Fitness consequences of physiological responses to environmental variation in wild great tits

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2020
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Mentesana, Lucia
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Environments change continuously. Fluctuations in temperature, rainfall, and food availability, can be predictable on the long term, but unpredictable within short time frames. Additionally, fluctuations in the environment can now occur unpredictably and with increasing frequency and duration because of human activities. Changes in an organism’s environment can be challenging because they destabilize its homeostatic processes. Understanding how organisms respond to these homeostatic disturbances, and if and how they can cope with them has become critically important and urgently needed in the light of climate change and increasing human disturbance. Physiological signals serve to integrate environmental and genomic information, and transmit that information within the organism to mediate a phenotypic response. Physiological traits, which refer to aspects of organism functioning, like nutrition, metabolism, thermal relationships, endocrine responses, and changes in immune parameters are important mechanisms to cope with fluctuating environments. If these traits directly affect an organism’s fitness and have transgenerational effects that also affect the phenotype and survival of its offspring, then they are potentially important drivers for evolutionary processes in response to rapidly changing environments. The general aim of my thesis was to determine the fitness consequences of physiological responses to environmental variation. For this, I studied how the physiological response of parents to environmental conditions relates to patterns of reproductive investment, reproductive success and offspring fitness in a wild population of great tits (Parus major). I first studied how the physiological response of parents to environmental conditions relates to their reproductive success (chapter 2). I tested the hypothesis that physiological traits covary and predict fitness primarily under challenging environmental conditions. I used data on six physiological traits (i.e., glucocorticoids: baseline and stress-induced concentrations, oxidative status: pro-oxidants, dietary and enzymatic antioxidant concentrations, and body condition) and fitness proxies (i.e., fledgling number and mass) collected over two breeding seasons that significantly differed in environmental conditions. Chapter 2 shows that physiological traits do not covary but they predict, in a sex-specific way, reproductive success when environmental conditions are challenging. In the year with low ambient temperature and high cumulated rainfall, females in a better oxidative condition produced more and heavier fledglings, while males with high body condition fledged more offspring. In males, but not in females, high baseline and low stress-induced glucocorticoid concentrations were also positively and negatively related to high fledgling mass. Chapter 2 suggests that glucocorticoids, oxidative state and body condition might be important mediators to successfully cope with challenging environmental circumstances. The way in which mothers cope with environmental changes can affect their reproductive investment, by altering the resources mothers pass on to their developing embryos. In egg laying species, females deposit hormones, nutrients and immune components into their eggs. In birds, the patterns of yolk deposition of these components along the laying sequence vary across and within species, but the processes that shape female yolk deposition are not yet fully understood. In chapter 3, I used a statistical approach based on repeated measures to study female yolk deposition along the laying sequence at both the population and among-female levels. I used data on the concentrations of 11 yolk components including steroid hormones, antioxidants, and fatty acids, which I determined in the eggs of 11 entire clutches collected during one breeding season. Chapter 3 shows that variation in yolk deposition at a population level is underpinned by different individual patterns, and that these individual patterns may be shaped by both genetic and environmental components. It also confirms that the method of analyzing the fourth egg from a nest is a suitable way to estimate clutch-level yolk composition in studies of wild populations. Further, chapter 3 shows that mothers concomitantly secret steroid hormones, antioxidants and fatty acids into their egg yolks, suggesting that maternal substances work interactively within an egg to influence the phenotype of the offspring. In chapter 4, I built on the knowledge obtained in the previous chapter to test for interactive effects of yolk components on offspring phenotypic traits (i.e., oxidative state and body condition) and fitness proxies (i.e., hatchling number, fledgling number, mass and tarsus). I used data on concentrations of 31 yolk components measured in the fourth egg from 69 nests collected over two breeding seasons. Chapter 4 shows that offspring phenotypes relate to the interactions among the yolk components that females deposit into their eggs. This chapter also provides the first evidence for a relationship between yolk fatty acids and hatchling and fledgling number in a wild population; thus, suggesting that these yolk components, which are strongly influenced by the quantity and quality of the food consumed by mothers during egg laying, can greatly influence an individual’s fitness. In summary, chapter 3 and 4 show that the way mothers cope with environmental changes affects the resources they transfer to their eggs, which interact to shape phenotypic and fitness traits in the offspring. With this thesis I thus contributed empirically to the study of how changes in physiological traits due to environmental variation relate to fitness and phenotypic responses. My thesis shows that birds from a free-living population can successfully cope with unpredictable environmental disturbances during the breeding season, such as low temperatures and high cumulated rainfall, and suggests that glucocorticoids, oxidative state and body condition are important mediators to do so. However, female reproductive success might be negatively affected via transgenerational effects on offspring fitness if fluctuations in environmental conditions cause a decrease in food supply, and therefore a decrease in essential yolk components transferred by the mothers into the eggs. Overall, my thesis shows that the interactions between parents and offspring fitness are an important point to include in studies aiming to understand if and how organisms cope with environmental changes.

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570 Biowissenschaften, Biologie
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fitness, physiological traits, wild birds, maternal effects, glucocorticoids, oxidative status, antioxidants, fatty acids, yolk, egg
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undefined / . - undefined, undefined
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ISO 690MENTESANA, Lucia, 2020. Fitness consequences of physiological responses to environmental variation in wild great tits [Dissertation]. Konstanz: University of Konstanz
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@phdthesis{Mentesana2020Fitne-51458,
  year={2020},
  title={Fitness consequences of physiological responses to environmental variation in wild great tits},
  author={Mentesana, Lucia},
  address={Konstanz},
  school={Universität Konstanz}
}
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Physiological traits, which refer to aspects of organism functioning, like nutrition, metabolism, thermal relationships, endocrine responses, and changes in immune parameters are important mechanisms to cope with fluctuating environments. If these traits directly affect an organism’s fitness and have transgenerational effects that also affect the phenotype and survival of its offspring, then they are potentially important drivers for evolutionary processes in response to rapidly changing environments. The general aim of my thesis was to determine the fitness consequences of physiological responses to environmental variation. For this, I studied how the physiological response of parents to environmental conditions relates to patterns of reproductive investment, reproductive success and offspring fitness in a wild population of great tits (Parus major). I first studied how the physiological response of parents to environmental conditions relates to their reproductive success (chapter 2). I tested the hypothesis that physiological traits covary and predict fitness primarily under challenging environmental conditions. I used data on six physiological traits (i.e., glucocorticoids: baseline and stress-induced concentrations, oxidative status: pro-oxidants, dietary and enzymatic antioxidant concentrations, and body condition) and fitness proxies (i.e., fledgling number and mass) collected over two breeding seasons that significantly differed in environmental conditions. Chapter 2 shows that physiological traits do not covary but they predict, in a sex-specific way, reproductive success when environmental conditions are challenging.  In the year with low ambient temperature and high cumulated rainfall, females in a better oxidative condition produced more and heavier fledglings, while males with high body condition fledged more offspring. In males, but not in females, high baseline and low stress-induced glucocorticoid concentrations were also positively and negatively related to high fledgling mass. Chapter 2 suggests that glucocorticoids, oxidative state and body condition might be important mediators to successfully cope with challenging environmental circumstances. The way in which mothers cope with environmental changes can affect their reproductive investment, by altering the resources mothers pass on to their developing embryos. In egg laying species, females deposit hormones, nutrients and immune components into their eggs. In birds, the patterns of yolk deposition of these components along the laying sequence vary across and within species, but the processes that shape female yolk deposition are not yet fully understood. In chapter 3, I used a statistical approach based on repeated measures to study female yolk deposition along the laying sequence at both the population and among-female levels. I used data on the concentrations of 11 yolk components including steroid hormones, antioxidants, and fatty acids, which I determined in the eggs of 11 entire clutches collected during one breeding season. Chapter 3 shows that variation in yolk deposition at a population level is underpinned by different individual patterns, and that these individual patterns may be shaped by both genetic and environmental components. It also confirms that the method of analyzing the fourth egg from a nest is a suitable way to estimate clutch-level yolk composition in studies of wild populations. Further, chapter 3 shows that mothers concomitantly secret steroid hormones, antioxidants and fatty acids into their egg yolks, suggesting that maternal substances work interactively within an egg to influence the phenotype of the offspring. In chapter 4, I built on the knowledge obtained in the previous chapter to test for interactive effects of yolk components on offspring phenotypic traits (i.e., oxidative state and body condition) and fitness proxies (i.e., hatchling number, fledgling number, mass and tarsus). I used data on concentrations of 31 yolk components measured in the fourth egg from 69 nests collected over two breeding seasons. Chapter 4 shows that offspring phenotypes relate to the interactions among the yolk components that females deposit into their eggs. This chapter also provides the first evidence for a relationship between yolk fatty acids and hatchling and fledgling number in a wild population; thus, suggesting that these yolk components, which are strongly influenced by the quantity and quality of the food consumed by mothers during egg laying, can greatly influence an individual’s fitness. In summary, chapter 3 and 4 show that the way mothers cope with environmental changes affects the resources they transfer to their eggs, which interact to shape phenotypic and fitness traits in the offspring. With this thesis I thus contributed empirically to the study of how changes in physiological traits due to environmental variation relate to fitness and phenotypic responses. My thesis shows that birds from a free-living population can successfully cope with unpredictable environmental disturbances during the breeding season, such as low temperatures and high cumulated rainfall, and suggests that glucocorticoids, oxidative state and body condition are important mediators to do so. However, female reproductive success might be negatively affected via transgenerational effects on offspring fitness if fluctuations in environmental conditions cause a decrease in food supply, and therefore a decrease in essential yolk components transferred by the mothers into the eggs. 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September 14, 2020
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Konstanz, Univ., Diss., 2020
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