The ability to maintain a (relatively) stable body temperature in a wide range of thermal environments by use of endogenous heat production is a unique feature of endotherms such as birds. Endothermy is acquired and regulated via various endocrine and molecular pathways, and ultimately allows wide aerial, aquatic, and terrestrial distribution in variable environments. However, due to our changing climate, birds are faced with potential new challenges for thermoregulation, such as more frequent extreme weather events, lower predictability of climate, and increasing mean temperature. We provide an overview on thermoregulation in birds and its endocrine and molecular mechanisms, pinpointing gaps in current knowledge and recent developments, focusing especially on non-model species to understand the generality of, and variation in, mechanisms. We highlight plasticity of thermoregulation and underlying endocrine regulation, because thorough understanding of plasticity is key to predicting responses to changing environmental conditions. To this end, we discuss how changing climate is likely to affect avian thermoregulation and associated endocrine traits, and how the interplay between these physiological processes may play a role in facilitating or constraining adaptation to a changing climate. We conclude that while the general patterns of endocrine regulation of thermogenesis are quite well understood, at least in poultry, the molecular and endocrine mechanisms that regulate, e.g. mitochondrial function and plasticity of thermoregulation over different time scales (from transgenerational to daily variation), need to be unveiled. Plasticity may ameliorate climate change effects on thermoregulation to some extent, but the increased frequency of extreme weather events, and associated changes in resource availability, may be beyond the scope and/or speed for plastic responses. This could lead to selection for more tolerant phenotypes, if the underlying physiological traits harbour genetic and individual variation for selection to act on – a key question for future research.
Abstract Maternal hormones, such as thyroid hormones transferred to embryos and eggs, are key signalling pathways to mediate maternal effects. To be able to respond to maternal cues, embryos must express key molecular ‘machinery’ of the hormone pathways, such as enzymes and receptors. While altricial birds begin thyroid hormone (TH) production only at/after hatching, experimental evidence suggests that their phenotype can be influenced by maternal THs deposited in the egg. However, it is not understood, how and when altricial birds express genes in the TH-pathway. For the first time, we measured the expression of key TH-pathway genes in altricial embryos, using two common altricial ecological model species (pied flycatcher, Ficedula hypoleuca and blue tit Cyanistes caeruleus ). Deiodinase DIO1 gene expression could not be reliably confirmed in either species, but deiodinase enzyme DIO2 and DIO3 genes were expressed in both species. Given that DIO2 coverts T4 to biologically active T3, and DIO3 mostly T3 to inactive forms of thyroid hormones, our results suggest that embryos may modulate maternal signals. Thyroid hormone receptor ( THRA and THRB ) and monocarboxyl membrane transporter gene ( SLC15A2 ) were also expressed, enabling TH-responses. Our results suggest that early altricial embryos may be able to respond and potentially modulate maternal signals conveyed by thyroid hormones.
Hormones transferred from mothers to their offspring are thought to be a tool for mothers to prepare their progeny for expected environmental conditions, thus increasing fitness. Thyroid hormones (THs) are crucial across vertebrates for embryonic and postnatal development and metabolism. Yet yolk THs have mostly been ignored in the context of hormone-mediated maternal effects. In addition, the few studies on maternal THs have yielded contrasting results that could be attributed to either species or environmental differences. In this study, we experimentally elevated yolk THs (within the natural range) in a wild population of a migratory passerine, the European pied flycatcher (Ficedula hypoleuca), and assessed the effects on hatching success, nestling survival, growth, and oxidative status (lipid peroxidation, antioxidant enzyme activity, and oxidative balance). We also sought to compare our results with those of a closely related species, the collared flycatcher (Ficedula albicolis), that has strong ecological and life-history similarities with our species. We found no effects of yolk THs on any of the responses measured. We could detect only a weak trend on growth: elevated yolk THs tended to increase growth during the second week after hatching. Our results contradict the findings of previous studies, including those of the collared flycatcher. However, differences in fledging success and nestling growth between both species in the same year suggest a context-dependent influence of the treatment. This study should stimulate more research on maternal effects mediated by THs and their potential context-dependent effects.
Predation risk is an environmental stressor that can induce changes in prey behavior and physiology. Perception of predation risk may indirectly affect offspring traits and future fitness prospects via impacts on the condition of parents. Females may influence the survival of their offspring via maternal effects, especially when breeding in stressful conditions. We investigated the effects of continuous predation risk perceived by mothers on the maternal allocation of immune factors and carotenoids in eggs of the pied flycatcher Ficedula hypoleuca . We collected eggs from wild pied flycatchers that bred in the vicinity of a predator nest (pygmy owl Glaucidium passerinum ), were exposed to cues of a mammalian nest predator (urine of least weasel Mustela nivalis ), or received appropriate controls for these two groups. Pied flycatchers transferred more immunoglobulin in eggs under high predation risk in both owl and mammalian predator treatments. The presence of owl nests also lowered the level of lysozyme transferred in the eggs in one of the two study years. Predation risk did not modify egg size or overall carotenoid levels. Our results show that continuous predation risk perceived by females during egg‐laying affects egg composition. This different allocation of maternal immune factors may be an adaptive response evolved to increase the probability of offspring survival.
ABSTRACT The gut microbiome (hereafter, GM) varies across individuals of the same species and this pattern has been observed in multiple wild species. Evidence shows that the GM connects to individual health and survival especially in captive species, but more research is needed to understand how the GM connects to host fitness in wild species. We used long-term monitoring data to investigate whether the GM of collared flycatchers Ficedula albicollis associates with annual and lifetime reproductive success (LRS), and survival to the following breeding season. This is the first study that 1) characterized the collared flycatcher GM, and 2) investigated how variation in the GM related to LRS in wild birds. Our results showed that higher GM diversity was associated with a higher annual and lifetime reproductive success in especially male collared flycatchers. We also found that the compositional variation in collared flycatcher GMs was explained by sex, age, and breeding habitat, but not by annual or lifetime reproductive success. Individuals that died before the next breeding season had higher abundances of ASVs belonging to the pathogenic families Enterobacteriaceae and Parachlamydiaceae , and the genera Corynebacteria and Sphingomonas . Our results show that the GM associates with different aspects of host fitness in a wild bird population. More research is needed to evaluate if there is a causal relationship between the GM and individual fitness. These findings also contribute to our understanding of the GMs role in evolution by elucidating the connection between the GM (trait) and reproductive success.
Abstract The thermal sensitivity of early life stages can play a fundamental role in constraining species distribution. For egg-laying ectotherms, cool temperatures often extend development time and exacerbate developmental energy cost. Despite these costs, egg laying is still observed at high latitudes and altitudes. How embryos overcome the developmental constraints posed by cool climates is crucial knowledge for explaining the persistence of oviparous species in such environments and for understanding thermal adaptation more broadly. Here, we studied maternal investment, and embryo energy use and allocation in wall lizards spanning altitudinal regions, as potential mechanisms of local adaptation to development in cool climates. Specifically, we compared population-level differences in (1) investment from mothers (egg mass, embryo retention and thyroid yolk hormone concentration), (2) embryo energy expenditure during development, and (3) embryo energy allocation from yolk towards tissue. We found evidence that energy expenditure was greater under cool compared with warm incubation temperatures. Females from relatively cool regions did not compensate for this energetic cost of development by producing larger eggs or increasing thyroid hormone concentration in yolk. Instead, embryos from the high-altitude region used less energy to complete development, i.e., they developed faster without a concomitant increase in metabolic rate, compared with those from the low-altitude region. Embryos from high altitudes also allocated relatively more energy towards tissue production, hatching with lower residual yolk:tissue ratios than low-altitude region embryos. These results suggest that local adaptation to cool climate in wall lizards involves mechanisms that regulate embryonic utilisation of yolk reserves and its allocation towards tissue, rather than shifts in maternal investment of yolk content or composition.
