Enlarged Broods Research Articles

Early developmental carry-over effects on exploratory behaviour and DNA methylation in wild great tits (Parus major).

Adverse, postnatal conditions experienced during development are known to induce lingering effects on morphology, behaviour, reproduction and survival. Despite the importance of early developmental stress for shaping the adult phenotype, it is largely unknown which molecular mechanisms allow for the induction and maintenance of such phenotypic effects once the early environmental conditions are released. Here we aimed to investigate whether lasting early developmental phenotypic changes are associated with post-developmental DNA methylation changes. We used a cross-foster and brood size experiment in great tit (Parus major) nestlings, which induced post-fledging effects on biometric measures and exploratory behaviour, a validated personality trait. We investigated whether these post-fledging effects are associated with DNA methylation levels of CpG sites in erythrocyte DNA. Individuals raised in enlarged broods caught up on their developmental delay after reaching independence and became more explorative as days since fledging passed, while the exploratory scores of individuals that were raised in reduced broods remained stable. Although we previously found that brood enlargement hardly affected the pre-fledging methylation levels, we found 420 CpG sites that were differentially methylated between fledged individuals that were raised in small versus large sized broods. A considerable number of the affected CpG sites were located in or near genes involved in metabolism, growth, behaviour and cognition. Since the biological functions of these genes line up with the observed post-fledging phenotypic effects of brood size, our results suggest that DNA methylation provides organisms the opportunity to modulate their condition once the environmental conditions allow it. In conclusion, this study shows that nutritional stress imposed by enlarged brood size during early development associates with variation in DNA methylation later in life. We propose that treatment-associated DNA methylation differences may arise in relation to pre- or post-fledging phenotypic changes, rather than that they are directly induced by the environment during early development.

Ectoparasite presence and brood size manipulation interact to accelerate telomere shortening in nestling jackdaws.

Early-life conditions impact fitness, but whether the combined effect of extrinsic stressors is additive or synergistic is not well known. This is a major knowledge gap because exposure to multiple stressors is frequent. Telomere dynamics may be instrumental when testing how stressors interact because many factors affect telomere shortening, and telomere shortening predicts survival. We evaluated the effect of manipulated brood size and natural infestation by the carnid fly Carnus hemapterus on nestling growth and telomere shortening of wild jackdaws (Corvus monedula). Telomere length, measured in blood using TRF, shortened on average by 264 bp, and on average, Carnus infection induced more telomere shortening. Further analyses showed that in enlarged broods, nestlings' telomeres shortened more when parasitized, while in reduced broods there was no effect of infection on telomere shortening. We conclude that there is a synergistic effect of number of siblings and Carnus infection on telomere shortening rate: blood-sucking parasites may negatively impact telomeres by increasing cell proliferation and/or physiological stress, and coping with infection may be less successful in enlarged broods with increased sibling competition. Larger nestlings had shorter telomeres independent of age, brood manipulation or infection. Growth was independent of infestation but in enlarged broods, nestlings were lighter at fledging. Our findings indicate that (i) evaluating consequences of early-life environmental conditions in isolation may not yield a full picture due to synergistic effects, and (ii) effects of environmental conditions may be cryptic, for example, on telomeres, with fitness consequences expressed beyond the temporal framework of the study.

Variation in oxidative status, but not structural and physiological development, associated with changing ontogenetic environments.

Despite the potential for temporally-dependent relationships between trait values and fitness (e.g., as juveniles approach life-stage transitions such as fledging), how developmental stage affects canalization (a measure of robustness to environmental variation) of morphological and physiological traits is rarely considered. To test the sensitivity of morphological and physiological traits to environmental variation in two developmental stages, we manipulated brood size at hatch in European starlings (Sturnus vulgaris) and cross-fostered chicks between enlarged and reduced broods approaching fledging. We measured body size (mass, tarsus, wing length) and physiological state (aerobic capacity, oxidative status) at asymptotic mass on day 15, then cross-fostered chicks between 'high' and 'low' quality environments and assessed the same traits again on day 20, after five days of pre-fledging mass recession. Chicks in reduced broods were heavier at asymptotic mass and had lower reactive oxygen metabolites than enlarged broods, while structural size, aerobic capacity, and antioxidant capacity were unaffected by experimental brood size. The observed canalization of structural and physiological traits during early development was maintained after cross-fostering, during late development. However, in contrast to early development, antioxidant capacity approaching fledging appeared sensitive to environmental conditions, as trajectories varied by cross-fostering treatment. Elevated reactive oxygen metabolites observed after early development in enlarged brood chicks were maintained after cross-fostering, suggesting canalized development in low-quality environments could produce oxidative costs that carry over between life-stages, even when conditions improve. These data reveal trait-specific relationships between environmental conditions and development and highlight how natal environment effects may vary by developmental stage.

When parents play favorites: brood demand shapes parental preference for offspring UV color.

Parents might initially produce more offspring than they might be able to raise. However, when offspring demand exceeds their parents´ rearing capacity, parents might shift care towards the offspring which yield greater fitness returns to achieve their optimal brood size via brood reduction. Such favoritism could rely on offspring signaling traits if these inform parents about offspring quality and hence about the pay-offs of their investment. Here we investigated whether favoritism of blue tit (Cyanistes caeruleus) parents for an offspring signal (i.e., ultraviolet (UV) plumage coloration) varies with brood demand. To test this, we experimentally blocked the UV reflectance of yellow breast feathers in half of the nestlings of each brood, and then we sequentially performed two opposing brood size manipulations to vary nestling demand below or above parental rearing capacity. In reduced broods, nestlings begged overall less intensely and gained more body mass, supporting that parental rearing capacities sufficed to satisfy brood demand. Moreover, in reduced broods, UV-blocked nestlings (i.e., low-quality offspring) were fed and prey-tested more often. Yet, they begged more than control nestlings, suggesting that they were perhaps treated differently by other family members or which they may exploit parental preferences beyond actual need (at least in reduced nests). Parents flexibly shifted their feeding rate and favoritism in response to short-term changes in family size, as there was no parental preference for enlarged broods. Such flexible parental feeding rules may allow parents to gain the upper hand in parent-offspring conflict. However, we did not find evidence that parental favoritism facilitated brood reduction, at least in conditions where demand was temporally enhanced.

Developmental stress does not induce genome-wide DNA methylation changes in wild great tit (Parus major) nestlings.

The environment experienced during early life is a crucial factor in the life of many organisms. This early life environment has been shown to have profound effects on morphology, physiology and fitness. However, the molecular mechanisms that mediate these effects are largely unknown, even though they are essential for our understanding of the processes that induce phenotypic variation in natural populations. DNA methylation is an epigenetic mechanism that has been suggested to explain such environmentally induced phenotypic changes early in life. To investigate whether DNA methylation changes are associated with experimentally induced early developmental effects, we cross-fostered great tit (Parus major) nestlings and manipulated their brood sizes in a natural study population. We assessed experimental brood size effects on pre-fledging biometry and behaviour. We linked this to genome-wide DNA methylation levels of CpG sites in erythrocyte DNA, using 122 individuals and an improved epiGBS2 laboratory protocol. Brood enlargement caused developmental stress and negatively affected nestling condition, predominantly during the second half of the breeding season, when conditions are harsher. Brood enlargement, however, affected nestling DNA methylation in only one CpG site and only if the hatch date was taken into account. In conclusion, this study shows that nutritional stress in enlarged broods does not associate with direct effects on genome-wide DNA methylation. Future studies should assess whether genome-wide DNA methylation variation may arise later in life as a consequence of phenotypic changes during early development.

Visitation rate, but not foraging range, responds to brood size manipulation in an aerial insectivore

Life history theory predicts that increased investment in current offspring decreases future fecundity or survival. Avian parental investment decisions have been studied either via brood size manipulation or direct manipulation of parental energetic costs (also known as handicapping). However, we have limited experimental data on the potential interactive effects of these manipulations on parent behavior. Additionally, we know little about how these manipulations affect spatial foraging behavior away from the nest. We simultaneously manipulated brood size and parental costs (via added weight in the form of a GPS tag) in wild female barn swallows (Hirundo rustica). We measured multiple aspects of parent behavior at and away from the nest while controlling for measures of weather conditions. We found no significant interactive effects of manipulated brood size and parental costs. Both sexes increased their visitation rate with brood size, but nestlings in enlarged broods grew significantly less post-brood size manipulation than those in reduced broods. Foraging range area was highly variable among GPS-tagged females but was unaffected by brood size. As such, increased visitation rate in response to brood size may be more energetically costly for far-ranging females. GPS-tagged females did not alter their visitation rate relative to un-tagged birds, but their mates had higher visitation rates. This suggests that GPS tagging may affect some unmeasured aspect of female behavior, such as prey delivery. Our findings indicate that investigation of foraging tactics alongside visitation rate is critical to understanding parental investment and the benefits and costs of reproduction.Significance statementAvian parental investment decisions have been studied by either brood size manipulation or direct manipulation of parental costs, but rarely both simultaneously. We simultaneously manipulated brood size and parental costs (via addition of a GPS tag) in a wild avian system, allowing us to examine interactive effects of these manipulations. Additionally, studies of parental investment often examine behaviors at the nest, but measurements of parental care behavior away from the nest are rare. Our study is unique in that we measured multiple aspects of parental care, including spatial foraging behavior tracked with GPS tags. We found no interactive effects of manipulated brood size and parental costs on visitation rate or nestling growth, and spatial foraging behavior of females was individually variable. Documenting foraging tactics alongside visitation rate is critical to understanding parental investment because the same visitation rate might be more costly for far-ranging females.

First Records of Conspecific Brood Parasitism in Two Species of Small Passerines: Lesser Whitethroat and Common Linnet

We provide the first records of possible conspecific brood parasitism in the lesser whitethroat Sylvia curruca and the common linnet Linaria cannabina, two species of small passerines. In 2018 we found two unusually large clutches, one for each species (8 and 9 eggs, respectively), both containing two distinct egg morphs differing in coloration. Further detailed analysis of egg morphology and brood phenology (in the whitethroat) suggested that the eggs in each nest had been laid by different females. Surprisingly, two seemingly full sized clutches were laid in both nests, a pattern that is unusual in conspecific brood parasitism in passerines, whose nests are typically parasitized with single eggs. Alternatives to conspecific brood parasitism are therefore discussed. We argue that traditional field-based methods, when carefully used, may be sufficient to document brood parasitism recorded during occasional observations. We finally conclude that enlarged broods, resulting from conspecific brood parasitism, are probably more frequent than expected, but they may be often overlooked.

Triparental care in the collared flycatcher (Ficedula albicollis): Cooperation of two females with a cuckolded male in rearing a brood.

Certain predominant forms of mating and parental care systems are assumed in several model species among birds, but the opportunistic and apparently infrequent variations of “family structures” may often remain hidden due to methodological limitations with regard to genetic or behavioral observations. One of the intensively studied model species, the collared flycatcher (Ficedula albicollis), is usually characterized by social monogamy with polyterritorial, facultative social polygyny, and frequent extrapair mating and extrapair paternity. During a brood‐size manipulation experiment, we observed two females and a male delivering food at an enlarged brood. A combination of breeding phenology data (egg laying and hatching date), behavioral data (feeding rates) from video recordings at 10 days of nestling age, and microsatellite genotyping for maternity and paternity suggests a situation of an unrelated female helping a pair in chick rearing. Such observations highlight the relevance of using traditional techniques and genetic analyses together to assess the parental roles within a population, which becomes more important where individuals may dynamically switch from their main and presupposed roles according to the actual environmental conditions.

Phenotypic differences among wild passerine nestlings in relation to early-life rearing environment

Subtle changes in stress physiology during critical developmental stages have been linked to long-term fitness; however, the biological processes and phenotypic responses to early-life rearing environments, such as anthropogenic land use conditions, have not been fully evaluated in insectivorous birds. We manipulated Tree Swallow (Tachycineta bicolor (Vieillot, 1808)) brood sizes at sites with contrasting agricultural land use to assess phenotypic changes in body condition and genetic and physiological biomarkers of stress during the sensitive nestling growth phase. We predicted that nestling swallows raised on cropland-dominated sites, especially those in enlarged broods, would have lower body condition, shorter telomeres, and higher feather corticosterone than nestlings raised in smaller broods at grassland sites. Body condition was highest among nestlings raised in reduced broods but was unrelated to land use. Telomere lengths tended to be shorter in nestlings from enlarged broods and at cropland sites. Corticosterone was not related to any factor. Locally abundant insect populations associated with wetlands may have dampened the effects and (or) parent swallows assumed higher costs of reproduction rather than passing these costs to nestlings. Results suggest that food or other environmental stressors could reduce fledgling survival via telomere shortening; a hypothesis that requires further investigation due to its potential importance to population viability in multiple declining aerial insectivore species.

Effects of maternal exposure to a bacterial antigen and altered post-hatching rearing conditions on avian offspring behaviour

The early-life environment plays a crucial role in shaping morphological, physiological, and behavioural traits, with potential long-term consequences for fitness. Indeed, a set of factors experienced by offspring during prenatal and early post-natal development has been recognised to affect behavioural trait expression in later life. Several studies have shown that in birds, nutritional and social rearing conditions and maternal and/or neonatal immunisations may profoundly determine the development and establishment of behaviour in offspring. To our knowledge, no research has examined whether and how the interaction between immune-mediated maternal effects and post-hatching rearing conditions affects offspring behaviour. Here, we studied the effects of maternal exposure to a bacterial antigen and altered brood size on docility, breathing rate, and aggression in the offspring of great tit, Parus major. We used a 2 × 2 design to investigate the interactive effects of maternal immunisation and brood size manipulation on offspring behavioural development. We found no such interactive effect on offspring behaviour, although we observed it regarding to offspring body mass and tarsus length. Maternal immunisation itself did not affect offspring behaviour. However, we demonstrated that the offspring breathing rate and level of aggression were affected by brood size manipulation. Both breathing rate and aggression in offspring reared in enlarged broods were lower than those in offspring reared in non-manipulated broods. Our study did not confirm earlier reports that immune-mediated maternal effects modulate offspring behavioural development, but we showed that brood size during rearing might indeed be a factor that affects offspring behaviour.Significance statementThe early environment experienced by offspring constitutes a significant source of developmental plasticity, which may profoundly affect the establishment of their behavioural traits. Food availability, social conditions, and maternal or offspring infection are crucial factors shaping various behavioural traits in birds. However, there remains a lack of studies emphasising the potential interactive effects of early-life conditions on behavioural trait development in natural bird populations. Here, to our knowledge for the first time, we experimentally examined how maternal immunisation and altered post-hatching rearing conditions interact to determine the behaviour of fledged offspring. We found that maternal treatment and brood size manipulation interactively affected offspring body mass and tarsus length, but this interaction had no effect on offspring behaviour. Our findings suggest that different mechanisms may underlie the development of morphological and behavioural traits.

Oxidative Stress Experienced during Early Development Influences the Offspring Phenotype.

AbstractOxidative stress (OS) experienced early in life can affect an individual's phenotype. However, its consequences for the next generation remain largely unexplored. We manipulated the OS level endured by zebra finches (Taeniopygia guttata) during their development by transitorily inhibiting the synthesis of the key antioxidant glutathione ("early-high-OS"). The offspring of these birds and control parents were cross fostered at hatching to enlarge or reduce its brood size. Independent of parents' early-life OS levels, the chicks raised in enlarged broods showed lower erythrocyte glutathione levels, revealing glutathione sensitivity to environmental conditions. Control biological mothers produced females, not males, that attained a higher body mass when raised in a benign environment (i.e., the reduced brood). In contrast, biological mothers exposed to early-life OS produced heavier males, not females, when allocated in reduced broods. Early-life OS also affected the parental rearing capacity because 12-day-old nestlings raised by a foster pair with both early-high-OS members grew shorter legs (tarsus) than chicks from other groups. The results indicate that environmental conditions during development can affect early glutathione levels, which may in turn influence the next generation through both pre- and postnatal parental effects. The results also demonstrate that early-life OS can constrain the offspring phenotype.

Increased allocation to reproduction reduces future competitive ability in a burying beetle.

The existence of a trade-off between current and future reproduction is a fundamental prediction of life history theory. Support for this prediction comes from brood size manipulations, showing that caring for enlarged broods often reduces the parent's future survival or fecundity. However, in many species, individuals must invest in competing for the resources required for future reproduction. Thus, a neglected aspect of this trade-off is that increased allocation to current reproduction may reduce an individual's future competitive ability. We tested this prediction in the burying beetle, Nicrophorus vespilloides, a species where parents care for their offspring and where there is fierce competition for resources used for breeding. We manipulated reproductive effort by providing females with either a small brood of 10 larvae or a large brood of 40 larvae and compared the ability of these females, and virgin females that had no prior access to a carcass, to compete for a second carcass against a virgin competitor. We found that increased allocation to current reproduction reduced future competitive ability, as females that had cared for a small brood were more successful when competing for a second carcass against a virgin competitor than females that had cared for a large brood. In addition, the costs of reproduction were offset by the benefits of feeding from the carcass during an initial breeding attempt, as females that had cared for a small brood were better competitors than virgin females that had no prior access to a carcass, whilst females that had cared for a large brood were similar in competitive ability to virgin females. Our results add to our understanding of the trade-off between current and future reproduction by showing that this trade-off can manifest through differences in future competitive ability and that direct benefits of reproduction can offset some of these costs.

Experimentally increased brood size accelerates actuarial senescence and increases subsequent reproductive effort in a wild bird population.

The assumption that reproductive effort decreases somatic state, accelerating ageing, is central to our understanding of life‐history variation. Maximal reproductive effort early in life is predicted to be maladaptive by accelerating ageing disproportionally, decreasing fitness.Optimality theory predicts that reproductive effort is restrained early in life to balance the fitness contribution of reproduction against the survival cost induced by the reproductive effort. When adaptive, the level of reproductive restraint is predicted to be inversely linked to the remaining life expectancy, potentially resulting in a terminal effort in the last period of reproduction.Experimental tests of the reproductive restraint hypothesis require manipulation of somatic state and subsequent investigation of reproductive effort and residual life span. To our knowledge the available evidence remains inconclusive, and hence reproductive restraint remains to be demonstrated.We modulated somatic state through a lifelong brood size manipulation in wild jackdaws and measured its consequences for age‐dependent mortality and reproductive success.The assumption that lifelong increased brood size reduced somatic state was supported: Birds rearing enlarged broods showed subsequent increased rate of actuarial senescence, resulting in reduced residual life span.The treatment induced a reproductive response in later seasons: Egg volume and nestling survival were higher in subsequent seasons in the increased versus reduced broods' treatment group. We detected these increases in egg volume and nestling survival despite the expectation that in the absence of a change in reproductive effort, the reduced somatic state indicated by the increased mortality rate would result in lower reproductive output. This leads us to conclude that the higher reproductive success we observed was the result of higher reproductive effort.Our findings show that reproductive effort negatively covaries with remaining life expectancy, supporting optimality theory and confirming reproductive restraint as a key factor underpinning life‐history variation.

A fixed agreement-consequences of brood size manipulation on alternation in blue tits.

Recent studies have proposed that conditional cooperation may resolve sexual conflict over the amount of care provided by each parent. Such conditional cooperation may allow parents to equalize their investment by alternating their provisioning visits. This alternated pattern of male and female visits, that is, alternation, is thought to stimulate each other’s investment leading to higher levels of provisioning and potential benefits for offspring development. However, experimental studies testing the role of alternation as an adaptive parental strategy to negotiate the level of investment are still absent. Therefore, we manipulated blue tit (Cyanistes caeruleus) parents by temporarily changing their brood sizes to induce changes in demand and thus visit rates. Parents were expected to visit more—assuming that prey sizes were constant—and alternate at higher levels when confronted with an enlarged brood given the greater potential for sexual conflict. In contrast, in reduced broods visit rates and alternation may become lower due to the smaller investment that is needed for reduced broods. We show that the level of alternation did not differ in response to the manipulated brood sizes, despite a directional change in visit rates for enlarged and reduced broods as expected. Nestlings did not benefit from high levels of alternation as no effects on nestling mass gain were present in either of the different manipulations. These findings indicate that alternation does not serve as a mechanism to motivate each other to feed at higher rates. Parents hence appeared to be inflexible in their level of alternation. We therefore suggest that the level of alternation might reflect a fixed agreement about the relative investment by each of the caring parents.

Early-life social environment predicts social network position in wild zebra finches.

Early-life experience can fundamentally shape individual life-history trajectories. Previous research has suggested that exposure to stress during development causes differences in social behaviour later in life. In captivity, juvenile zebra finches exposed to elevated corticosterone levels were less socially choosy and more central in their social networks when compared to untreated siblings. These differences extended to other aspects of social life, with 'stress-exposed' juveniles switching social learning strategies and juvenile males less faithfully learning their father's song. However, while this body of research suggests that the impacts of early-life stress could be profound, it remains unknown whether such effects are strong enough to be expressed under natural conditions. Here, we collected data on social associations of zebra finches in the Australian desert after experimentally manipulating brood sizes. Juveniles from enlarged broods experienced heightened sibling competition, and we predicted that they would express similar patterns of social associations to stress-treated birds in the captive study by having more, but less differentiated, relationships. We show striking support for the suggested consequences of developmental stress on social network positions, with our data from the wild replicating the same results in 9 out of 10 predictions previously tested in captivity. Chicks raised in enlarged broods foraged with greater numbers of conspecifics but were less 'choosy' and more central in the social network. Our results confirm that the natural range of variation in early-life experience can be sufficient to predict individuals' social trajectories and support theory highlighting the potential importance of developmental conditions on behaviour.

The effect of pre-laying maternal immunization on offspring growth and immunity differs across experimentally altered postnatal rearing conditions in a wild songbird

BackgroundPrenatal antibody transfer is an immune-mediated maternal effect by which females can shape postnatal offspring resistance to pathogens and parasites. Maternal antibodies passed on to offspring provide primary protection to neonates against diverse pathogenic antigens, but they may also affect offspring growth and influence the development of an offspring’s own immune response. The effects of maternal antibodies on offspring performance commonly require that the disease environment experienced by a mother prior to breeding matches the environment encountered by her offspring after hatching/birth. However, other circumstances, like postnatal rearing conditions that affect offspring food availability, may also determine the effects of maternal antibodies on offspring growth and immunity. To date, knowledge about how prenatal immune-mediated maternal effects interact with various postnatal rearing conditions to affect offspring development and phenotype in wild bird population remains elusive. Here we experimentally studied the interactive effects of pre-laying maternal immunization with a bacterial antigen (lipopolysaccharide) and post-hatching rearing conditions, altered by brood size manipulation, on offspring growth and humoral immunity of wild great tits (Parus major).ResultsWe found that maternal immunization and brood size manipulation interactively affected the growth and specific humoral immune response of avian offspring. Among nestlings reared in enlarged broods, only those that originated from immunized mothers grew better and were heavier at fledging stage compared to those that originated from non-immunized mothers. In contrast, no such effects were observed among nestlings reared in non-manipulated (control) broods. Moreover, offspring of immunized females had a stronger humoral immune response to lipopolysaccharide during postnatal development than offspring of non-immunized females, but only when the nestling was reared in control broods.ConclusionsThis study demonstrates that offspring development and their ability to cope with pathogens after hatching are driven by mutual influences of pathogen-induced prenatal maternal effects and post-hatching rearing conditions. Our findings suggest that immune-mediated maternal effects may have context-dependent influences on offspring growth and immune function, related to the postnatal environmental conditions experienced by the progeny.

Experimental brood enlargement differentially influences the magnitude of the corticosterone stress response in closely related, co‐occurring songbirds

Abstract Rearing environments can shape offspring phenotype across taxa, yet little is known about how brood size influences hypothalamic–pituitary axis functioning, whether its expression trades off with growth, and the degree to which these relationships vary between species. We evaluated how brood size influenced nestling physiological (glucocorticoids) and somatic traits (growth), and the extent to which their relationship differed between two closely related, sympatric songbirds when experiencing identical rearing environments. Specifically, we used a cross‐fostering approach to alter brood size and create an experimental gradient of nestmate competition, and then tested whether experimentally manipulated brood sizes resulted in nestlings with altered concentrations of corticosterone and whether corticosterone responses traded off with growth. Nestlings of both species experienced elevated concentrations of baseline and stressor‐induced corticosterone when raised in enlarged broods, relative to control and reduced broods, but neither measurement was found to trade off with growth or be linked to survival to fledging. In contrast, we found divergence in the magnitude of the corticosterone stress response between species across all brood treatments, with greater stressor‐induced corticosterone concentrations found in the Violet‐green Swallow (Tachycineta thalassina) relative to the closely related Tree Swallow (T. bicolor). Our study demonstrated that brood size can lead to changes in offspring corticosterone concentrations in swallows and that nestlings of sympatric species, even those that are closely related and ecologically similar, can diverge in their corticosterone stress response when experiencing identical rearing conditions. We conclude that corticosterone appears to play a key role for balancing energetic demands that arise in the face of nestmate competition in Tachycineta swallows and that elevated concentrations of corticosterone may enhance offspring survival during challenging environmental conditions, such as when brood competition is strong. A plain language summary is available for this article.

Carry-over effects of brood size on morphology, reproduction, and lifespan in barn swallows

Early life ecological conditions have well-documented short-term effects on offspring phenotype and survival, but the extent to which these effect carry-over into adulthood is much less known. Yet, unveiling such carry-over effects is essential to understand the evolution of parental life-history strategies. In altricial birds, the number of brood mates can affect competition regime and other nest ecological conditions, whose effects may be at least partly expressed in adulthood. We either increased or decreased the size of barn swallow (Hirundo rustica) broods and analyzed the consequences of brood size manipulation on morphological feather traits, breeding performance, and lifespan of the offspring when adult. Upon recruitment (age 1 year), individuals from enlarged broods had shorter wings, later reproduction, and lower breeding output than those from reduced broods. The negative effect of brood enlargement on wing length persisted at age 2 years. Recruits from enlarged broods had longer lifespan but the proportion of nestlings that were recruited tended to be smaller for enlarged compared to reduced broods. Hence, large brood size had negative phenotypic effects in adulthood. Our results also suggest that stronger viability selection on offspring from enlarged broods results in differential survival of highly viable offspring that express longer life expectancy when adult and/or that smaller reproductive effort of 1-year-old offspring from enlarged broods boosts their life expectancy, potentially compensating for reduced annual fecundity. Number of brood mates can thus have carry-over effects on fitness components, including lifespan, which should be incorporated in the analysis of complex reproductive trade-offs. Ecological conditions in early life can affect survival and physical conditions but the extent to which these effects extend into adulthood is largely unknown. In this experiment, we altered the size of barn swallow broods and monitored the consequences of the change in competition regime in the brood of rearing in adulthood. When adult, individuals that had been reared in an enlarged brood had shorter wings and decreased breeding success. However, individuals from enlarged broods lived longer, possibly because only high-quality individuals from such broods survived through the first year of life. Thus, rearing conditions have important long-term effects, implying that parents have to optimize the number of offspring they decide to produce.

Oxidative physiology of reproduction in a passerine bird: a field experiment

Organisms face resource trade-offs to support their parental effort and survival. The life-history oxidative stress hypothesis predicts that an individual’s redox state modulates the trade-off between current and residual fitness, but this has seldom been tested experimentally in non-captive organisms. In this study, we manipulated the brood size in breeding pairs of barn swallows (Hirundo rustica) and found that females tending enlarged broods had increased levels of plasma oxidative damage (malondialdehyde concentration). This effect, however, was not accompanied by either a depletion, or defensive upregulation in antioxidants (glutathione, total antioxidant capacity, and uric acid) that may explain the increase in oxidative damage. Brood size manipulation and the level of plasma oxidative damage during brood rearing are not translated into decreased annual return rate, which does not support the oxidative stress hypothesis of life-history trade-offs. On the contrary, we found that female’s oxidative damage and total glutathione levels, an important intracellular non-enzymatic antioxidant measured at hatching decreased and correlated positively, respectively with annual return rate, suggesting that oxidative condition at hatching might be a more important contributor to fitness than the oxidative physiology measured during chick rearing. We also show that individual traits and ecological factors, such as the timing of breeding and the abundance of blood-sucking nest mites, correlated with the redox state of males and females during brood care. Oxidative stress is one of the most important physiological costs of reproduction and thus a key modulator of life-history trade-offs. In this study, we manipulated reproductive effort in breeding pairs of barn swallows and found that females tending enlarged broods had increased levels of plasma oxidative damage. This effect, however, was not accompanied by either a depletion or upregulation in antioxidants that may explain the increase in oxidative damage. We found that female’s oxidative damage and total glutathione levels measured at hatching decreased and correlated positively, respectively with annual return rate, suggesting that oxidative condition at hatching might be an important contributor to fitness. Brood size manipulation and the increased levels of plasma oxidative damage are not translated into decreased annual return rate; thus, our results support the hypothesis that reproductive effort has a transient effect on oxidative physiology.

The use of the nest for parental roosting and thermal consequences of the nest for nestlings and parents

At temperate latitudes, altricial birds and their nestlings need to handle night temperatures well below thermoneutrality during the breeding season. Thus, energy costs of thermoregulation might constrain nestling growth, and low nocturnal temperatures might require resources that parents could otherwise have invested into nestlings during the day. To manipulate parental work rate, we performed brood size manipulations in breeding marsh tits (Poecile palustris). Nest box temperatures were always well above ambient temperature and increased with increasing brood size. In line with predictions, a large majority of females (but no males) made use of this benign environment for roosting. Furthermore, females tending enlarged broods, thereby having to work harder during the day, reduced their body temperature at night. This might have reduced nocturnal energy expenditure. Our finding that a higher proportion of enlarged, as compared to control, females continued to use the nest box as roosting sites even after a simulated predation event despite increased vulnerability to predation, further highlighting the need for energy conservation in this group. High nest box attendance and reduced body temperature in brood-reduced females may indicate that these females prioritised self-maintenance by initiating other costly physiological adjustments, e.g. moult, when relieved from parental work. We suggest that the energy demand for defending homeothermy is an element of the general trade-off between current and future reproduction, i.e. between daytime investment in food provisioning and the potential short- and long-term costs of a reduction in body temperature and increased predation risk.Significance statementEven during summer at temperate latitudes, breeding birds need to use energy to maintain stable body temperature. Parents, thus, need to enter the night with sufficient body reserves to cover energy requirements for thermoregulation. As these resources could be used for feeding nestling during the day, adaptations to reduce the cost of thermoregulation would be selected for. We performed brood size manipulations, thereby increasing the need for nestling provisioning in marsh tits (Parus palustris). We found that females typically spent the night in the thermally benign environment of the nest box together with their brood. Females working hard during the day continued to roost in the nest box during the night despite an increase in the perceived risk of nest predation. Furthermore, these females reduced their body temperature at night, thereby reducing the gradient between ambient and body temperature, further reducing the cost of thermoregulation.