or their own mating decisions. In dynamic environments, such as the rivers where these fish live, problem-solving ability is a neurological attribute that may preferred by females because it is important in the contexts of male foraging or parental care. Additionally, we argue that males and females experience different selection pressures for cognitive abilities, and therefore express different preferences for cognition in their mates. Our research adds to the expanding body of literature linking cognition and sexual selection, demonstrates that cognitive ability may play an important role in a diverse array of mating systems, and explains how cognition may assist in the maintenance of variation sexual signals within natural populations

L’influence des capacités cognitives mâles et femelles sur le choix de partenaire chez le diamant mandarin (Taeniopygia guttata)

S’approvisionner en nourriture est essentiel à la survie et au succès reproducteur. Lorsque les animaux font face à des changements environnementaux brutaux, ils doivent s’ajuster rapidement à leur nouvel environnement et parfois même innover dans leur façon de s’approvisionner. Des processus comportementaux et cognitifs, tels que l’innovation et l’apprentissage, permettent aux animaux d'intégrer de nouveaux comportements à leur répertoire comportemental afin de s'adapter de façon optimale. Les performances cognitives varient entre les individus d’une même population et bien que des études récentes se soient intéressées aux causes de ce phénomène, de convaincantes évidences sont manquantes afin d’expliquer pourquoi ces variations sont maintenues. Au cours de ce mémoire, les questions des pressions de sélection s'exerçant sur les performances d’alimentation par une tâche motrice nouvelle sont abordées afin de mieux comprendre l'évolution des capacités cognitives au sein d'une population captive de diamants mandarins (Taeniopygia guttata). Nous avons tout d'abord testé si les femelles diamants mandarins modifient leurs préférences d'accouplement après avoir observé la performance d'alimentation par une tâche motrice nouvelle des mâles. Afin de déterminer si les femelles sont capables de discriminer entre les mâles sur la base de leur capacité cognitive, nous avons également évalué les performances d’apprentissage de chacune d’elles. En effet, des études ont suggéré qu’il peut être coûteux, spécialement en terme de temps, de discriminer entre des partenaires potentiels sur cette base. La généralisation d’une préférence pour un mâle performant à d’autres mâles possédant le même phénotype permettrait la réduction de ces coûts. Nous avons donc finalement testé si les femelles diamants mandarins peuvent généraliser leur préférence après avoir observé les performances d’alimentation pour une tâche motrice nouvelle d’un mâle. Nos résultats suggèrent que les femelles diamants mandarins ne peuvent évaluer les capacités cognitives d’un mâle par l’intermédiaire de traits indicateurs. Toutefois, nous avons démontré qu’une observation directe des performances d’alimentation d’un mâle guide le choix d’appariement des femelles. Également, nous avons montré que les femelles peuvent généraliser l’apparence du mâle le plus performant et utiliser cette information lors de l’évaluation de nouveaux mâles. La relation entre les performances cognitives et le choix de partenaire pourraient s’expliquer par exemple par une meilleure exploitation de l’habitat, mais nécessite des études plus approfondies.Successful foraging is essential for survival and reproductive success. When animals face rapidly change due to climate change or anthropogenic habitat destruction, they are force to quickly adjust their behaviour such as foraging. Innovation and learning, two processes related to cognitive functions, are know to allow animals to incorporate novel behaviours into their behavioural repertoires and thus to facilitate optimal responses to environmental change. Cognitive performance vary between and within individuals and although several studies have rencently addressed the causes, convicing evidences for why inter-individual variations in cognitive performance are maintained in a population are still lacking. During my Masters, I investigated different selective pressures acting on foraging performance on a novel motor task to better understand the evolution of cognitive abilities in a captive population of zebra finch (Taeniopygia guttata). Firstly, we investigated whether female zebra finches modify their mating preferences after having observed the foraging performance of males on a novel motor task. We also assessed each bird’s learning performance in a color associative task in order to check whether females could discriminate between the two males based on their learning performance. Discriminating among mates based on their cognitive ability might be very costly for females, especially in terms of time. Therefore, one way to reduce the cost of assessing mate would be to generalize their preferences to any male with the same phenotype as the most efficient observed individual. We finaly investigated whether female zebra finches can generalize their mating preferences after having observed a male’s foraging performance on a novel motor task. Our findings suggest that female zebra finches would be unable to assess male cognitive ability indirectly via morphological traits. However our results demonstrate that direct observation of the males’ performance on a foraging task can guide female mating preferences. We also demonstrates that female zebra finches can generalize the appearance of the male that is the most efficient at solving a motor task and then use this information to assessing new males. The relationship between cognitive performance and mating preference might be mediated throught habitat exploitation for example, but requires further investigation

Cognitive ability is heritable and predicts the success of an alternative mating tactic

The research was funded through the Czech Science Foundation 457 (P505/12/G112).The ability to attract mates, acquire resources for reproduction, and successfully outcompete rivals for fertilisations may make demands on cognitive traits - the mechanisms by which an animal acquires, processes, stores, and acts upon information from its environment. Consequently, cognitive traits potentially undergo sexual selection in some mating systems. We investigated the role of cognitive traits on the reproductive performance of male rose bitterling (Rhodeus ocellatus), a freshwater fish with a complex mating system and alternative mating tactics. We quantified the learning accuracy of males and females in a spatial learning task and scored them for learning accuracy. Males were subsequently allowed to play the roles of a guarder and a sneaker in competitive mating trials, with reproductive success measured using paternity analysis. We detected a significant interaction between male mating role and learning accuracy on reproductive success, with the best performing males in maze trials showing greater reproductive success in a sneaker role than as a guarder. Using a cross-classified breeding design, learning accuracy was demonstrated to be heritable, with significant additive maternal and paternal effects. Our results imply that male cognitive traits may undergo intra-sexual selection.PostprintPeer reviewe