Plasticity in social behaviour varies with reproductive status in an avian cooperative breeder.

Cooperatively breeding vertebrates are common in unpredictable environments where the costs and benefits of providing offspring care fluctuate temporally. To balance these fitness outcomes, individuals of cooperatively breeding species often exhibit behavioural plasticity according to environmental conditions. Although individual variation in cooperative behaviours is well-studied, less is known about variation in plasticity of social behaviour. Here, we examine the fitness benefits, plasticity and repeatability of nest guarding behaviour in cooperatively breeding superb starlings (Lamprotornis superbus). After demonstrating that the cumulative nest guarding performed at a nest by all breeders and helpers combined is a significant predictor of reproductive success, we model breeder and helper behavioural reaction norms to test the hypothesis that individuals invest more in guarding in favourable seasons with high rainfall. Variation in nest guarding behaviour across seasons differed for individuals of different reproductive status: breeders showed plastic nest guarding behaviour in response to rainfall, whereas helpers did not. Similarly, we found that individual breeders show repeatability and consistency in their nest guarding behaviour while individual helpers did not. Thus, individuals with the potential to gain direct fitness benefits exhibit greater plasticity and individual-level repeatability in cooperative behaviour.

The development of behavioral and endocrine coping styles in nestlings from urban and rural sites.

Urbanization is increasing globally and altering the stressors that animals face in their everyday lives. Organisms often differ in their coping styles-both behavioral and endocrine-across urban to rural habitats. For example, urban animals are often bolder, more exploratory, and mount stronger glucocorticoid stress responses compared to their rural counterparts. While these coping styles are important in shaping fitness across the urban-to-rural gradient, it remains unclear when these differences arise in the life of organisms. We explore the development of coping styles in European starling nestlings (Sturnus vulgaris), an urban-adapted species. We test whether breathing rate, handling struggle rate, and bag struggle rate differ across sites and find no difference in the behavioral coping styles of nestlings raised in urban versus rural sites. We also explore differences in baseline and stress-induced glucocorticoids, finding that urban nestlings develop a stronger stress response than rural birds before fledging the nest. We find no significant correlations between behavioral and endocrine traits for urban or rural birds, which supports the two-tiered model of coping styles. One possibility is that behavioral and endocrine differences develop at different times over the lives of organisms. Our findings support prior work suggesting that behavioral and endocrine coping mechanisms act independently of one another, and suggests that endocrine coping mechanisms develop in early life and before differences in behavioral coping styles might arise. Future work on the mechanisms leading to early-life differences in coping styles-from genetics to maternal effects to environmental effects-is needed to best predict how urban-adapted organisms cope with environmental change. Studies across a greater number of sites will help disentangle site from urbanization effects.

Long-Term Measures of Climate Unpredictability Shape the Avian Endocrine Stress Axis.

AbstractThe vertebrate glucocorticoid stress response is an important mechanism facilitating pleiotropic phenotypic adjustments for coping with environmental change and optimizing fitness. Although circulating glucocorticoid hormones are mediators of plasticity that individuals can adjust rapidly in response to environmental challenges, they are also shaped by ecological selection. It remains unclear, however, how environmental variation on different timescales influences glucocorticoids. Here, we use an intraspecific comparative approach to determine how variation in precipitation on different timescales (months, years, decades) shapes distinct components of the glucocorticoid response. We sampled superb starlings (Lamprotornis superbus) at eight sites across Kenya in multiple years that differed in precipitation. Among-population variation in baseline glucocorticoids was shaped by both short- and long-term precipitation, whereas variation in stress-induced levels was poorly explained by precipitation on any timescale. Adrenal sensitivity, quantified via adrenocorticotropic hormone injections, was shaped by long-term precipitation and was highest in unpredictable environments. Together, these results suggest that variation in glucocorticoids can be best explained by environmental variation at timescales that extend beyond the lives of individuals, although baseline glucocorticoids also reflect short-term environmental conditions. Patterns of long-term precipitation may represent a microevolutionary selective pressure shaping the endocrine stress axis across populations and influencing how individuals cope with environmental change.

Survival Benefits of Group Living in a Fluctuating Environment.

Group living is predicted to arise only when the fitness benefits outweigh the costs of sociality. Group-living species-including cooperatively breeding and family-living birds and mammals-occur most frequently in environments where climatic conditions fluctuate unpredictably from year to year. The fitness consequences of group living are thus expected to vary with changing environmental conditions, though few studies have examined this possibility. We examined whether living in large social groups improves adult survivorship in cooperatively breeding superb starlings (Lamprotornis superbus). We also tested the hypothesis that larger groups buffer against harsh conditions by increasing survivorship most under periods of low rainfall. We found that group size was positively correlated with adult survival but in a sex-specific manner: female survival increased with group size across all environmental conditions, whereas male survival increased with group size only in wet years. Together with previous work in this system, our results suggest that larger groups confer survival benefits by reducing predation, rather than by improving access to food or buffering against physiological stress. Although group living does not appear to buffer against harsh conditions in adult starlings living in a fluctuating environment, living in larger groups does confer a survival advantage.

Individual variation in phenotypic plasticity of the stress axis.

Phenotypic plasticity-one individual's capacity for phenotypic variation under different environments-is critical for organisms facing fluctuating conditions within their lifetime. North American red squirrels (Tamiasciurus hudsonicus) experience drastic among-year fluctuations in conspecific density. This shapes juvenile competition over vacant territories and overwinter survival. To help young cope with competition at high densities, mothers can increase offspring growth rates via a glucocorticoid-mediated maternal effect. However, this effect is only adaptive under high densities, and faster growth often comes at a cost to longevity. While red squirrels can adjust hormones in response to fluctuating density, the degree to which mothers differ in glucocorticoid plasticity across changing densities remains unknown. Findings from our reaction norm approach revealed significant individual variation not only in a female red squirrel's mean endocrine phenotype but also in endocrine plasticity in response to changes in local density. Future work on proximate and ultimate drivers of variation in endocrine plasticity and maternal effects is needed, particularly in free-living animals experiencing fluctuating environments.

Testosterone, social status and parental care in a cooperatively breeding bird.

The steroid hormone testosterone not only plays an important role in gamete production, but also influences social and aggressive behavior. Testosterone varies seasonally, peaking when competition for mates is high and declining during parental care. Surprisingly, little is known about how testosterone mediates social conflict and parental care behavior in highly social species like cooperative breeders, where group members compete for breeding opportunities and provide parental or alloparental care. We examined how testosterone differs across breeding roles in the tropical cooperatively breeding superb starling, Lamprotornis superbus. We determined whether testosterone was elevated in larger groups, and whether testosterone was negatively related to total levels of parental and alloparental care. We found that male breeders had higher testosterone than male helpers and female breeders and helpers during incubation. However, breeding males exhibited a significant decline in testosterone from incubation to chick rearing, and all individuals had similar levels during the chick rearing stage. Additionally, helpers-but not breeders-in large social groups had higher testosterone than those in small groups. Finally, testosterone was not correlated with nestling provisioning rates during chick rearing, suggesting that natural variation in the low levels of testosterone observed during periods of high parental care does not affect nestling provisioning. Together, these results offer insight into how testosterone is related to breeding roles, intra-group conflict, and parental care in a highly social species.

No short-term physiological costs of offspring care in a cooperatively breeding bird.

The cost of reproduction results in a life-history trade-off where investment in current reproduction via costly parental care decreases subsequent fitness. Although this trade-off is thought to occur ubiquitously across animals, there is equivocal evidence that parental care behaviours are costly. A major challenge of studying the cost of parental care has been a lack of consensus over which physiological mechanisms underlie this trade-off. Here, we compare four traits believed to mediate the cost of parental care by examining whether glucocorticoids, oxidative stress, immune function or body condition represent a cost of performing offspring care and shape subsequent fitness. We use a 4 year dataset collected in free-living cooperatively breeding superb starlings (Lamprotornis superbus), a species in which parental and alloparental care effort varies widely among individuals and across years. Our results showed that within-individual change in physiology was unrelated to investment in offspring care, and physiological state during chick rearing did not predict the likelihood that an individual would breed in subsequent seasons. Instead, individuals that had elevated baseline corticosterone during incubation performed more nest guarding, suggesting that this hormone may play a preparatory role for investing in offspring care. Together, our results indicate that superb starlings modify their investment in offspring care according to their physiological state during incubation, despite there being no evidence of a short-term physiological cost of parental or alloparental care. Thus, breeding cooperatively appears to provide individuals with the flexibility to adjust their investment in offspring care and overcome any potential costs of reproduction.

The oxidative costs of parental care in cooperative and pair-breeding African starlings.

The cost of parental care has long been thought to favor the evolution of cooperative breeding, because breeders can provide reduced parental care when aided by alloparents. Oxidative stress-the imbalance between reactive oxygen species and neutralizing antioxidants-has been proposed to mediate the cost of parental care, though results from empirical studies remain equivocal. We measured changes in oxidative status during reproduction in cooperatively breeding superb starlings (Lamprotornis superbus) to gain insight into the relationships among breeding status, parental care, and oxidative stress. We also compared the oxidative cost of reproduction in the cooperatively breeding superb starling to that in a sympatric non-cooperatively breeding species, the greater blue-eared glossy starling (L. chalybaeus), to determine whether cooperatively breeding individuals face reduced oxidative costs of parental care relative to non-cooperatively breeding individuals. Breeders and alloparents of the cooperative species did not differ in oxidative status throughout a breeding attempt. However, individuals of the non-cooperative species incurred an increase in reactive oxygen metabolites proportionally to an individual's workload during offspring care. These findings suggest that non-cooperative starlings experience an oxidative cost of parental care, whereas cooperatively breeding starlings do not. It is possible that high nest predation risk and multi-brooding in the cooperatively breeding species may have favored reduced physiological costs of parental care more strongly compared to pair-breeding starlings. Reduced physiological costs of caring for young may thus represent a direct benefit that promotes cooperative breeding.

Elevated lead (Pb) in urban European starling (Sturnus vulgaris) feathers is not correlated to physiology or behavior.

Urbanization is rapidly changing the environment and creating new challenges in the lives of animals across the globe. Anthropogenic contaminants-like heavy metals-can persist within the environment for prolonged periods of time and present a widespread problem for those living near contaminated areas. Lead (Pb) was a commonly used heavy metal that continues to threaten the health of all organisms despite being phased out, especially in urban areas where historical use was more common. In this study, a common urban-adapter, the European starling (Sturnus vulgaris), was trapped to explore whether feather Pb burden is greater in birds from urban habitats than rural habitats, as well as whether Pb burdens were correlated with behavior, physiology, and feather development. Across four sites (two rural and two urban), soil Pb concentrations were measured and 197 free-living starlings were captured to measure feather Pb concentrations. Using linear mixed models, this study found that urban starling nestlings had elevated feather Pb burdens compared to rural nestlings. In contrast, there was no correlation between Pb and urbanization in adult birds whose exposure to Pb may reflect a larger spatial range compared to nestlings. For both nestlings and adults, feather Pb was uncorrelated to corticosterone, testosterone, aggressive behavior, or feather growth rates. These findings suggest that starlings may be a useful biomonitoring tool to detect Pb in the local environment, however, the age and spatial range of birds is a critical consideration in applying this tool. Further work is needed to understand the intricate relationship between heavy metals, behavior, morphological development, and physiology in free-living organisms.

Individual Variation in Glucocorticoid Plasticity: Considerations and Future Directions.

The hypothalamic-pituitary-adrenal (HPA) axis regulates the secretion of glucocorticoids, hormones with diverse roles ranging from regulating daily metabolic demand to coping with sudden perturbations. As a result, glucocorticoids are thought to help vertebrates track their changing environments and coordinate plasticity in diverse phenotypes. While this endocrine system is highly plastic-where one individual can produce multiple phenotypes across varying environmental conditions-little is understood about the degree to which individuals, populations, or species differ in circulating glucocorticoid plasticity. Empirical research quantifying individual variation in glucocorticoid plasticity has increased in recent years, though the multiple complex roles of the HPA-axis make it challenging to generalize the extent to which individual variation in plasticity exists. I provide an overview of current findings on variation in glucocorticoids plasticity, and outline multiple types of glucocorticoid plasticity researchers should consider in future work to advance our understanding of the causes and consequences of individual variation in glucocorticoid plasticity.

The Evolutionary Endocrinology of Circulating Glucocorticoids in Free-Living Vertebrates: Recent Advances and Future Directions across Scales of Study.

Circulating glucocorticoid hormone concentrations are dynamic, flexible, and promote adaptive responses following perturbations in an animal's environment. As a result, circulating glucocorticoid levels are thought to shape fitness and have been suggested to be a key trait for predicting how species will cope with novel environmental change. Nevertheless, the factors that shape variation in glucocorticoid-mediated coping mechanisms remain unclear because the evolutionary underpinnings of the function and regulation of these hormones are poorly understood. Here, I summarize recent advances in our understanding of the evolution of circulating glucocorticoids, which have included (i) longitudinal studies exploring microevolutionary processes that shape within- and between-individual variation in glucocorticoids, (ii) interspecific comparative studies highlighting macro-evolutionary patterns of among-species variation in glucocorticoids, and (iii) intraspecific comparative studies which help to disentangle the relative roles of environment, life-history, and behavior in shaping among-population variation in glucocorticoids. Important avenues for future research will include exploring how natural selection may act on different components of the hypothalamus-pituitary-adrenal axis, characterizing patterns of phenotypic plasticity in circulating glucocorticoids across populations and species, as well as exploring how microevolutionary processes differ across taxa or gradients of environmental conditions.

Multiple benefits of alloparental care in a fluctuating environment.

Although cooperatively breeding vertebrates occur disproportionately in unpredictable environments, the underlying mechanism shaping this biogeographic pattern remains unclear. Cooperative breeding may buffer against harsh conditions (hard life hypothesis), or additionally allow for sustained breeding under benign conditions (temporal variability hypothesis). To distinguish between the hard life and temporal variability hypotheses, we investigated whether the number of alloparents at a nest increased reproductive success or load-lightening in superb starlings (Lamprotornis superbus), and whether these two types of benefits varied in harsh and benign years. We found that mothers experienced both types of benefits consistent with the temporal variability hypothesis, as larger contingents of alloparents increased the number of young fledged while simultaneously allowing mothers to reduce their provisioning rates under both harsh and benign rainfall conditions. By contrast, fathers experienced load-lightening only under benign rainfall conditions, suggesting that cooperative breeding may serve to take advantage of unpredictable benign breeding seasons when they do occur. Cooperative breeding in unpredictable environments may thus promote flexibility in offspring care behaviour, which could mitigate variability in the cost of raising young. Our results highlight the importance of considering how offspring care decisions vary among breeding roles and across fluctuating environmental conditions.

Effects of sibling competition on growth, oxidative stress, and humoral immunity: a two-year brood-size manipulation.

We investigated the effects of ecological context (by comparing data from two consecutive years) and experimentally manipulated nestling developmental conditions (large vs. small brood size) on immune function (immunoglobulin Y [IgY]) and oxidative stress in nestling European starlings Sturnus vulgaris. On the basis of annual differences in chicks' morphological traits and body masses close to fledging, we established that 2007 was a relative low-quality year and 2008 was a relatively high-quality year. Total antioxidant capacity (TAC) was significantly lower in experimentally enlarged broods, but only in the low-quality year (2007). Total oxidant status (TOS) was independent of brood size in both years but was 45% higher in the low-quality year. Consequently, plasma oxidative status (the ratio between TOS and TAC) was higher in 2007. In contrast, plasma IgY levels were higher in the experimentally enlarged broods and in the high-quality year (2008). Thus, immune function and oxidative stress showed inverse relationships with developmental conditions and annual variation in year quality. Finally, TOS and TAC were positively correlated, but only in the low-quality year (2007), and there was no relationship observed between IgY and markers of oxidative stress. Our results demonstrate the importance of taking into account year effects or ecological context when assessing environmental effects on physiological mechanisms underlying the life-history traits of chicks, such as oxidative stress.

Variation in the timing of autonomous selfing among populations that differ in flower size, time to reproductive maturity, and climate.

PREMISE OF THE STUDY: Early reproductive maturity is common in dry and ephemeral habitats and often associated with smaller flowers with increased potential for within-flower (autonomous) self-pollination. We investigated whether populations from locations that differ in moisture availability, known to vary for whole-plant development rate, also varied in the timing of autonomous selfing. This timing is of interest because the modes of selfing (prior, competing, and delayed) have different fitness consequences. • METHODS: We measured timing of anther dehiscence, stigma receptivity, and herkogamy under pollinator-free conditions for plants from three populations of Collinsia parviflora that differed in annual precipitation, flower size, and time to sexual maturity. Using a manipulative experiment, we determined potential seed production via prior, competing, and delayed autonomous selfing for each population. • KEY RESULTS: Stigma receptivity, anther dehiscence, and selfing ability covaried with whole-plant development and climate. Plants from the driest site, which reached sexual maturity earliest, had receptive stigmas and dehiscent anthers in bud. Most seeds were produced via prior selfing. The population from the wettest site with slowest development was not receptive until after flowers opened. Although competing selfing was possible, all selfing was delayed. The intermediate population was between these extremes, with significant contributions from both competing and delayed selfing. • CONCLUSIONS: Our results demonstrate that within-species variation in the timing of selfing occurs and is related to both environmental conditions and whole-plant development rates. We suggest that, if these results can be generalized to other species, mating systems may evolve in response to ongoing climatic change.