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An organism’s response to its environment is largely determined by changes in the energy supplied by aerobic mitochondrial metabolism via adenosine triphosphate (ATP) production. ATP is especially important under energy-demanding conditions, such as during rapid growth. It is currently poorly understood how environmental factors influence energy metabolism and mitochondrial functioning, but recent studies suggest the role of thyroid hormones (TH). TH are key regulators of growth and metabolism and can be flexibly adjusted to environmental conditions, such as environmental temperature or food availability. To test whether TH enhancement is causally linked to mitochondrial function and growth, we provided TH orally at physiological concentrations during the main growth phase in zebra finch (Taeniopygia guttata) nestlings reared in a challenging environment. TH treatment accelerated maximal mitochondrial working capacity—a trait that reflects mitochondrial ATP production, without affecting growth. To our knowledge, this is the first study to characterize the regulation of mitochondria by TH during development in a semi-naturalistic context and to address implications for fitness-related traits, such as growth.

Abstract Offspring phenotype at birth is determined by its genotype and the prenatal environment including exposure to maternal hormones. Variation in both maternal glucocorticoids and thyroid hormones can affect offspring phenotype, but the underlying molecular mechanisms, especially those contributing to long‐lasting effects, remain unclear. Epigenetic changes (such as DNA methylation) have been postulated as mediators of long‐lasting effects of early‐life environment. In this study, we determined the effects of elevated prenatal glucocorticoid and thyroid hormones on handling stress response (breath rate) as well as DNA methylation and gene expression of glucocorticoid receptor (GR) and thyroid hormone receptor (THR) in great tits (Parus major). Eggs were injected before incubation onset with corticosterone (the main avian glucocorticoid) and/or thyroid hormones (thyroxine and triiodothyronine) to simulate variation in maternal hormone deposition. Breath rate during handling and gene expression of GR and THR were evaluated 14 days after hatching. Methylation status of GR and THR genes was analyzed from the longitudinal blood cells sampled 7 and 14 days after hatching, as well as the following autumn. Elevated prenatal corticosterone level significantly increased the breath rate during handling, indicating an enhanced metabolic stress response. Prenatal corticosterone manipulation had CpG‐site‐specific effects on DNA methylation at the GR putative promoter region, while it did not significantly affect GR gene expression. GR expression was negatively associated with earlier hatching date and chick size. THR methylation or expression did not exhibit any significant relationship with the hormonal treatments or the examined covariates, suggesting that TH signaling may be more robust due to its crucial role in development. This study provides some support to the hypothesis suggesting that maternal corticosterone may influence offspring metabolic stress response via epigenetic alterations, yet their possible adaptive role in optimizing offspring phenotype to the prevailing conditions, context‐dependency, and the underlying molecular interplay needs further research.

Abstract Background The gut microbiome forms at an early stage, yet data on the environmental factors influencing the development of wild avian microbiomes is limited. As the gut microbiome is a vital part of organismal health, it is important to understand how it may connect to host performance. The early studies with wild gut microbiome have shown that the rearing environment may be of importance in gut microbiome formation, yet the results vary across taxa, and the effects of specific environmental factors have not been characterized. Here, wild great tit (Parus major) broods were manipulated to either reduce or enlarge the original brood soon after hatching. We investigated if brood size was associated with nestling bacterial gut microbiome, and whether gut microbiome diversity predicted survival. Fecal samples were collected at mid-nestling stage and sequenced with the 16S rRNA gene amplicon sequencing, and nestling growth and survival were measured. Results Gut microbiome diversity showed high variation between individuals, but this variation was not significantly explained by brood size or body mass. Additionally, we did not find a significant effect of brood size on body mass or gut microbiome composition. We also demonstrated that early handling had no impact on nestling performance or gut microbiome. Furthermore, we found no significant association between gut microbiome diversity and short-term (survival to fledging) or mid-term (apparent juvenile) survival. Conclusions We found no clear association between early-life environment, offspring condition and gut microbiome. This suggests that brood size is not a significantly contributing factor to great tit nestling condition, and that other environmental and genetic factors may be more strongly linked to offspring condition and gut microbiome. Future studies should expand into other early-life environmental factors e.g., diet composition and quality, and parental influences.

Anthropogenic pollution is known to negatively influence an organism’s physiology, behaviour, and fitness. Epigenetic regulation, such as DNA methylation, has been hypothesized as a potential mechanism to mediate such effects, yet studies in wild species are lacking. We first investigated the effects of early-life exposure to the heavy metal lead (Pb) on DNA methylation levels in a wild population of great tits (Parus major), by experimentally exposing nestlings to Pb at environmentally relevant levels. Secondly, we compared nestling DNA methylation from a population exposed to long-term heavy metal pollution (close to a copper smelter), where birds suffer from pollution-related decrease in food quality, and a control population. For both comparisons, the analysis of about one million CpGs covering most of the annotated genes revealed that pollution-related changes in DNA methylation were not genome wide, but enriched for genes underlying developmental processes. However, the results were not consistent when using binomial or beta binomial regression highlighting the difficulty of modelling variance in CpGs. Our study indicates that post-natal anthropogenic heavy metal exposure can affect methylation levels of development related genes in a wild bird population.

In fish, the lipid resources of the female form a link between the environment and progeny, contributing to the contents of the egg yolk. Variation of the environmental conditions is therefore expected to affect the egg quality via maternal pathways, reflecting the female’s response to the environmental factors before spawning. We investigated the content of lipids and thyroid hormones in the ovary and eggs of the Baltic herring during 1988–2019, when salinity of the Baltic Sea first declined and then stabilized to a lower level, and winters varied between severe and mild. The total lipid resources of spawning females decreased by 40–50% during the study, and the ovarian lipid concentration followed this trend resulting in a decrease of the lipid content of eggs. The concentration of thyroid hormones in the ovary suggested a hormonal response in females to salinity and winter temperature and was observable also in the content of thyroid hormones in the eggs. A change in the egg lipid content took place approximately around 1998 (SE ± 3 years) suggesting that in declining salinity, egg quality was associated with salinity and intrinsic factors in the female, i.e., fecundity and amount of lipids deposited into the ovary. However, during the period of stable salinity, egg quality was mainly limited by the female’s lipid resources. As also the body size of the females decreased over the years, it is suggested that small body size can be a key phenotypic trait to reduce the environmental impact on egg quality in variable environmental conditions.

Maternal thyroid hormones (THs) are known to be crucial in embryonic development in humans, but their influence on other, especially wild, animals remains poorly understood. So far, the studies that experimentally investigated the consequences of maternal THs focused on short-term effects, while early organisational effects with long-term consequences, as shown for other prenatal hormones, could also be expected. In this study, we aimed at investigating both the short- and long-term effects of prenatal THs in a bird species, the Japanese quail Coturnix japonica. We experimentally elevated yolk TH content (the prohormone T4, and its active metabolite T3, as well as a combination of both hormones). We analysed hatching success, embryonic development, offspring growth and oxidative stress as well as their potential organisational effects on reproduction, moult and oxidative stress in adulthood. We found that eggs injected with T4 had a higher hatching success compared with control eggs, suggesting conversion of T4 into T3 by the embryo. We detected no evidence for other short-term or long-term effects of yolk THs. These results suggest that yolk THs are important in the embryonic stage of precocial birds, but other short- and long-term consequences remain unclear. Research on maternal THs will greatly benefit from studies investigating how embryos use and respond to this maternal signalling. Long-term studies on prenatal THs in other taxa in the wild are needed for a better understanding of this hormone-mediated maternal pathway.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Bird feces are commonly used as a proxy for measuring dietary metal exposure levels in wild populations. Our study aims to improve the reliability and repeatability of fecal metal measurements and gives some recommendations for sampling. First, we studied levels of variation in metallic element (arsenic, calcium, cadmium, cobalt, copper, nickel, lead) concentrations: temporal variation within an individual, among siblings in a brood and among-brood/spatial variation. Second, we explored the variation caused by dual composition (urate vs. feces) of bird droppings. Two sets of fresh fecal samples were collected from pied flycatcher (Ficedula hypoleuca) nestlings living in a metal polluted area in summers 2017 (dataset 1) and 2018 (dataset 2). We found a great deal of temporal intra-individual variation in metal levels, suggesting that dietary exposure varied markedly in a short time scale (within a day). A sample from only one nestling per brood did not well describe the brood mean value, and we recommend that at least four siblings should be sampled. Brood level samples give relatively good temporal repeatability for most metals. For all the metals, the levels in the fecal portion were more than double to those in the urate portion. Since the mass proportion of urate in the bird droppings varied a great deal among samples, standardizing sampling, e.g., by collecting only the fecal part, would markedly reduce the variation due to composition. Alternatively, urate portion could be used for biomonitoring of internally circulated bioavailable metal.

Reproductive, phenotypic and life-history traits in many animal and plant taxa show geographic variation, indicating spatial variation in selection regimes. Maternal deposition to avian eggs, such as hormones, antibodies and antioxidants, critically affect development of the offspring, with long-lasting effects on the phenotype and fitness. Little is however known about large-scale geographical patterns of variation in maternal deposition to eggs. We studied geographical variation in egg components of a passerine bird, the pied flycatcher (Ficedula hypoleuca), by collecting samples from 16 populations and measuring egg and yolk mass, albumen lysozyme activity, yolk immunoglobulins, yolk androgens and yolk total carotenoids. We found significant variation among populations in most egg components, but ca. 90% of the variation was among individuals within populations. Population however explained 40% of the variation in carotenoid levels. In contrast to our hypothesis, we found geographical trends only in carotenoids, but not in any of the other egg components. Our results thus suggest high within-population variation and leave little scope for local adaptation and genetic differentiation in deposition of different egg components. The role of these maternally-derived resources in evolutionary change should be further investigated.