Divorce in the socially monogamous zebra finch: Hormonal mechanisms and reproductive consequences

Up to 80% of all bird species are socially monogamous. Divorce (switching partners) or pair disruption (due to the death of a partner) has been associated with decreased reproductive success, suggesting social monogamy is a strategy that may maximize fitness via coordination between partners. Previous studies have demonstrated the effects of divorce and pair disruption on immediate reproductive success. Here, we used a paired experimental design in the zebra finch (Taeniopygia guttata) to examine the hormonal mechanisms that modulate parental behavior and reproductive success in response to a partnership change (hereafter divorce). Specifically, we examined the effects of divorce on the avian stress hormone corticosterone (CORT) in both parents and nestlings, parental behaviors (incubation and nestling provisioning), prolactin (PRL), and reproductive success. We found that divorce resulted in delayed clutch initiation, reduced clutch mass, and an increase in nestling CORT response to a standardized stressor. These effects on reproductive investment and chick CORT response were not clearly determined by parental endocrine responses. Divorce had no effect on the level of parental CORT. PRL levels were highly correlated within a pair regardless of treatment, were negatively related to the investment that males made in incubation, and increased in experimental males as a result of pair disruption. This study demonstrates the fundamental impact which divorce has not only on reproduction, but also the physiological stress responses of offspring and suggests that in socially monogamous animals the maintenance of a stable partnership over time could be advantageous for long term fitness.     

Resource levels,reproduction and resistance to haematozoan infections

Compromise of immune function during reproduction may form a link between parental effort and the cost of reproduction, but the role of environmental variation in structuring intra-individual life-history trade-offs has been poorly investigated. We manipulated the need for parental effort in Eurasian kestrels, Falco tinnunculus, by food-supplementing broods for three nestling periods, during which the natural main food supply (voles) varied, and found that parental parasitaemia was inversely related to yearly vole densities. The level of parasitaemia in females was, however, reduced by food supplements. No effect on males was expected, as earlier work has shown that only females responded to the supplements by changing their behaviour. We show directly that the likelihood of female parasitaemia was diminished by spending less time in flight-hunting, which was related to reproduction during a good vole year, to our supplementary feeding, and to being mated to a male with high parental effort. Our results represent a novel direct benefit for females in resource - providing species, linked to female, as well as offspring, well-being, and they provide insight into why the appearance of reproductive costs may be linked to gender or environmental conditions.     

A possible link between parasite defence and residual reproduction

Life-history theory centres around trade-offs between current and future reproduction, but we have little understanding of how such trade-offs are mediated. We supplementary fed Ural owls (Strix uralensis) during the nestling period and quantified parents' current and future life-history components as well as their physiological health by monitoring haematocrit, leucocyte profile, intra- and extracellular blood parasites. Feeding led to reduced parental effort but did not improve offspring viability, male parasite defence, or parental survival. Intracellular leucocytozoan infection was reduced in fed females which lasted to the following year's reproductive season (carry-over effect), when fed females also laid larger and earlier clutches. Leucocytozoon infection therefore may mediate the life-history trade-off between current and residual reproduction in this species.     

Differential reproductive responses to stress reveal the role of life-history strategies within a species

Life-history strategies describe that ‘slow’- in contrast to ‘fast’-living species allocate resources cautiously towards reproduction to enhance survival. Recent evidence suggests that variation in strategies exists not only among species but also among populations of the same species. Here, we examined the effect of experimentally induced stress on resource allocation of breeding seabirds in two populations with contrasting life-history strategies: slow-living Pacific and fast-living Atlantic black-legged kittiwakes. We tested the hypothesis that reproductive responses in kittiwakes under stress reflect their life-history strategies. We predicted that in response to stress, Pacific kittiwakes reduce investment in reproduction compared with Atlantic kittiwakes. We exposed chick-rearing kittiwakes to a short-term (3-day) period of increased exogenous corticosterone (CORT), a hormone that is released during food shortages. We examined changes in baseline CORT levels, parental care and effects on offspring. We found that kittiwakes from the two populations invested differently in offspring when facing stress. In response to elevated CORT, Pacific kittiwakes reduced nest attendance and deserted offspring more readily than Atlantic kittiwakes. We observed lower chick growth, a higher stress response in offspring and lower reproductive success in response to CORT implantation in Pacific kittiwakes, whereas the opposite occurred in the Atlantic. Our findings support the hypothesis that life-history strategies predict short-term responses of individuals to stress within a species. We conclude that behaviour and physiology under stress are consistent with trade-off priorities as predicted by life-history theory. We encourage future studies to consider the pivotal role of life-history strategies when interpreting inter-population differences of animal responses to stressful environmental events.     

Coping with the extremes: stress physiology varies between winter and summer in breeding opportunists

Seasonal changes in stress steroid hormone secretions are thought to reflect investment in self-maintenance versus reproduction. The capricious conditions hypothesis (CCH) posits that reduced corticosterone (CORT) secretion during stress coincident with parental phases of breeding is necessary in harsh environments because a full response would otherwise trigger repeated nest abandonments. To test this hypothesis, we measured seasonal changes in stress physiology in free-living red crossbills (Loxia curvirostra), an opportunistically breeding songbird that regularly breeds in summer and winter. This species allows unique comparisons of breeding physiology under very different seasonal environmental conditions within locations. We found strong support for the CCH: red crossbills showed reduced CORT secretion only when in high reproductive condition in the winter, when compared with summer breeders and winter non-breeders. These data demonstrate that behavioural status and local environmental conditions interact to affect mechanisms underlying investment trade-offs, presumably in a way that maximizes lifetime reproductive success.     

The Roles of Stimuli from Young, Previous Breeding Experience, and Prolactin in Regulating Parental Behavior in Ring Doves (Streptopelia risoria)

In addition to stimulating crop "milk" formation in ring doves, prolactin (PRL) may promote the parental regurgitation behavior that transfers this "milk" to the young at the time of hatching. Although earlier studies suggest that previous breeding experience is an important modulator of PRL-induced parental regurgitation behavior in ring doves, the ways in which experience, hormones, and stimuli from young interact to promote parental behavior have not been well characterized in this species. In the first study, untreated, nonbreeding female doves with and without previous breeding experience were given 10 daily parental behavior tests (2 h/day) with a hungry 5- to 10-day-old foster squab. Experienced females exhibited a higher incidence of regurgitation behavior, defensive behavior, and crouching or sitting in the nest than did inexperienced females. In a second study, nonbreeding females were given 10 daily tests for parental behavior while they received sc injections of ovine PRL or vehicle. Prolactin reduced squab-directed aggression and increased the incidence of regurgitation feeding behavior of foster squabs in both experienced and inexperienced females. However, the average number of regurgitation feeding acts displayed by those PRL-treated females that showed the behavior was over eight times higher in experienced females than in inexperienced females. Previous experience also enhanced the stimulatory effects of PRL on defensive behavior and crouching or sitting in the nest. The parental behavior exhibited by nonbreeding, PRL-treated experienced females was qualitatively and quantitatively similar to that observed in normally breeding females during a single test with their own hungry 5- to 10-day-old squabs. These findings indicate that PRL and previous breeding experience both enhance the parental responsiveness of nonbreeding female doves and that under optimal hormonal, experiential, and squab exposure conditions, nonbreeding doves exhibit levels of parental activity that rival those of normally breeding parents.     

Individual heterogeneity in life-history trade-offs with age at first reproduction in capital breeding elephant seals

Recruitment age plays a key role in life-history evolution. Because individuals allocate limited resources among competing life-history functions, theory predicts trade-offs between current reproduction and future growth, survival and/or reproduction. Reproductive costs tend to vary with recruitment age, but may also be overridden by fixed individual differences leading to persistent demographic heterogeneity and positive covariation among demographic traits at the population level. We tested for evidence of intra- and inter-generational trade-offs and individual heterogeneity relating to age at first reproduction using three decades of detailed individual life-history data of 6,439 capital breeding female southern elephant seals. Contrary to the predictions from trade-off hypotheses, we found that recruitment at an early age was associated with higher population level survival and subsequent breeding probabilities. Nonetheless, a survival cost of first reproduction was evident at the population level, as first-time breeders always had lower survival probabilities than prebreeders and experienced breeders of the same age. However, models accounting for hidden persistent demographic heterogeneity revealed that the trade-off between first reproduction and survival was only expressed in “low quality” individuals, comprising 35% of the population. The short-term somatic costs associated with breeding at an early age had no effect on the ability of females to allocate resources to offspring in the next breeding season. Our results provide strong evidence for individual heterogeneity in the life-history trajectories of female elephant seals. By explicitly modeling hidden persistent demographic heterogeneity we show that individual heterogeneity governs the expression of trade-offs with first reproduction in elephant seals.     

Feather corticosterone of a nestling seabird reveals consequences of sex-specific parental investment

Offspring of long-lived species should face costs of parental trade-offs that vary with overall energetic demands encountered by parents during breeding. If sex differences exist in how parents make the trade-off, sex-specific differences may exist in the contribution of each parent to those costs. Adaptations of offspring facing such costs are not well understood, but the hormone corticosterone probably plays a role. We manipulated breeding effort in Cory's shearwaters (Calonectris diomedea) to increase costs to offspring and used an integrated measure of corticosterone from chick feathers to investigate how experimental variation in parental investment influences offspring physiology. Average foraging trip duration and foraging efficiency (FE) of breeding pairs were not related to chick corticosterone, but sex biases in FE were. Adult male investment was more strongly related to chick corticosterone than was female investment. Importantly, we show for the first time suppression of adrenocortical activity in nestling Procellariiform seabirds, and explain how our results indicate an adaptive mechanism invoked by chicks facing increased costs of parental trade-offs.     

Signaling stress? An analysis of phaeomelanin-based plumage color and individual corticosterone levels at two temporal scales in North American barn swallows, Hirundo rustica erythrogaster

Sexually selected traits confer greater reproductive benefits to individuals with more elaborate forms of the signal. However, whether these signals convey reliable information about the physiology underlying trait development remains unknown in many species. The steroid hormone corticosterone (CORT) mediates important physiological and behavioral processes during the vertebrate stress response, and CORT secretion itself can be modulated by melanocortins. Thus, sexually selected melanin-based plumage coloration could function as an honest signal of an individual's ability to respond to stressors. This hypothesis was tested in North American barn swallows, Hirundo rustica erythrogaster, where males with darker ventral plumage color exhibit higher phaeomelanin content and are more successful at reproduction. Because reproductive behavior occurs months after plumage signals are developed, we also addressed the potential temporal disconnect of physiological state during trait development and trait advertisement by analyzing three different measurements of CORT levels in adult males during the breeding season (trait advertisement) and in nestling males while they were growing their feathers (trait development). Variation in adult plumage color did not predict baseline or stress-induced CORT, or stress responsiveness. Likewise, there was no relationship between nestling plumage color and any of the CORT measurements, but heavier nestlings had significantly lower baseline CORT. Our finding that a predominantly phaeomelanin-based trait is unrelated to circulating CORT suggests that phaeomelanin and eumelanin signals may convey different physiological information, and highlights the need for further study on the biochemical links between the hypothalamic–pituitary–adrenal (HPA) axis and the production of different melanin-based pigments.     

Natural variation in a testosterone-mediated trade-off between mating effort and parental effort

Male birds frequently face a trade-off between acquiring mates and caring for offspring. Hormone manipulation studies indicate that testosterone often mediates this trade-off, increasing mating effort while decreasing parental effort. Little is known, however, about individual covariation between testosterone and relevant behavior on which selection might act. Using wild, male dark-eyed juncos (Junco hyemalis), we measured individual variation in testosterone levels before and after standardized injections of gonadotropin-releasing hormone (GnRH). The GnRH challenges have been shown to produce short-term testosterone increases that are similar to those produced naturally in response to social stimuli, repeatable in magnitude, and greater in males with more attractive ornaments. We correlated these testosterone increases with behavioral measures of mating and parental effort (aggressive response to a simulated territorial intrusion and nestling feeding, respectively). Males that showed higher postchallenge testosterone displayed more territorial behavior, and males that produced higher testosterone increases above initial levels displayed reduced parental behavior. Initial testosterone levels were positively but nonsignificantly correlated with aggression but did not predict parental behavior. These relationships suggest that natural variation in testosterone, specifically the production of short-term increases, may underlie individual variation in the mating effort/parental effort trade-off. We discuss the implications of these results for the evolution of hormonally mediated trade-offs.     

The costs of parental care: a meta-analysis of the trade-off between parental effort and survival in birds

A fundamental premise of life-history theory is that organisms that increase current reproductive investment suffer increased mortality. Possibly the most studied life-history phenotypic relationship is the trade-off between parental effort and survival. However, evidence supporting this trade-off is equivocal. Here, we conducted a meta-analysis to test the generality of this tenet. Using experimental studies that manipulated parental effort in birds, we show that (i) the effect of parental effort on survival was similar across species regardless of phylogeny; (ii) individuals that experienced reduced parental effort had similar survival probabilities than control individuals, regardless of sex; and (iii) males that experienced increased parental effort were less likely to survive than control males, whereas females that experienced increased effort were just as likely to survive as control females. Our results suggest that the trade-off between parental effort and survival is more complex than previously assumed. Finally, our study provides recommendations of unexplored avenues of future research into life-history trade-offs.     

A theoretical analysis of the energetic costs and consequences of parental care decisions

Should a parent care for its young or abandon them before they reach independence? We consider parental care behaviour as an adaptive decision, involving trade-offs between current and future reproduction. The condition of the parent is expected to influence these trade-offs. Using a dynamic programming model we explore how changes in the levels of energetic reserves, and time in the season, determine changes in parental care decisions. The novel feature of our model is that we have included the possibility of remating within the current breeding season in a consistent manner by explicitly modelling the behaviour of unmated animals. We show that there may be several fluctuations in the average duration of care during the breeding season. We also show that, because of the dependence of parental care behaviour on both the condition of the parent and time during the breeding season, changing some of the costs of care may increase the duration of care during one part of the season and decrease it at another. The model also shows that the conditions prevailing for animals with dependent offspring can affect the way in which an unmated animal behaves. For example, the behaviour of unmated animals may change to compensate (partly) for increases in the costs of raising offspring, which are produced at a later date (for example, by increasing the duration of foraging between breeding attempts). Overall, the model provides a good framework for understanding how various ecological and life-history variables should influence parental care behaviour during a breeding season.     

Clutch size and the costs of incubation in the house wren

Trade-offs in the allocation of finite resources among differentstages of a breeding attempt as well as between different reproductiveevents should shape the evolution of life-history traits. Toinvestigate the effects of incubation effort on within-broodand between-brood trade-offs in house wrens (Troglodytes aedon),we manipulated the clutch size that females incubated. We isolatedeffects of incubation by reversing the manipulation at hatchingto allow all parents to provision their natural brood sizes.Females that incubated enlarged clutches had longer incubationperiods than control females, both early and late in the season,suggesting that the experimental treatment increased incubationeffort. Contrary to predictions, however, increased incubationeffort did not adversely affect the allocation of effort tonestling provisioning. Rather, in the early season, but notin the late season, females that incubated enlarged clutchesappeared to allocate more effort to nestling provisioning, producingheavier and larger fledglings than control females. Althoughfemales with enlarged early-season clutches consequently lostmore mass than control females, this was likely an adaptiveresponse to reduce wing loading in anticipation of high provisioningdemands. There were no treatment-related differences in fledglingmass or size, or in female mass loss, in the late season. Thus,elevated incubation demands negatively affected a fitness-relatedtrait (duration of incubation) that may constrain clutch sizebut not the allocation of resources to subsequent stages ofthe same breeding event or to subsequent breeding events. Wesuggest that environmental conditions may mediate clutch-sizeeffects on trade-offs in allocation of resources between incubationand nestling provisioning.     

Reproductive Effort and Reproductive Values in Periodic Environments

Life-history theory concerns the optimal spread of reproduction over an organism's life span. In variable environments, there may be extrinsic differences between breeding periods within an organism's life, affecting both offspring and parent and giving rise to intergenerational trade-offs. Such trade-offs are often discussed in terms of reproductive value for parent and offspring. Here, we consider parental life-history optimization in response to varying offspring values of a population regulated by territoriality, where the quality of the environment varies periodically. Periods are interpreted as either within-year (seasonality) or between-years variation (cyclicity). The evolutionarily stable strategy in a general model with two-phased periodicity in the environment can generate either higher or lower effort in the more favorable of the two phases; hence knowing survival prospects of offspring does not suffice for predicting reproductive effort-the future of all descendants and the parent must be tracked. We also apply our method to data on the Ural owl Strix uralensis, a species preying on cyclically fluctuating voles. The observed dynamics are best predicted by assuming delayed reproductive costs and Type II functional response. Accounting for varying offspring values can lead to cases where both reproductive effort and recruitment of offspring are higher in the phase when voles are not maximally abundant, a pattern supported by our data.     

Ectoparasites and reproductive trade-offs in the barn swallow (Hirundo rustica)

Parents are predicted to trade offspring number and quality against the costs of reproduction. In altricial birds, parasites can mediate these costs because intensity of parasitism may increase with parental effort. In addition, parasites may mediate a trade-off between offspring number and quality because nestlings in large broods may have reduced anti-parasite immune defence. In this study, we experimentally analysed the effect of brood size on infestation by an ectoparasitic mite in nests of barn swallows (Hirundo rustica). Nests with an enlarged brood had larger prevalence and intensity of infestation than those with a reduced brood. Importantly, each nestling in enlarged broods was exposed to a larger number of mites, even when measured on a per nestling basis, than in reduced broods. Nestlings in enlarged broods had smaller body mass and T-cell-mediated immune response compared to reduced broods. T-cell-mediated immune response and feather growth were negatively correlated with per nestling intensity of infestation in enlarged but not in reduced broods. The results suggest that nestlings in enlarged broods have depressed immunity leading to larger per nestling mite infestation. Hence, exposure to parasites of offspring and parents increases with brood size, and parasitism can thus mediate trade-offs between reproduction and number and quality of the progeny in the barn swallow.     

Effects of sexual experience, season, and mating stimuli on endocrine concentrations in the adult ram.

Two behavioral trials were conducted to determine the endocrine response of cortisol (C), luteinizing hormone (LH), testosterone (T), prolactin (PRL), and growth hormone (GH) in adult rams during exposure to estrous ewes during the breeding and nonbreeding seasons. One-half of the rams in each season were sexually experienced (SE) and the remainder were sexually inexperienced (SI). All SE rams (100%) achieved at least one ejaculation, but only 33% (summer) and 67% (fall) SI rams achieved ejaculation. In the fall, mean C, T, and GH concentrations were elevated (P less than .001) compared to values measured in the summer, whereas LH and PRL levels were higher (P less than .01) in the summer. Overall levels of C, LH, T, and PRL were higher (P less than .05) in SE rams than in SI rams. Mean GH concentration was higher (P less than .10) in SI than in SE rams during restricted and complete access to estrous ewes. In general, LH, PRL, and GH responses were similar during restricted and complete access to females for both SE and SI rams. Cortisol levels were higher (P less than .06) during periods of mating and T levels were higher (P less than .001) during periods where activity was limited to courtship behavior (nasogenital investigation). Correlations of hormones to reproductive behaviors indicated that mounting and intromission were associated with elevations in C and PRL, whereas elevated LH and T tended to be associated with courtship behaviors. Correlations between GH and behaviors were inconsistent. However, there was an increased coincidence between time of female exposure and hormonal response that occurred in the fall; brief exposure to estrous ewes resulted in increases in concentrations of all hormones examined. The most consistent response was observed in sexually experienced rams during restricted access to females during the breeding season. These results provide new information on the effects of season and level of sexual experience upon hormonal and behavioral characteristics of the ram during mating activity.     

An evaluation of feather corticosterone as a biomarker of fitness and an ecologically relevant stressor during breeding in the wild

Feather corticosterone (CORT) levels are increasingly employed as biomarkers of environmental stress. However, it is unclear if feather CORT levels reflect stress and/or workload in the wild. We investigated whether feather CORT represents a biomarker of environmental stress and reproductive effort in tree swallows (Tachycineta bicolor). Specifically, we examined whether individual state and investment during reproduction could predict feather CORT levels in subsequently moulted feathers and whether those levels could predict future survival and reproductive success. Through a manipulation of flight cost during breeding, we also investigated whether an increase in stress level would be reflected in subsequently grown feathers, and whether those levels could predict future success. We found that CORT levels of feathers grown during moult did not (1) reflect past breeding experience (n = 29), (2) predict reproductive output (n = 18), or (3) respond to a manipulation of flight effort during reproduction (10 experimental, 14 control females). While higher feather CORT levels predicted higher return rate (a proxy for survival), they did so only in the manipulated group (n = 36), and this relationship was opposite to expected. Overall, our results add to the mixed literature reporting that feather CORT levels can be positively, negatively, or not related to proxies of within-season and longer-term fitness (i.e., carryover effects). In addition, our results indicate that CORT levels or disturbances experienced during one time (e.g., breeding) may not carry over to subsequent stages (e.g., moult). We, therefore, petition for directed research investigating whether feather CORT represents exposure to chronic stress in feathers grown during moult.     

Immediate and delayed effects of poor developmental conditions on growth and flight ability of juvenile mourning doves Zenaida macroura

Adaptations that minimize the effects of stress are important components of avian development and have a role in structuring the relationship between development and fitness. I examined the effect of experimental manipulations of developmental stress during the nestling and fledgling stages on weight gain, growth in structural size, and take‐off flight speed of juvenile mourning doves Zenaida macroura. Brood size was manipulated during the nestling stage (≤11 days) and feeding rates during the fledgling stage (13–25 days) using a full factorial design. Effects of nutritional stress differed between the two treatments and depended on the response that was measured and the age at which it was measured. Treatment effects on flight ability were delayed and were greater for the treatment during the nestling stage than during the fledgling stage. Immediate treatment effects were greater than delayed effects on weight and size. Young were able to minimize effects of stress on flight ability at early ages when they would be most vulnerable to predation. However, by 90 days birds from enlarged broods were slower and flight time at 90 days was negatively correlated with weight and size at 25 days. There was no evidence for a cost of compensatory growth after experimental treatments ended on flight ability at 90 days. Results suggest that the effects of stress occur in a hierarchical manner across phenotypic components and that at early ages flight ability is prioritized through phenotypic plasticity.     

Corticosterone manipulations alter morph-specific nestling provisioning behavior in male white-throated sparrows,Zonotrichia albicollis

In the polymorphic white-throated sparrow (Zonotrichia albicollis), tan-striped males provision nestlings at higher rates than do white-striped males. In a previous study, we found that tan-striped males had lower baseline corticosterone levels than white-striped males during the nestling stage. To determine if this variation in corticosterone influences morph-specific differences in nestling provisioning behavior, we used intraperitoneal osmotic pumps to increase baseline corticosterone levels in tan-striped males (TS CORT) and administer RU486, a glucocorticoid receptor antagonist, in white-striped males (WS RU486). These manipulations essentially reversed morph-specific nestling provisioning behavior in males. TS CORT males fed nestlings at lower rates than TS controls (vehicle-only implant), and at similar rates to WS controls (vehicle-only implant), while WS RU486 males fed nestlings at higher rates than WS controls, and at similar rates to TS controls. These results demonstrate that (1) increases in baseline corticosterone (i.e., below concentrations associated with the adrenocortical response to stress) can directly or indirectly inhibit nestling provisioning behavior, and (2) corticosterone influences morph-specific variation in parental behavior in male white-throated sparrows. This study contributes to the growing evidence that modulating baseline CORT mediates parental care and self-maintenance activities in birds, and thus may serve as a mechanism for balancing current reproductive success with survival.