The stress of parenthood? Increased glucocorticoids in birds with experimentally enlarged broods

Variation in baseline glucocorticoid (cort) levels can be attributed, at least in part, to differences in energetic demands confronting individuals. Elevated baseline cort levels are routinely interpreted as indicating individuals in poor condition, with low relative fitness. However, when greater reproductive effort increases energetic demands, individuals with high cort might paradoxically be those with the highest fitness. Here, we experimentally test the hypothesis that increased reproductive demand causes increases in baseline cort (the Cort-Adaptation hypothesis). We measured maternal baseline cort before and after experimentally enlarging and reducing brood sizes in tree swallows (Tachycineta bicolor). Females with experimentally enlarged broods had greater increases in baseline cort and fledged more offspring than females with reduced broods. Additionally, females with greater increases in baseline cort had higher offspring-provisioning rates than females with lower changes in cort. These findings demonstrate that increased reproductive demand can cause increased baseline cort. As yet, we do not know if these increases in cort cause increased allocation of resources towards reproduction, but the positive relationship between parental behaviour and cort suggests that increased cort does not always interfere with reproductive investment, and might instead facilitate it.     

Behavioral and endocrine correlates of reproductive failure in social aggregations of captive wolverines (Gulo gulo)

Sociality in mammals is often viewed as a dichotomy, with sociality contrasted against solitariness. However, variation within these broad categories may have strong effects on individual fitness. For example, reproductive suppression of social subordinates is generally associated with group living, but suppression may also occur in solitary species if the behavioral and physiological processes involved can be modulated by the demographic environment. To investigate whether behavioral and physiological traits that normally are associated with group living might be latent even in a solitary species, we explored the level of sociality and investigated causes and mechanisms of reproductive failure in female wolverines Gulo gulo that experienced a highly aggregated social environment in captivity. Behaviorally, females showed low levels of aggression and intermediate levels of social interactions. Reproductive failure seemed to have been related to low social rank and to have occurred between ovulation and implantation in 13 out of 15 breeding attempts. However, three of eight females observed to mate produced offspring, indicating that no individual female fully managed to monopolize breeding. Reproductive failure was not related to elevated levels of glucocorticoid stress hormones. Rather, elevated glucocorticoid levels during the mating season were associated with successful reproduction. We suggest that social tendencies and physiological mechanisms mediating reproductive suppression may be viewed as reaction norms to the social environment. We further suggest that the social flexibility of solitary carnivores might be greater than is commonly observed, due to ecological constraints that may limit aggregation.     

Testosterone and cortisol concentrations vary with reproductive status in wild female red deer

Although hormones are key regulators of many fitness and life history traits, the causes of individual level variation in hormones, particularly in wild systems, remain understudied. Whilst we know that androgen and glucocorticoid levels vary within and among individuals in mammalian populations, how this relates to key reproductive processes such as gestation and lactation, and their effects on a female''s measurable hormone levels are poorly understood in wild systems. Using fecal samples collected from females in a wild red deer population between 2001 and 2013, we explore how fecal androgen (FAM) and cortisol (FCM) metabolite concentrations change with age and season, and how individual differences relate to variation in reproductive state. Both FAM and FCM levels increase toward parturition, although this only affects FCM levels in older females. FCM levels are also higher when females suckle a male rather than a female calf, possibly due to the higher energetic costs of raising a son. This illustrates the importance of accounting for a female''s life history and current reproductive status, as well as temporal variation, when examining individual differences in hormone levels. We discuss these findings in relation to other studies of mammalian systems and in particular to the relatively scarce information on variation in natural levels of hormones in wild populations.     

Sex-specific consequences of life in the city

The vast majority of species are excluded from human-dominatedlandscapes, but some species persist and appear to thrive, despitefacing challenges they would not encounter in less disturbedhabitat. Corticosteroid (cort) secretion may play a significantrole in enabling an animal to cope with urban breeding habitatbecause it helps mediate physiological and behavioral responsesto environmental challenges. Here we present tests of 3 hypothesesrelating to cort secretion in urban animals: 1) environmentalchallenges vary between urban and rural habitat, as reflectedin differing levels of cort secretion in animals breeding inthese habitat types, 2) there are fitness correlates associatedwith variation in cort levels within populations, and 3) parasiteload is one of the mechanistic links between variation in cortlevels and reproductive success. Male white-crowned sparrows(Zonotrichia leucophrys) in urban habitat had significantlyhigher baseline corticosterone levels than males in rural habitat,whereas female Z. leucophrys' hormone levels did not differbetween the 2 habitat types. To assess the fitness correlatesof variation in hormone levels, we monitored seasonal reproductivesuccess in one urban population and found that baseline corticosteronelevels were predictive of female, but not male, reproductivesuccess: females with higher corticosterone fledged fewer offspring.Data do not suggest a direct relationship between corticosteronelevels and fitness and instead indicate an indirect relationshipbetween hormone secretion, territory quality, body condition,and reproductive success. Females with blood parasites had lowerheterophil:lymphocyte ratios, lower body condition scores, fewermates, and fledged fewer offspring than females without parasites.In contrast, parasites did not negatively affect reproductivesuccess in males but were associated with reduced body condition.Corticosterone levels did not differ between birds with andwithout parasites. In tests of all 3 of our hypotheses, we foundsex-specific effects, highlighting the importance of consideringsex in investigation of physiological responses to disturbance.     

Non-breeding feather concentrations of testosterone, corticosterone and cortisol are associated with subsequent survival in wild house sparrows

Potential mechanistic mediators of Darwinian fitness, such as stress hormones or sex hormones, have been the focus of many studies. An inverse relationship between fitness and stress or sex hormone concentrations has been widely assumed, although empirical evidence is scarce. Feathers gradually accumulate hormones during their growth and provide a novel way to measure hormone concentrations integrated over time. Using liquid chromatography-tandem mass spectrometry, we measured testosterone, corticosterone and cortisol in the feathers of house sparrows (Passer domesticus) in a wild population which is the subject of a long-term study. Although corticosterone is considered the dominant avian glucocorticoid, we unambiguously identified cortisol in feathers. In addition, we found that feathers grown during the post-nuptial moult in autumn contained testosterone, corticosterone and cortisol levels that were significantly higher in birds that subsequently died over the following winter than in birds that survived. Thus, feather steroids are candidate prospective biomarkers to predict the future survival of individuals in the wild.     

Red-winged blackbirds (Agelaius phoeniceus) with higher baseline glucocorticoids also invest less in incubation and clutch mass

Glucocorticoid hormones facilitate responses to environmental challenges by mediating diverse physiological and behavioral changes, including resource mobilization and altered reproductive effort. Elevated glucocorticoids might indicate that an individual is facing high levels of environmental challenges and thus, elevated concentrations might be associated with reduced fitness (CORT-fitness hypothesis). Alternatively, the energetic demands of reproduction might be a challenge that requires elevated glucocorticoids to mobilize resources to support reproductive effort, ultimately increasing reproductive investment and fitness (CORT-adaptation hypothesis). Investigations of glucocorticoid-fitness relationships have yielded mixed results. Variation in the direction of this relationship could be caused in part by differences in the contexts in which the relationship was assessed. Incorporating context, such as life history stage, could be key to understanding the role of glucocorticoids in influencing fitness outcomes. We investigated the relationship between corticosterone and reproductive effort and success within a single life history stage: incubation of eggs. In an observational study, we measured baseline corticosterone in incubating female red-winged blackbirds (Agelaius phoeniceus), monitored incubation behavior, and determined hatching success for each nest. Incubating birds with higher baseline corticosterone concentrations had more frequent, shorter incubation bouts and spent less time overall incubating their clutches of eggs than birds with lower corticosterone concentrations. Elevated corticosterone was also associated with lower clutch mass, but neither corticosterone nor incubation effort were correlated with hatching success. Although experimental tests are needed to establish causation, these results suggest that during the incubation period, corticosterone might shift resource investment towards self-maintenance, and away from current reproductive effort.     

Hormonal correlates of individual quality in a long-lived bird: a test of the ‘corticosterone–fitness hypothesis’

Measuring individual quality in vertebrates is difficult. Focusing on allostasis mechanisms may be useful because they are functionally involved in the ability of an individual to survive and reproduce in its environment. Thus, a rise in stress hormones levels (corticosterone) occurs when an organism has to cope with challenging environmental conditions. This has recently led to the proposal of the ‘cort–fitness hypothesis’, which suggests that elevated baseline corticosterone levels should be found in individuals of poor quality that have difficulty coping with their environment. We tested this hypothesis by comparing an integrative measure of individual quality to baseline corticosterone in black-browed albatrosses (Thalassarche melanophrys). We found that individual baseline corticosterone levels were related to individual quality and highly repeatable from one breeding season to the next. Importantly, this relationship was found in males, but not in females. Therefore, we suggest that the relationship between quality and baseline corticosterone levels may depend on the environmental and energetic constraints that individuals have to cope with.     

Effectiveness of baseline corticosterone as a monitoring tool for fitness: a meta-analysis in seabirds

Many ecosystems have experienced anthropogenically induced changes in biodiversity, yet predicting these patterns has been difficult. Recently, individual behavioural and physiological measures have been proposed as more rapid links between environmental variation and fitness compared to demographics. Glucocorticoid hormones have received much attention given that they mediate energetic demands, metabolism, and foraging behaviour. However, it is currently unclear whether glucocorticoids can reliably predict environmental and fitness-related traits and whether they may be useful in specific groups of taxa. In particular, seabirds are a well-studied avian group often employed as biomonitoring tools for environmental change given their wide distribution and reliance on large oceanic patterns. Despite the increase in studies attempting to link variation in baseline corticosterone (the primary avian glucocorticoid) to variation in fitness-related traits in seabirds, there has been no comprehensive review of the relationship in this taxon. We present a phylogenetically controlled systematic review and meta-analysis of correlative and experimental studies examining baseline corticosterone as a predictor of fitness-related traits relevant to predicting seabird population health. Our results suggest that, while variation in baseline corticosterone may be a useful predictor of larger-scale environmental traits such as overall food availability and fitness-related traits such as reproductive success, this hormone may not be sensitive enough to detect variation in body condition, foraging effort, and breeding effort. Overall, our results support recent work suggesting that the use of baseline glucocorticoids as conservation biomarkers is complex and highly context dependent, and we suggest caution in their use and interpretation as simplified, direct biomarkers of fitness.     

Patterns of interventions and the effect of coalitions and sociality on male fitness

In group living animals, especially among primates, there is consistent evidence that high-ranking males gain a higher reproductive output than low-ranking males. Primate studies have shown that male coalitions and sociality can impact male fitness; however, it remains unclear whether males could potentially increase their fitness by preferentially supporting and socializing with females. Here we investigate patterns of male interventions and the effect of coalitions and sociality on male fitness in rhesus macaques (Macaca mulatta) with particular focus on male-female interactions. We combined behavioural observations collected on Cayo Santiago with genetic data analysed for male reproductive output and relatedness. Our results revealed that the ten top-ranking males provided the majority of all male support observed. In contrast to other primates, male rhesus macaques mainly formed all-down coalitions suggesting that coalitions are less likely used to enhance male dominance. Males supporting females during and before their likely conception were not more likely to fertilize those females. We also found no evidence that males preferably support their offspring or other close kin. Interestingly, the most important predictor of male support was sociality, since opponents sharing a higher sociality index with a given male were more likely to be supported. Furthermore, a high sociality index of a given male-female dyad resulted in a higher probability of paternity. Overall, our results strengthen the evidence that sociality affects fitness in male primates, but also suggest that in species in which males queue for dominance, it is less likely that males derive fitness benefits from coalitions.     

Consequences of acute stress and cortisol manipulation on the physiology, behavior, and reproductive outcome of female Pacific salmon on spawning grounds

Life-history theory predicts that stress responses should be muted to maximize reproductive fitness. Yet, the relationship between stress and reproduction for semelparous salmon is unusual because successfully spawning individuals have elevated plasma cortisol levels. To tease apart the effects of high baseline cortisol levels and stress-induced elevation of cortisol titers, we determined how varying degrees of cortisol elevation (i.e., acute and chronic) affected behavior, reproductive physiology, and reproductive success of adult female pink salmon (Oncorhynchus gorbuscha) relative to different states of ovulation (i.e., ripe and unripe). Exhaustive exercise and air exposure were applied as acute stressors to manipulate plasma cortisol in salmon either confined to a behavioral arena or free-swimming in a spawning channel. Cortisol (eliciting a cortisol elevation to levels similar to those in post-spawn female salmon) and metyrapone (a corticosteroid synthesis inhibitor) implants were also used to chemically manipulate plasma cortisol. Cortisol implants elevated plasma cortisol, and impaired reproductive success; cortisol-treated fish released fewer eggs and died sooner than fish in other treatment groups. In contrast, acute stressors elevated plasma cortisol and the metyrapone implant suppressed plasma cortisol, but neither treatment significantly altered reproductive success, behavior, or physiology. Our results suggest that acute stressors do not influence behavior or reproductive outcome when experienced upon arrival at spawning grounds. Thus, certain critical aspects of salmonid reproduction can become refractory to various stressful conditions on spawning grounds. However, there is a limit to the ability of these fish to tolerate elevated cortisol levels as revealed by experimental elevation of cortisol.     

Fitness and behavioral correlates of pre-stress and stress-induced plasma cortisol titers in pink salmon (Oncorhynchus gorbuscha) upon arrival at spawning grounds

Semelparous Pacific salmon (Onchorynchus spp.) serve as an excellent model for examining the relationships between life history, behavior and individual variation in glucocorticoid (GC) stress hormone levels because reproductive behaviors are highly variable between individuals and failure to reproduce results in zero fitness. Pink salmon (O. gorbuscha) were intercepted upon arrival at the spawning grounds across three time periods. Pre-stress and stress-induced plasma cortisol concentrations were assessed in relation to behavior, longevity and reproductive success. Results revealed differences between sexes and with arrival time. The study period marked a year of high reproductive success and only nine females (12% of sample) failed to spawn. Female pre-spawn mortalities were characterized by significantly elevated stress-induced cortisol concentrations and decreased longevity as well as pre-stress cortisol above the normal range in pink salmon from the study area. Interestingly, reproductive behaviors were only associated with pre-stress cortisol levels. For females, aggression and mate interaction time were reduced in individuals with elevated pre-stress cortisol concentrations. In males, a similar negative relationship between pre-stress cortisol concentration and mate interaction time was detected. The observed behavioral correlations are likely a factor of social status where dominant individuals, known to have higher reproductive success, are characterized by lower cortisol levels relative to subordinate conspecifics. Findings show both elevated pre-stress and stress-induced cortisol concentrations at arrival to the spawning grounds to be associated with reduced survival.     

Immune response of male barn swallows in relation to parental effort, corticosterone plasma levels, and sexual ornamentation

Life-history theory posits trade-offs between fitness components. Reproduction negatively affects physiology and immune systemfunctioning, and the effect of this form of stress may be mediatedby glucocorticosteroids. We manipulated brood size of barnswallows (Hirundo rustica) to study the effect of stress arisingfrom reproductive effort on corticosterone levels of males.We also measured T-cell—mediated immunocompetence by intradermally injecting birds with phytohemagglutinin, whichis mitogenic to T-lymphocytes. The results confirmed the predictionof a negative effect of parental effort on lymphoproliferativeresponse. We found no covariation between immune response andcorticosterone levels. Males with long tails, an ornament currentlyunder directional sexual selection, had a relatively large T-cell response to the mitogen, consistent with models of parasite-mediated sexual selection predicting higher levels of immune defensein highly ornamented males. In addition, males with large sexualornaments had relatively low corticosterone levels at the endof the parental period. These results can be reconciled withthe hypothesis proposing a trade-off between parental activitiesand adaptive immunity and suggest that highly ornamented malesare less exposed or less susceptible to stress arising fromparental effort.     

Fitness and behavioral correlates of pre-stress and stress-induced plasma cortisol titers in pink salmon (Oncorhynchus gorbuscha) upon arrival at spawning grounds

Semelparous Pacific salmon (Onchorynchus spp.) serve as an excellent model for examining the relationships between life history, behavior and individual variation in glucocorticoid (GC) stress hormone levels because reproductive behaviors are highly variable between individuals and failure to reproduce results in zero fitness. Pink salmon (O. gorbuscha) were intercepted upon arrival at the spawning grounds across three time periods. Pre-stress and stress-induced plasma cortisol concentrations were assessed in relation to behavior, longevity and reproductive success. Results revealed differences between sexes and with arrival time. The study period marked a year of high reproductive success and only nine females (12% of sample) failed to spawn. Female pre-spawn mortalities were characterized by significantly elevated stress-induced cortisol concentrations and decreased longevity as well as pre-stress cortisol above the normal range in pink salmon from the study area. Interestingly, reproductive behaviors were only associated with pre-stress cortisol levels. For females, aggression and mate interaction time were reduced in individuals with elevated pre-stress cortisol concentrations. In males, a similar negative relationship between pre-stress cortisol concentration and mate interaction time was detected. The observed behavioral correlations are likely a factor of social status where dominant individuals, known to have higher reproductive success, are characterized by lower cortisol levels relative to subordinate conspecifics. Findings show both elevated pre-stress and stress-induced cortisol concentrations at arrival to the spawning grounds to be associated with reduced survival.     

Behavioral,immunological, and hormonal responses associated with social change in rhesus monkeys (Macaca mulatta)

Twelve animals to be socially reorganized in a group of 49 animals were compared with ten animals in a socially stable group (n = 51) for reproductive hormones, cortisol concentrations, immune function, and behavioral patterns for a 6 week baseline and 16 week postreorganization period. Cortisol values, mitogen-induced lymphocyte blastogenesis, and rates of behavior reflected social events. Increased cortisols, increased noncontact aggression, and decreased mitogen response were associated with animal introductions. Increased cortisol concentration and decreased mitogen response correlated significantly only in animals removed from the group for trauma, and females successful at group membership exhibited lower cortisol concentrations. High-ranking animals in small stable groups exhibited significantly higher lymphocyte proliferation than middle- or low-ranking animals. While relative ranks established in small groups were maintained following reorganization, baseline cortisol values, immune measures, or male testosterone values did not predict success at group membership. © 1996 Wiley-Liss, Inc.     

First- and second-order sociality determine survival and reproduction in cooperative cichlids

Cooperative breeders serve as a model to study the evolution of cooperation, where costs and benefits of helping are typically scrutinized at the level of group membership. However, cooperation is often observed in multi-level social organizations involving interactions among individuals at various levels. Here, we argue that a full understanding of the adaptive value of cooperation and the evolution of complex social organization requires identifying the effect of different levels of social organization on direct and indirect fitness components. Our long-term field data show that in the cooperatively breeding, colonial cichlid fish Neolamprologus pulcher, both large group size and high colony density significantly raised group persistence. Neither group size nor density affected survival at the individual level, but they had interactive effects on reproductive output; large group size raised productivity when local population density was low, whereas in contrast, small groups were more productive at high densities. Fitness estimates of individually marked fish revealed indirect fitness benefits associated with staying in large groups. Inclusive fitness, however, was not significantly affected by group size, because the direct fitness component was not increased in larger groups. Together, our findings highlight that the reproductive output of groups may be affected in opposite directions by different levels of sociality, and that complex forms of sociality and costly cooperation may evolve in the absence of large indirect fitness benefits and the influence of kin selection.     

Endocrine phenotype,reproductive success and survival in the great tit,Parus major

A central goal in evolutionary ecology is to characterize and identify selection patterns on the optimal phenotype in different environments. Physiological traits, such as hormonal responses, provide important mechanisms by which individuals can adapt to fluctuating environmental conditions. It is therefore expected that selection shapes hormonal traits, but the strength and the direction of selection on plastic hormonal signals are still under investigation. Here, we determined whether, and in which way, selection is acting on the hormones corticosterone and prolactin by characterizing endocrine phenotypes and their relationship with fitness in free‐living great tits, Parus major. We quantified variation in circulating concentrations of baseline and stress‐induced corticosterone and in prolactin during the prebreeding (March) and the breeding season (May) for two consecutive years, and correlated these with reproductive success (yearly fledgling number) and overwinter survival in female and male individuals. In both years, individuals with high baseline corticosterone concentrations in March had the highest yearly fledgling numbers; while in May, individuals with low baseline corticosterone had the highest yearly reproductive success. Likewise, individuals that displayed strong seasonal plasticity in baseline corticosterone concentrations (high in March and low in May) had the highest reproductive success in each year. Prolactin concentrations were not related to reproductive success, but were positively correlated to the proximity to lay. Between‐year plasticity in stress‐induced corticosterone concentrations of males was related to yearly variation in food abundance, but not to overall reproductive success. These findings suggest that seasonally alternating directional selection is operating on baseline corticosterone concentrations in both sexes. The observed between‐year consistency in selection patterns indicates that a one‐time hormone sample in a given season can allow the prediction of individual fitness.     

No intra-locus sexual conflict over reproductive fitness or ageing in field crickets

Differences in the ways in which males and females maximize evolutionary fitness can lead to intra-locus sexual conflict in which genes delivering fitness benefits to one sex are costly when expressed in the other. Trade-offs between current reproductive effort and future reproduction and survival are fundamental to the evolutionary biology of ageing. This leads to the prediction that sex differences in the optimization of age-dependent reproductive effort may generate intra-locus sexual conflict over ageing rates. Here we test for intra-locus sexual conflict over age-dependent reproductive effort and longevity in the black field cricket, Teleogryllus commodus. Using a half-sib breeding design, we show that the most important components of male and female reproductive effort (male calling effort and the number of eggs laid by females) were positively genetically correlated, especially in early adulthood. However, the genetic relationships between longevity and reproductive effort were different for males and females, leading to low genetic covariation between male and female longevity. The apparent absence of intra-locus sexual conflict over ageing suggests that male and female longevity can evolve largely independently of one another.     

Social life-history response to individual immune challenge of workers of Bombus terrestris L.: a possible new cooperative phenomenon

Parasites typically reduce host survival or fecundity. To minimize fitness loss, hosts can make temporal adjustments of their reproductive effort. To date such plastic shifts of life‐history traits in response to parasitism are only known from solitary organisms where infected individuals can react by themselves. In the case of social insects, where brood care and reproductive effort is shared between reproductive individuals (typically the queen) and workers, adjustments of the reproductive effort would depend on collective decision‐making. We tested for this possibility by experimentally activating the immune response of individual workers in colonies of the bumblebee, Bombus terrestris L. This induction resulted, in combination with environmental conditions, in a reduction of fitness of the social unity (i.e. colony success, measured by number and biomass of offspring) and a collective response towards earlier reproduction. As both phenomena are expressed at the level of the colony, the result suggests that key elements of the use of immune defence have been maintained through the evolutionary transition to sociality.     

Competing pressures on populations: long-term dynamics of food availability,food quality,disease, stress and animal abundance

Despite strong links between sociality and fitness that ultimately affect the size of animal populations, the particular social and ecological factors that lead to endangerment are not well understood. Here, we synthesize approximately 25 years of data and present new analyses that highlight dynamics in forest composition, food availability, the nutritional quality of food, disease, physiological stress and population size of endangered folivorous red colobus monkeys (Procolobus rufomitratus). There is a decline in the quality of leaves 15 and 30 years following two previous studies in an undisturbed area of forest. The consumption of a low-quality diet in one month was associated with higher glucocorticoid levels in the subsequent month and stress levels in groups living in degraded forest fragments where diet was poor was more than twice those in forest groups. In contrast, forest composition has changed and when red colobus food availability was weighted by the protein-to-fibre ratio, which we have shown positively predicts folivore biomass, there was an increase in the availability of high-quality trees. Despite these changing social and ecological factors, the abundance of red colobus has remained stable, possibly through a combination of increasing group size and behavioural flexibility.