Full lifetime perspectives on the costs and benefits of lay date variation in tree swallows

Animals must balance various costs and benefits when deciding when to breed. The costs and benefits of breeding at different times have received much attention, but most studies have been limited to investigating short-term season-to-season fitness effects. However, breeding early, versus late, in a season may influence lifetime fitness over many years, trading off in complex ways across the breeder?s lifepan. In this study, we examined the complete life histories of 867 female tree swallows (Tachycineta bicolor) breeding in Ithaca, New York, between 2002 and 2016. Earlier breeders outperformed later breeders in short-term measures of reproductive output and offspring quality. Though there were weak indications that females paid long-term future survival costs for breeding early, lifetime fledgling output was markedly higher overall in early-breeding birds. Importantly, older females breeding later in the season did not experience compensating life-history advantages that suggested an alternative equal-fitness breeding strategy. Rather, most or all of the swallows appear to be breeding as early as they can, and differences in lay dates appear to be determined primarily by differences in individual quality or condition. Lay date had a significant repeatability across breeding attempts by the same female, and the first lay date of females fledged in our population was strongly influenced by the first lay date of their mothers, indicating the potential for ongoing selection on lay date. By examining performance over the entire lifespan of a large number of individuals, we were able to clarify the relationship between timing of breeding and fitness and gain new insight into the sources of variability in this important life history trait.Fil: Winkler, David Ward. Cornell University; Estados UnidosFil: Hallinger, Kelly K.. Cornell University; Estados UnidosFil: Pegan, Teresa M.. University of Michigan; Estados UnidosFil: Taff, Conor C.. Cornell University; Estados UnidosFil: Verhoeven, Mo A.. University of Groningen; Países BajosFil: Van Oordt, David Chang. Cornell University; Estados UnidosFil: Stager, Maria. University of Montana; Estados UnidosFil: Uehling, Jennifer J.. Cornell University; Estados UnidosFil: Vitousek, Maren N.. Cornell University; Estados UnidosFil: Andersen, Michael J.. University of New Mexico; Estados UnidosFil: Ardia, Daniel R.. Franklin & Marshall College; Estados UnidosFil: Belmaker, Amos. Tel Aviv University; IsraelFil: Ferretti, Valentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: Forsman, Anna M.. University Of Central Florida; Estados UnidosFil: Gaul, Jennifer R.. International High School at La Guardia Community College; Estados UnidosFil: Llambias, Paulo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto Argentino de Investigaciones de las Zonas Áridas. Provincia de Mendoza. Instituto Argentino de Investigaciones de las Zonas Áridas. Universidad Nacional de Cuyo. Instituto Argentino de Investigaciones de las Zonas Áridas; ArgentinaFil: Orzechowski, Sophia C.. Harvard University; Estados UnidosFil: Shipley, Ryan. Max Planck Institute For Animal Behavior; AlemaniaFil: Wilson, Maya. Virginia Polytechnic Institute. Department Of Geological Sciences; Estados UnidosFil: Yoon, Hyun Seok. University of Tennessee; Estados Unido

Hormones and Fitness: Evidence for Trade-Offs in Glucocorticoid Regulation Across Contexts

Glucocorticoid hormones are important regulators of metabolic processes, and of the behavioral and physiological responses to stressors. Within-population variation in circulating glucocorticoids has been linked with both reproductive success and survival, but the presence and direction of relationships vary. Although conceptual models suggest the potential for interactions between glucocorticoid secretion under acute stress and non-acute stress contexts to influence phenotype and fitness, very little is known about the presence or implications of such interactions. Here we use a large data set from breeding tree swallows (Tachycineta bicolor; n = 215 adults) to test the predictors of reproductive success and annual survival probability in females and males over a four-year period. Across years and life history stages, glucocorticoids predicted fitness in female tree swallows. Under challenging conditions, females that maintained low baseline corticosterone levels during incubation had higher reproductive success. During the nestling provisioning period, interactions between baseline glucocorticoids and the stress response suggest that females may face trade-offs in the regulation of glucocorticoids across contexts. Reproductive success was highest among females that maintained low baseline glucocorticoids coupled with a strong acute stress response, and among females with high baseline glucocorticoids and a weak acute stress response. Females with low or high glucocorticoid levels across contexts (baseline and acute stress) fledged fewer young. Glucocorticoid levels did not predict fledging success in males. None of the models of annual survival probability in females received strong support; model comparisons suggested weak negative effects of stress responsiveness during nestling provisioning, and positive effects of body condition and age, on survival. Male survival probability was not predicted by breeding phenotype. Within and across years the glucocorticoid stress response was individually repeatable; across-year repeatability was particularly high during the nestling provisioning period. Both measures of the acute stress response—circulating stress-induced corticosterone levels and their stress-induced increase—showed similar repeatability, but baseline corticosterone was not repeatable within or across years. Overall, our results suggest that taking into account the potential for individual differences in glucocorticoid trait expression in one context to influence optimal endocrine expression in other contexts could be important for understanding the evolution of endocrine systems

Data from: Heritable variation in circulating glucocorticoids and endocrine flexibility in a free-living songbird

Phenotypic flexibility is a central way that organisms cope with challenging and changing environments. As endocrine signals mediate many phenotypic traits, heritable variation in hormone levels, or their context-dependent flexibility, could present an important target for selection. Several studies have estimated the heritability of circulating glucocorticoid levels under acute stress conditions, but little is known about the potential for either baseline hormone levels or rapid endocrine flexibility to evolve. Here we assessed the potential for selection to operate on the elevation (circulating hormone levels) and flexibility of glucocorticoid reaction norms to acute restraint stress. Multivariate animal models revealed low but significant heritability in baseline (h2=0.13-0.14) and stress-induced glucocorticoids (h2=0.18), and moderate heritability in glucocorticoid flexibility in response to acute stress (h2=0.38) in free-living juvenile tree swallows (Tachycineta bicolor; n=408). Baseline glucocorticoids were not genetically correlated with either stress-induced glucocorticoids or glucocorticoid flexibility. These findings indicate that baseline glucocorticoids and the acute stress response are distinct traits that can be independently shaped by selection. Microevolutionary changes that influence the expression or flexibility of these endocrine mediators of phenotype may be an important way that populations adapt to changing environments and novel threats

Is there a context-dependent advantage of extra-pair mating in Tree Swallows?

The "good-genes'' hypothesis to explain female extra-pairmating states that females benefit from this behavior by acquiring better genes for their offspring. Despite extensive research, results are mixed, and the predictions of the good-genes hypothesis have beenmet in fewer than half of published papers. One possible explanation for this lack of consensus is that the benefits of extra-pair copulation are context-dependent. Here we use chick size, the probability of fledging, and telomeres, the protective caps of chromosomes, as markers for individual quality. Telomere length (TelL) integrates across many stressors and covaries with probability of survival and reproductive success. To test whether benefits to extra-pair (EP) matings are context-dependent we look at the telomere length of extra-pair and within-pair offspring (EPO and WPO, respectively) reared either in experimentally enlarged broods or in broods left at their natural size. We predicted that EPO would have longer telomeres than WPO, and that this difference would be more pronounced among nutritionally limited nestlings reared in enlarged broods. Contrary to our predictions, EP status did not predict chick size or TelL of nestlings reared in either treatment group. EPO from enlarged broods had a higher probability of fledging than similarly reared WPO, but this effect was only seen after a separate analysis per group and not in the full model. Even though these results give mixed support to the good-genes hypothesis they also highlight the difficulty in choosing the proper metric and context.Cornell Lab of Ornithology; Department of Ecology and Evolutionary Biology; Andrew W. Mellon Student research Grants at Cornell University; Sigma Xi; Society for Integrative and comparative Biology; American Ornithologists' Union; NSF LTREB grants [DEB-0717021, DEB 1242573]This item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at [email protected]

Pedigree and phenotypic data

Data on genetic parentage, rearing environment, and phenotype of nestling tree swallow

Table1.PDF

<p>Glucocorticoid hormones are important regulators of metabolic processes, and of the behavioral and physiological responses to stressors. Within-population variation in circulating glucocorticoids has been linked with both reproductive success and survival, but the presence and direction of relationships vary. Although conceptual models suggest the potential for interactions between glucocorticoid secretion under acute stress and non-acute stress contexts to influence phenotype and fitness, very little is known about the presence or implications of such interactions. Here we use a large data set from breeding tree swallows (Tachycineta bicolor; n = 215 adults) to test the predictors of reproductive success and annual survival probability in females and males over a four-year period. Across years and life history stages, glucocorticoids predicted fitness in female tree swallows. Under challenging conditions, females that maintained low baseline corticosterone levels during incubation had higher reproductive success. During the nestling provisioning period, interactions between baseline glucocorticoids and the stress response suggest that females may face trade-offs in the regulation of glucocorticoids across contexts. Reproductive success was highest among females that maintained low baseline glucocorticoids coupled with a strong acute stress response, and among females with high baseline glucocorticoids and a weak acute stress response. Females with low or high glucocorticoid levels across contexts (baseline and acute stress) fledged fewer young. Glucocorticoid levels did not predict fledging success in males. None of the models of annual survival probability in females received strong support; model comparisons suggested weak negative effects of stress responsiveness during nestling provisioning, and positive effects of body condition and age, on survival. Male survival probability was not predicted by breeding phenotype. Within and across years the glucocorticoid stress response was individually repeatable; across-year repeatability was particularly high during the nestling provisioning period. Both measures of the acute stress response—circulating stress-induced corticosterone levels and their stress-induced increase—showed similar repeatability, but baseline corticosterone was not repeatable within or across years. Overall, our results suggest that taking into account the potential for individual differences in glucocorticoid trait expression in one context to influence optimal endocrine expression in other contexts could be important for understanding the evolution of endocrine systems.</p