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Maternal glucocorticoid levels during incubation predict breeding success, but not reproductive investment, in a free-ranging bird.

ABSTRACT: The hormone corticosterone (CORT) has been hypothesized to be linked with fitness, but the directionality of the relationship is unclear. The 'CORT-fitness hypothesis' proposes that high levels of CORT arise from challenging environmental conditions, resulting in lower reproductive success (a negative relationship). In contrast, the CORT-adaptation hypothesis suggests that, during energetically demanding periods, CORT will mediate physiological or behavioral changes that result in increased reproductive investment and success (a positive relationship). During two breeding seasons, we experimentally manipulated circulating CORT levels in female tree swallows (Tachycineta bicolor) prior to egg laying, and measured subsequent reproductive effort, breeding success, and maternal survival. When females were recaptured during egg incubation and again during the nestling stage, the CORT levels were similar among individuals in each treatment group, and maternal treatment had no effect on indices of fitness. By considering variation among females, we found support for the CORT-adaptation hypothesis; there was a significant positive relationship between CORT levels during incubation and hatching and fledging success. During the nestling stage CORT levels were unrelated to any measure of investment or success. Within the environmental context of our study, relationships between maternal glucocorticoid levels and indices of fitness vary across reproductive stages.

SUBMITTER: Fischer D

PROVIDER: S-EPMC7595688 | biostudies-literature | 2020 Oct

REPOSITORIES: biostudies-literature

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Maternal glucocorticoid levels during incubation predict breeding success, but not reproductive investment, in a free-ranging bird.

Fischer Devin D Marrotte Robby R RR Chin Eunice H EH Coulson Smolly S Burness Gary G

Biology open 20201019 10

The hormone corticosterone (CORT) has been hypothesized to be linked with fitness, but the directionality of the relationship is unclear. The 'CORT-fitness hypothesis' proposes that high levels of CORT arise from challenging environmental conditions, resulting in lower reproductive success (a negative relationship). In contrast, the CORT-adaptation hypothesis suggests that, during energetically demanding periods, CORT will mediate physiological or behavioral changes that result in increased repr ...[more]

PMID: 33077551

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Project description:Body condition may predict individual fitness because those in better condition have more resources to allocate towards improving their fitness. However, the hypothesis that condition indices are meaningful proxies for fitness has been questioned. Here, we ask if intraspecific variation in condition indices predicts annual reproductive success and survival. We monitored a population of Neochmia phaeton (crimson finch), a sedentary, tropical passerine, for reproductive success and survival over four breeding seasons, and sampled them for commonly used condition indices: mass adjusted for body size, muscle and fat scores, packed cell volume, hemoglobin concentration, total plasma protein, and heterophil to lymphocyte ratio. Our study population is well suited for this research because individuals forage in common areas and do not hold territories such that variation in condition between individuals is not confounded by differences in habitat quality. Furthermore, we controlled for factors that are known to impact condition indices in our study population (e.g., breeding stage) such that we assessed individual condition relative to others in the same context. Condition indices that reflect energy reserves predicted both the probability of an individual fledging young and the number of young produced that survived to independence, but only during some years. Those that were relatively heavy for their body size produced about three times more independent young compared to light individuals. That energy reserves are a meaningful predictor of reproductive success in a sedentary passerine supports the idea that energy reserves are at least sometimes predictors of fitness. However, hematological indices failed to predict reproductive success and none of the indices predicted survival. Therefore, some but not all condition indices may be informative, but because we found that most indices did not predict any component of fitness, we question the ubiquitous interpretation of condition indices as surrogates for individual quality and fitness.

Project description:BackgroundDemonstrating the impact that parents have on the fitness of their children is a crucial step towards understanding how parental investment has affected human evolution. Parents not only transfer genes to their children, they also influence their environments. By analyzing reproductive patterns within and between different categories of close relatives, this study provides insight into the genetic and environmental effects that parents have on the fitness of their offspring.MethodsWe use data spanning over two centuries from an exceptionally accurate Icelandic genealogy, Íslendingabók, to analyze the relationship between the fertility rates of close relatives. Also, using genetic data, we determine narrow sense heritability estimates (h2) to further explore the genetic impact on lifetime reproductive success. Finally, we construct four simulations to model the expected contribution of genes and resources on reproductive success.ResultsThe relationship between the reproduction of all full sibling pairs was significant and positive across all birth decades (r = 0.19) while the reproductive relationship between parents and offspring was often negative across many decades and undetectable overall (r = 0.00) (Fig. 1 and Table 1). Meanwhile, genetic data among 8,456 pairs of full siblings revealed a narrow sense heritability estimate (h2) of 0.00 for lifetime reproductive success. A resources model (following the rule that resources are transmitted from parents to children, distributed equally among siblings, and are the only factor affecting reproductive success) revealed a similar trend: a negative relationship between parent and offspring reproduction (r = - 0.35) but a positive relationship among full siblings (r = 0.28). The relationship between parent and offspring lifetime reproductive success (LRS) and full sibling LRS was strongly and positively correlated across time (r = 0.799, p < 0.001). Similarly, the LRS among full siblings was positively correlated with both the LRS among half siblings (r = 0.532, p = 0.011) and the relationship between the LRS of aunts and uncles with their nieces and nephews (r = 0.438, p = 0.042).DiscussionWe show that an individual's lifetime reproductive success is best predicted by the reproduction of their full and half siblings, but not their parents, grandparents or aunts and uncles. Because all siblings share at least one parent, we believe parental investment has had an important impact on fitness. Overall, these results indicate that direct parental investment, but not genes, is likely to have had an important and persistent impact on lifetime reproductive success across more than two centuries of Icelandic history.

Dataset Information

Maternal glucocorticoid levels during incubation predict breeding success, but not reproductive investment, in a free-ranging bird.

Publications

Maternal glucocorticoid levels during incubation predict breeding success, but not reproductive investment, in a free-ranging bird.

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