Coping styles vary with species' sociality and life history: A systematic review and meta-regression analysis.

Despite a long history of animal studies investigating coping styles, the causal connections between behavior and stress physiology remain unclear. Consistency across taxa in effect sizes would support the idea of a direct causal link maintained by either functional or developmental dependencies. Alternatively, lack of consistency would suggest coping styles are evolutionarily labile. Here, we investigated correlations between personality traits and baseline and stress-induced glucocorticoid levels using a systematic review and meta-analysis. Most personality traits did not consistently vary with either baseline or stress-induced glucocorticoids. Only aggression and sociability showed a consistent negative correlation with baseline glucocorticoids. We found that life history variation affected the relationship between stress-induced glucocorticoid levels and personality traits, especially anxiety and aggression. The relationship between anxiety and baseline glucocorticoids depended on species' sociality with solitary species showing more positive effect sizes. Thus, integration between behavioral and physiological traits depends on species' sociality and life history and suggests high evolutionary lability of coping styles.

Linking Ecological Specialization to Its Macroevolutionary Consequences: An Example with Passerine Nest Type.

A long-standing hypothesis in evolutionary biology is that the evolution of resource specialization can lead to an evolutionary dead end, where specialists have low diversification rates and limited ability to evolve into generalists. In recent years, advances in comparative methods investigating trait-based differences associated with diversification have enabled more robust tests of this idea and have found mixed support. We test the evolutionary dead end hypothesis by estimating net diversification rate differences associated with nest-type specialization among 3224 species of passerine birds. In particular, we test whether the adoption of hole-nesting, a nest-type specialization that decreases predation, results in reduced diversification rates relative to nesting outside of holes. Further, we examine whether evolutionary transitions to the specialist hole-nesting state have been more frequent than transitions out of hole-nesting. Using diversification models that accounted for background rate heterogeneity and different extinction rate scenarios, we found that hole-nesting specialization was not associated with diversification rate differences. Furthermore, contrary to the assumption that specialists rarely evolve into generalists, we found that transitions out of hole-nesting occur more frequently than transitions into hole-nesting. These results suggest that interspecific competition may limit adoption of hole-nesting, but that such competition does not result in limited diversification of hole-nesters. In conjunction with other recent studies using robust comparative methods, our results add to growing evidence that evolutionary dead ends are not a typical outcome of resource specialization. [Cavity nesting; diversification; hidden-state models; passerines; resource specialization.].

Dynamic Changes in Begging Signal Short-Term Information on Hunger and Need.

AbstractDynamic signals can convey distinct information to a receiver on different timescales, making assessment of how quickly signal strength changes important for understanding signal function. Here, we combine repeated measures of offspring begging behavior of western bluebirds with assessments of fitness as well as quantitative genetic analyses of cross-fostered offspring to investigate whether variation in begging behavior conveys information about hunger, need, or quality or has no signaling function. Begging intensity increased with food deprivation, supporting the signal-of-hunger hypothesis. However, after controlling for this variation, multiple lines of evidence showed that begging also signaled need but not quality. Specifically, begging intensity was repeatable only on short timescales, and nestlings that begged more intensely were in poorer condition. Moreover, variation in mean begging intensity was not strongly related to measures of fitness. In general, we found that begging behavior is a highly flexible trait that appears to be unconstrained by both genetic and early developmental influences, as indicated by the cross-fostering experiment that confirmed that the nest environment, not genetic relatedness, explained variation in begging behavior. Together, these results support the idea that begging dynamically signals shorter-term information: hunger and need. More generally, they show the importance of assessing the timescale of signal change to understand its function.

Nest predation risk and deposition of yolk steroids in a cavity-nesting songbird: an experimental test.

Maternal hormones can shape offspring development and increase survival when predation risk is elevated. In songbirds, yolk androgens influence offspring growth and begging behaviors, which can help mitigate offspring predation risk in the nest. Other steroids may also be important for responding to nest predation risk, but non-androgen steroids have been poorly studied. We used a nest predator playback experiment and liquid chromatography with tandem mass spectrometry (LC-MS-MS) to assess whether nest predation risk influences deposition of 10 yolk steroids. We found no clear evidence that yolk androgen deposition changed when perception of nest predation risk was experimentally increased. However, elevated nest predation risk led to decreased yolk progesterone deposition. Overall, our results suggest yolk progesterone may be more important than yolk androgens in responses to offspring predation risk and highlight new avenues for research.

Maternally derived hormones, neurosteroids and the development of behaviour.

In a wide range of taxa, there is evidence that mothers adaptively shape the development of offspring behaviour by exposing them to steroids. These maternal effects have major implications for fitness because, by shaping early development, they can permanently alter how offspring interact with their environment. However, theory on parent-offspring conflict and recent physiological studies showing that embryos rapidly metabolize maternal steroids have placed doubt on the adaptive significance of these hormone-mediated maternal effects. Reconciling these disparate perspectives requires a mechanistic understanding of the pathways by which maternal steroids can influence neural development. Here, we highlight recent advances in developmental neurobiology and psychiatric pharmacology to show that maternal steroid metabolites can have direct neuro-modulatory effects potentially shaping the development of neural circuitry underlying ecologically relevant behavioural traits. The recognition that maternal steroids can act through a neurosteroid pathway has critical implications for our understanding of the ecology and evolution of steroid-based maternal effects. Overall, compared to the classic view, a neurosteroid mechanism may reduce the evolutionary lability of hormone-mediated maternal effects owing to increased pleiotropic constraints and frequently influence long-term behavioural phenotypes in offspring.

Multiple Environmental Stressors Induce an Adaptive Maternal Effect.

AbstractEvolution of adaptation requires predictability and recurrence of functional contexts. Yet organisms live in multifaceted environments that are dynamic and ever changing, making it difficult to understand how complex adaptations evolve. This problem is particularly apparent in the evolution of adaptive maternal effects, which are often assumed to require reliable and discrete cues that predict conditions in the offspring environment. One resolution to this problem is if adaptive maternal effects evolve through preexisting, generalized maternal pathways that respond to many cues and also influence offspring development. Here, we assess whether an adaptive maternal effect in western bluebirds is influenced by maternal stress pathways across multiple challenging environments. Combining 18 years of hormone sampling across diverse environmental contexts with an experimental manipulation of the competitive environment, we show that multiple environmental factors influenced maternal corticosterone levels, which, in turn, influenced a maternal effect on aggression of sons in adulthood. Together, these results support the idea that multiple stressors can induce a known maternal effect in this system. More generally, they suggest that activation of general pathways, such as the hypothalamic-pituitary-adrenal axis, may simplify and facilitate the evolution of adaptive maternal effects by integrating variable environmental conditions into preexisting maternal physiological systems.

Scrutinizing assortative mating in birds.

It is often claimed that pair bonds preferentially form between individuals that resemble one another. Such assortative mating appears to be widespread throughout the animal kingdom. Yet it is unclear whether the apparent ubiquity of assortative mating arises primarily from mate choice ("like attracts like"), which can be constrained by same-sex competition for mates; from spatial or temporal separation; or from observer, reporting, publication, or search bias. Here, based on a conventional literature search, we find compelling meta-analytical evidence for size-assortative mating in birds (r = 0.178, 95% CI 0.142-0.215, 83 species, 35,591 pairs). However, our analyses reveal that this effect vanishes gradually with increased control of confounding factors. Specifically, the effect size decreased by 42% when we used previously unpublished data from nine long-term field studies, i.e., data free of reporting and publication bias (r = 0.103, 95% CI 0.074-0.132, eight species, 16,611 pairs). Moreover, in those data, assortative mating effectively disappeared when both partners were measured by independent observers or separately in space and time (mean r = 0.018, 95% CI -0.016-0.057). Likewise, we also found no evidence for assortative mating in a direct experimental test for mutual mate choice in captive populations of Zebra finches (r = -0.020, 95% CI -0.148-0.107, 1,414 pairs). These results highlight the importance of unpublished data in generating unbiased meta-analytical conclusions and suggest that the apparent ubiquity of assortative mating reported in the literature is overestimated and may not be driven by mate choice or mating competition for preferred mates.

Hybridization Associated with Cycles of Ecological Succession in a Passerine Bird.

Identifying the diversity of contexts that can lead to hybridization is important for understanding its prevalence and dynamics in natural populations. Despite the potential of ecological succession to dramatically alter species co-occurrence and abundances, it is unknown whether it directly promotes hybridization and, if so, has long-lasting consequences. Here, we summarize 30 years of survey data across 10 populations to show that in western and mountain bluebirds, heterospecific pairing occurs during repeatable and transient colonization events at the early stages of species turnover. Despite mixed pairing occurring only during early succession, genetic data showed presence of hybrids at both early and late successional stages. Moreover, hybrids showed novel patterns of variation in morphology and behavior, emphasizing that even ephemeral contexts for hybridization can have important evolutionary consequences. Our results suggest that because ecological succession often brings together closely related competitors in disparate numbers but lasts for only a brief period of time, it may be a widespread but underappreciated context for hybridization.

Neuroendocrine mechanisms underlying behavioral stability: implications for the evolutionary origin of personality.

Personality traits are behaviors that show limited flexibility over time and across contexts, and thus understanding their origin requires an understanding of what limits behavioral flexibility. Here, I suggest that insight into the evolutionary origin of personality traits requires determining the relative importance of selection and constraint in producing limits to behavioral flexibility. Natural selection as the primary cause of limits to behavioral flexibility assumes that the default state of behavior is one of high flexibility and predicts that personality variation arises through evolution of buffering mechanisms to stabilize behavioral expression, whereas the constraint hypothesis assumes that the default state is one of limited flexibility and predicts that the neuroendocrine components that underlie personality variation are those most constrained in flexibility. Using recent work on the neurobiology of sensitive periods and maternal programming of offspring behavior, I show that some of the most stable aspects of the neuroendocrine system are structural components and maternally induced epigenetic effects. Evidence of numerous constraints to changes in structural features of the neuroendocrine system and far fewer constraints to flexibility of epigenetic systems suggests that structural constraints play a primary role in the origin of behavioral stability and that epigenetic programming may be more important in generating adaptive variation among individuals.

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

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.

Maternal effects and range expansion: a key factor in a dynamic process?

Species that depend on ephemeral habitat often evolve distinct dispersal strategies in which the propensity to disperse is closely integrated with a suite of morphological, behavioural and physiological traits that influence colonizing ability. These strategies are maintained by natural selection resulting from spatial and temporal variation in resource abundance and are particularly evident during range expansion. Yet the mechanisms that maintain close alignment of such strategies with resource availability, integrate suites of dispersal traits and generate variability in dispersal propensity are rarely known. Breeding females can influence offspring phenotype in response to changes in current environmental conditions, making maternal effects uniquely suited to bridge fluctuations in resource abundance in the maternal generation and variation in offspring dispersal ability. Western bluebirds' (Sialia mexicana) dependence on nest cavities--an ephemeral resource--has led to the evolution of two distinct dispersal phenotypes: aggressive males that disperse and non-aggressive males that remain philopatric and cooperate with their relatives. Over the last 40 years, western bluebirds rapidly expanded their geographical range, providing us with an opportunity to test, in newly established populations, the importance of maternal effects for generating variability in dispersal propensity. Here, I show that, under variable resource conditions, breeding females group offspring of different competitive ability in different positions in the egg-laying order and, consequently, produce aggressive males that are more likely to disperse when resources are low and non-aggressive philopatric males when resources are abundant. I then show experimentally that the association between resource availability and sex-specific birth order is robust across populations. Thus, this maternal effect enables close tracking of resource availability and may explain how variation in dispersal is generated in newly colonized populations. More generally, these results suggest that, as a key source of variation in colonizing phenotypes, maternal effects are of crucial importance for understanding the dynamics of range expansion.

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 long-term 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 organism's fit in its current environment, may be limited and thereby enable integration with less flexible traits.

Adaptive dispersal strategies and the dynamics of a range expansion.

In species undergoing range expansion, newly established populations are often more dispersive than older populations. Because dispersal phenotypes are complex and often costly, it is unclear how highly dispersive phenotypes are maintained in a species to enable their rapid expression during periods of range expansion. Here I test the idea that metapopulation dynamics of local extinction and recolonization maintain distinct dispersal strategies outside the context of range expansion. Western bluebirds display distinct dispersal phenotypes where aggressive males are more dispersive than nonaggressive males, resulting in highly aggressive populations at the edge of their expanding range. I experimentally created new habitat interior to the range edge to show that, as on the range front, it was colonized solely by aggressive males. Moreover, fitness consequences of aggression depended on population age: aggressive males had high fitness when colonizing new populations, while nonaggressive males performed best in an older population. These results suggest that distinct dispersal strategies were maintained before range expansion as an adaptation for the continual recolonization of new habitat. These results emphasize similarities between range expansion and metapopulation dynamics and suggest that preexisting adaptive dispersal strategies may explain rapid changes in dispersal phenotypes during range expansion.

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.

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.

Adaptive sex differences in growth of pre-ovulation oocytes in a passerine bird.

Maternal modification of offspring sex in birds has strong fitness consequences, however the mechanisms by which female birds can bias sex of their progeny in close concordance with the environment of breeding are not known. In recently established populations of house finches (Carpodacus mexicanus), breeding females lay a sex-biased sequence of eggs when ambient temperature causes early onset of incubation. We studied the mechanisms behind close association of incubation and sex-determination strategies in this species and discovered that pre-ovulation oocytes that produce males and females differed strongly in the temporal patterns of proliferation and growth. In turn, sex-specific exposure of oocytes to maternal secretion of prolactin and androgens produced distinct accumulation of maternal steroids in oocyte yolks in relation to oocyte proliferation order. These findings suggest that sex difference in oocyte growth and egg-laying sequence is an adaptive outcome of hormonal constraints imposed by the overlap of early incubation and oogenesis in this population, and that the close integration of maternal incubation, oocytes' sex-determination and growth might be under control of the same hormonal mechanism. We further document that population establishment and the evolution of these maternal strategies is facilitated by their strong effects on female and offspring fitness in a recently established part of the species range.

Sex-biased hatching order and adaptive population divergence in a passerine bird.

Most species of birds can lay only one egg per day until a clutch is complete, and the order in which eggs are laid often has strong and sex-specific effects on offspring growth and survival. In two recently established populations of the house finch (Carpodacus mexicanus) in Montana and Alabama, breeding females simultaneously adjusted the sex and growth of offspring in relation to their position in the laying order, thereby reducing the mortality of sons and daughters by 10 to 20% in both environments. We show experimentally that the reduction in mortality is produced by persistent and sex-specific maternal effects on the growth and morphology of offspring. These strong parental effects may have facilitated the rapid adaptive divergence among populations of house finches.