Renée A. Duckworth

Coupling of dispersal and aggression facilitates the rapid range expansion of a passerine bird

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.

The role of behavior in evolution: a search for mechanism

Behavior has been viewed as a pacemaker of evolutionary change because changes in behavior are thought to expose organisms to novel selection pressures and result in rapid evolution of morphological, life history and physiological traits. However, the idea that behavior primarily drives evolutionary change has been challenged by an alternative view of behavior as an inhibitor of evolution. According to this view, a high level of behavioral plasticity shields organisms from strong directional selection by allowing individuals to exploit new resources or move to a less stressful environment. Here, I suggest that absence of clear mechanisms underlying these hypotheses impedes empirical evaluation of behavior’s role in evolution in two ways. First, both hypotheses focus on behavioral shifts as a key step in the evolutionary process but ignore the developmental mechanisms underlying these shifts and this has fostered unwarranted assumptions about the specific types of behavioral shifts that are important for evolutionary change. Second, neither hypothesis provides a means of connecting within-individual changes in behavior to population-level processes that lead to evolutionary diversification or stasis. To resolve these issues, I incorporate developmental and evolutionary mechanisms into a conceptual framework that generates predictions about the types of behavior and types of behavioral shifts that should affect both micro and macroevolutionary processes.

A condition dependent link between testosterone and disease resistance in the house finch

Testosterone has recently been proposed as a link between male quality and health and the expression of sexual traits. We investigated the relationship between testosterone and measures of the individual condition and health of males in a natural population of house finches (Carpodacus mexicanus). We also conducted a captive experiment in order to test for the effects of testosterone on resistance to coccidia, which is a common parasite of house finches. Free-living males in better condition had higher testosterone levels and lower corticosterone levels than free-living males in poor condition. In our captive experiment, increased testosterone accelerated the rate of coccidial infection as compared with sham-implanted or gonadectomized males. Although the differences were not significant, free-living males infected with coccidia had lower levels of testosterone and higher levels of corticosterone than males that were not infected. Thus, experimentally elevating testosterone levels in captive males resulted in a higher percentage of infected males, while free-living males with coccidial infection had low testosterone levels. This apparent discrepancy between captive and free-living males in the association of testosterone and disease may be explained by the condition dependence of testosterone. These results suggest that the testosteronedependent sexual traits reliably indicate male overall condition and health and, thus, females could benefit from assessing potential mates based on these traits.

Context‐dependent sexual advertisement: plasticity in development of sexual ornamentation throughout the lifetime of a passerine bird

Abstract Male investment into sexual ornamentation is a reproductive decision that depends on the context of breeding and life history state. In turn, selection for state‐ and context‐specific expression of sexual ornamentation should favour the evolution of developmental pathways that enable the flexible allocation of resources into sexual ornamentation. We studied lifelong variation in the expression and condition‐dependence of a sexual ornament in relation to age and the context of breeding in male house finches (Carpodacus mexicanus) – a species that develops a new sexual ornament once a year after breeding. Throughout males’ lifetime, the elaboration of ornamentation and the allocation of resources to the development of sexual ornamentation depended strongly on pairing status in the preceding breeding season – males that were single invested more resources into sexual ornamentation and changed ornamentation more than males that were paired. During the initial (post‐juvenile) moult, the expression of ornamentation was closely dependent on individual condition, however the condition‐dependence of ornamentation sharply decreased throughout a males lifetime and in older males expression of sexual ornamentation was largely independent of condition during moult. Selection for early breeding favoured greater ornamentation in males that were single in the preceding seasons and the strength of this selection increased with age. On the contrary, the strength of selection on sexual ornamentation decreased with age in males that were paired in the preceding breeding season. Our results reveal strong context‐dependency in investment into sexual ornamentation as well as a high flexibility in the development of sexual ornamentation throughout a males life.

Evolution of genetic integration between dispersal and colonization ability in a bird

Discrete behavioral strategies comprise a suite of traits closely integrated in their expression with consistent natural selection for such coexpression leading to developmental and genetic integration of their components. However, behavioral traits are often also selected to respond rapidly to changing environments, which should both favor their context-dependent expression and inhibit evolution of genetic integration with other, less flexible traits. Here we use a multigeneration pedigree and longterm data on lifetime fitness to test whether behaviors comprising distinct dispersal strategies of western bluebirds—a species in which the propensity to disperse is functionally integrated with aggressive behavior—are genetically correlated. We further investigated whether selection favors flexibility in the expression of aggression in relation to current social context. We found a significant genetic correlation between aggression and dispersal that is concordant with consistent selection for coexpression of these behaviors. To a limited extent, individuals modified their aggression to match their mate; however, we found no fitness consequences on such adjustments. These results introduce a novel way of viewing behavioral strategies, where flexibility of behavior, while often aiding an organisms fit in its current environment, may be limited and thereby enable integration with less flexible traits.

Aggressive behaviour affects selection on morphology by influencing settlement patterns in a passerine bird

The importance of behaviours as instigators or inhibitors of evolutionary change remains largely unresolved and this is in part because there are very few empirical examples of how behaviours affect evolutionary processes. By determining the environment of breeding, aggressive interactions over territories have the potential to strongly impact selection pressures experienced by individuals. Western bluebirds (Sialia mexicana) provide a unique opportunity to investigate the evolutionary importance of aggression, since their highly variable breeding habitat favours distinct foraging techniques and they also compete aggressively for nest boxes, a resource that is easy to manipulate. Here, I show experimentally that more aggressive males compete more effectively for territories with a high density of nest boxes and, as a consequence, aggressive and non-aggressive males are sorted into distinct breeding habitats that differ in the strength of selection on morphological traits. Specifically, males with longer tails and tarsi were favoured in open habitats where high agility is required to forage efficiently, whereas in forested habitats, where agility is less important, selection was weak. These results show that aggression can affect selection on a local scale by determining individual settlement patterns. More generally, because territorial interactions are important across a wide variety of taxa, these results suggest that aggressive behaviour has the potential to impact the evolutionary trajectory of many animal populations.

Cycles of species replacement emerge from locally induced maternal effects on offspring behavior in a passerine bird

Mother knows best Dynamic natural environments are challenging places to start life. In many species, however, the environment the mother lives in can actually shape the environment in which her offspring grow. Such maternal effects facilitate the exchange of important environmental information across generations. Duckworth et al. show that a mothers physiological responses to her environment can convey more complex information than we thought (see the Perspective by Dantzer). Female western bluebirds deposit more androgens in their eggs when competition for nest sites increases. This results in more-aggressive male chicks that are more likely to move on and colonize new, less crowded habitats. Science, this issue p. 875; see also p. 822 Bluebird colonization of new habitats is driven by the mother’s experience of overcrowding affecting her sons’ aggression levels. [Also see Perspective by Dantzer] An important question in ecology is how mechanistic processes occurring among individuals drive large-scale patterns of community formation and change. Here we show that in two species of bluebirds, cycles of replacement of one by the other emerge as an indirect consequence of maternal influence on offspring behavior in response to local resource availability. Sampling across broad temporal and spatial scales, we found that western bluebirds, the more competitive species, bias the birth order of offspring by sex in a way that influences offspring aggression and dispersal, setting the stage for rapid increases in population density that ultimately result in the replacement of their sister species. Our results provide insight into how predictable community dynamics can occur despite the contingency of local behavioral interactions.

Evolution of sex‐biased maternal effects in birds. IV. Intra‐ovarian growth dynamics can link sex determination and sex‐specific acquisition of resources

The evolutionary importance of maternal effects is determined by the interplay of maternal adaptations and strategies, offspring susceptibility to these strategies, and the similarity of selection pressures between the two generations. Interaction among these components, especially in species where males and females differ in the costs and requirements of growth, limits inference about the evolution of maternal strategies from their expression in the offspring phenotype alone. As an alternative approach, we examine divergence in the proximate mechanisms underlying maternal effects across three house finch populations with contrasting patterns of sex allocation: an ancestral population that shows no sex‐biased ovulation, and two recently established populations at the northern and southern boundaries of the species range that have opposite sequences of ovulation of male and female eggs. For each population, we examined how oocyte acquisition of hormones, carotenoids and vitamins was affected by oocyte growth and overlap with the same and opposite sexes. Our results suggest that sex‐specific acquisition of maternal resources and sex determination of oocytes are linked in this system. We report that acquisition of testosterone by oocytes that become males was not related to growth duration, but instead covaried with temporal exposure to steroids and overlap with other male oocytes. In female oocytes, testosterone acquisition increased with the duration of growth and overlap with male oocytes, but decreased with overlap with female oocytes. By contrast, acquisition of carotenoids and vitamins was mostly determined by organism‐wide partitioning among oocytes and oocyte‐specific patterns of testosterone accumulation, and these effects did not differ between the sexes. These results provide important insights into three unresolved phenomena in the evolution of maternal effects – (i) the evolution of sex‐specific maternal allocation in species with simultaneously developing neonates of both sexes; (ii) the link between sex determination and sex‐specific acquisition of maternal products; and (iii) the evolution of context‐dependent modulation of maternal effects.

FIRST CASE OF MYCOPLASMA GALLISEPTICUM INFECTION IN THE WESTERN RANGE OF THE HOUSE FINCH (CARPODACUS MEXICANUS)

Abstract We report the first case of mycoplasmosis in the western range of the House Finch (Carpodacus mexicanus). This disease originated in the eastern United States and has been previously documented only in eastern introduced House Finch populations where it reached epizootic proportions causing extensive and widespread mortality. Documentation of this dis-ease in western Montana suggests that previously disjunct eastern and western populations of House Finches are now mixing in the northern part of their range. More importantly, as native House Finches are highly susceptible to this novel pathogen, western populations may now be at risk of high mortality, similar to that experienced by non-native eastern populations. Close monitoring of this disease in the western part of the House Finch range will provide important insight into the dynamics of the emerging disease and evolution of resistance to the pathogen.

Kin aggression and resource availability influence phenotype-dependent dispersal in a passerine bird

Understanding the causes of dispersal is important as it strongly influences population dynamics and evolution. However, context dependency of dispersal decisions, such as effects of social interactions and resource availability, is rarely disentangled from intrinsic factors, such as animal personality. Western bluebirds provide a unique opportunity to investigate the relative importance of intrinsic versus extrinsic factors in dispersal decisions because they display distinct aggressive personality types, have high recruitment of sons to the natal population, and depend on nest cavities, a resource that is easy to quantify. Here, we measured territorial interactions among kin and non-kin, resource availability, and aggressive behavior over an 11-year period to determine how they influenced dispersal decisions of male offspring. We found that distance dispersed from kin was driven by a male’s own aggression, the aggression of his nearest kin, and the resources available on the natal territory. Both aggressive males and males with aggressive kin dispersed longer distances, as did males who had fewer resources on their natal territories. Thus, dispersal in this species is influenced jointly by intrinsic and extrinsic factors. Because resource acquisition and personality type are interdependent in this species, changes in the social environment are likely to have important consequences for population dynamics.