Behaviors can facilitate colonization of a novel environment, but the mechanisms underlying this process are poorly understood. On one hand, behavioral flexibility allows for an immediate response of colonizers to novel environments, which is critical to population establishment and persistence. On the other hand, integrated sets of behaviors that display limited flexibility can enhance invasion success by coupling behaviors with dispersal strategies that are especially important during natural range expansions. Direct observations of colonization events are required to determine the mechanisms underlying changes in behavior associated with colonization, but such observations are rare. Here, we studied changes in aggression on a large temporal and spatial scale across populations of two sister taxa of bluebirds (Sialia) to show that coupling of aggression and dispersal strongly facilitated the range expansion of western bluebirds across the northwestern United States over the last 30 years. We show that biased dispersal of highly aggressive males to the invasion front allowed western bluebirds to displace less aggressive mountain bluebirds. However, once mountain bluebirds were excluded, aggression of western bluebirds decreased rapidly across consecutive generations in concordance with local selection on highly heritable aggressive behavior. Further, the observed adaptive microevolution of aggression was accelerated by the link between dispersal propensity and aggression. Importantly, our results show that behavioral changes among populations were not caused by behavioral flexibility and instead strongly implicate adaptive integration of dispersal and aggression in facilitating the ongoing and rapid reciprocal range change of these species in North America.
Abstract:
Elaboration of costly sexual traits can reduce investment in other aspects of reproduction, such as parental care or intrasexual competition, which may lead to the evolution of alternative mating tactics. In house finches (Carpodacus mexicanus), less elaborately ornamented (dull) males tend to dominate more elaborated (redder) males, but redder males pair earlier and invest more in parental care. This suggests that males may pursue alternative parental or competitive tactics, depending on the elaboration of their sexual trait. Elevation of testosterone, a hormone that is closely associated with condition in male house finches, influences dominance and sexual behaviors but is antagonistic to parental behaviors. We tested the hypothesis that the higher dominance status of dull males reflects an alternative testosterone-dependent mating tactic. First, we experimentally manipulated the testosterone levels of captive males and measured the effect on dominance rank, and second, we measured the association of testosterone elevation and plumage hue in free-living males. We found that, as predicted, testosterone elevation increased dominance rank in captive males. However, in free-living males, testosterone levels were higher in redder males, suggesting that testosterone is dissociated from dominance status under natural circumstances. This may be because the context of social interactions and the higher motivation of dull males to access food resources have a stronger influence on the outcome of dominance interactions than does the physiological effects of testosterone elevation. In turn, the strong positive correlation between testosterone levels and plumage elaboration likely reflects the common condition dependence of these traits.
1. Behaviour is often assumed to be the most flexible of traits, yet recent studies show a high repeatability of behaviour within individuals even across different functional contexts. Such consistent expression of behaviour may evolve either when selection favours its integration with less flexible components of the phenotype or when pleiotropic effects produce correlations between behaviours that have different optimal timing of expression. Examining the physiological mechanisms underlying correlated expression of behaviours provides powerful insight into the evolution of personalities by establishing the extent to which pleiotropic effects might limit the independent evolution of distinct behaviours. 2. Here, we investigated proximate mechanisms behind aggressive and non-aggressive personality types in western bluebirds, Sialia mexicana, to determine whether consistency in the expression of aggression is because of shared effects of plasma-circulating androgens on aggression and mating behaviour. 3. We found that androgen concentration was unrelated to variation in both intra- and interspecific aggression even though it was closely linked to variation in male mating behaviour. These results suggest that pleiotropic effects of circulating androgens are unlikely to cause consistent differences among individuals in aggression. 4. These findings suggest that decoupling of the activational effects of hormones on behaviour is an important step in the evolution of personality traits.
