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Studying the causes of phenotypic variation, and their consequences, is fundamental to understand organismal adaptation. Phenotypic variation among individuals can occur in response to environmental signals, such as the phenotypic variation observed in the offspring as a result from the environment provided by the parents (Mousseau and Fox 1998). That is, parents can shape their offspring’s phenotype not only through the genes they pass on, but also by influencing the environment they provide (Mousseau and Fox 1998, Uller 2008, 2012). Maternal effects are now recognized to have an important effect on determining offspring phenotype (meta-analysis by Moore et al. 2019, Yin et al. 2019, Sánchez-Tójar et al. 2020). Maternal effects are widely distributed in nature, from plants to invertebrates and vertebrates, and they can exert their effects at different stages in the life-cycle. Prenatal maternal effects are particularly important because the environmental conditions provided by the mother are likely to lead to irreversible and long-lasting modifications in the developing embryo; potentially influencing offspring survival and reproductive outcome (Mousseau and Fox 1998, Groothuis et al. 2005, Marshall and Uller 2007, Uller 2008). Egg-laying species have been key models to understand the adaptive significance of maternal effects. Compared to most mammalian species, embryos develop outside the mother’s body, which narrows the time frame during which mothers can directly influence the environment they provide to their offspring. In egg-laying species, mothers can influence this prenatal environment via the deposition of compounds into the egg (e.g., McCormick 1999, Lovern and Wade 2001, Weiss et al. 2011, Valcu et al. 2019, Mentesana et al. 2019). In 1993, Hubert Schwabl reported for the first time the presence of maternal hormones in bird eggs. These findings were then extended to other egg-laying vertebrate taxa, such as fish, reptiles and amphibians, thus bringing attention to the role of egg hormones as mediators of maternal effects (e.g., review by Groothuis et al. 2005). Since then, the field has seen a surge of experimental studies showing how hormones, especially steroid hormones and particularly in the yolk, can shape offspring growth, behavior (e.g., begging, aggression, boldness, activity, food competitiveness), and physiological systems (e.g., immune system, HPA axis, oxidative condition; Lovern and Wade 2001, Groothuis et al. 2005, Gil 2008, von Engelhardt and Groothuis 2011). Yet, whether such phenotypic changes translate into fitness benefits for the mother, the father or the offspring has remained under debate (reviewed by Bebbington and Groothuis 2021), especially for free-living populations (e.g., Tschirren et al. 2014). Hence, almost 30 years after the discovery of maternal hormones in eggs it is still unclear how evolutionary relevant hormone-mediated maternal effects are. The aim of this study is to use an evidence synthesis approach to test to what extent prenatal maternal egg hormone deposition relates to fitness in free-living populations of egg-laying vertebrates. In particular, we will analyze the relationships between androgens (i.e., androstenedione, 5-α dihydrotestosterone and testosterone), estradiol, progesterone, glucocorticoids and thyroid hormones (i.e., T3 and T4) present in the egg and maternal and offspring fitness proxies (Fig. 1). The relationship between egg hormones and offspring fitness has received most of the attention, while the relationship between egg hormones and maternal fitness has been less studied. Hence, we will test specific hypotheses for the former relationship (egg hormones & offspring fitness; see next section) and do an explorative analysis for the latter one (egg hormones & maternal fitness; see section 24). Lastly, the relationship between maternal egg components and paternal fitness proxies will not be considered in this study given that information on this link is remarkably lacking (reviewed by Bebbington and Groothuis 2021).

Additional file 2. Results of linear models and linear mixed-effects models to test for relationships between yolk composition and fitness traits.

Additional file 3. Results of linear mixed-effects models to test for relationships between yolk composition and phenotypic traits on nestling day 6.

Additional file 7. Linear models testing for differences in yolk composition between years.

Additional file 1. Principal component analysis of 31 yolk components measured in the fourth egg of 69 wild great tit clutches.

Additional file 6. Methods.

Additional file 5. Results of linear mixed-effects models used to test for relationships between nestling tarsus length on days 6 and 12 and survival in the nest.

Additional file 4. Results of linear mixed-effects models to test for relationships between yolk composition and phenotypic traits on day 12.

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. published