Maternal effects in birds - the ecological and evolutionary significance of yolk androgens and other egg components

Siirretty Doriast

Testing the short- and long-term effects of elevated prenatal exposure to different forms of thyroid hormones

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

Explorative behaviour is not associated with metabolism in the European Pied Flycatcher Ficedula hypoleuca

The pace‐of‐life syndrome hypothesis (POLS) represents an attractive theoretical framework suggesting that physiological and behavioural traits have evolved together with environmental conditions and life‐history strategies. POLS predicts that metabolic differences covary with behavioural variation such that high metabolic rate is associated with risk‐prone behaviour and a faster pace‐of‐life, whereas a low metabolic rate is associated with risk‐averse behaviour and a slower pace‐of‐life. We tested the POLS hypothesis in captive European Pied Flycatchers during their first year by examining the relationship between explorative behaviour and basal metabolic rate. Our results are inconsistent with POLS. The positive association of explorative behaviour with basal metabolic rate was not recovered for either sex, possibly due to foraging conditions in the aviaries where control and trial groups were fed twice a day, the birds' young age, developmental plasticity, or a non‐existent syndrome.</p

Plastic but repeatable : rapid adjustments of mitochondrial function and density during reproduction in a wild bird species

Funding: The project was funded by a ‘Turku Collegium for Science and Medicine’ Fellowship to AS and an Academy of Finland grant (#286278) to SR. Data used in this manuscript are available as part of the electronic supplementary material.Peer reviewedPostprin

Experimental copper exposure, but not heat stress, leads to elevated intraovarian thyroid hormone levels in three-spined sticklebacks (Gasterosteus aculeatus)

Climate change and pollution are some of the greatest anthropogenic threats to wild animals. Transgenerational plasticity-when parental exposure to environmental stress leads to changes in offspring phenotype-has been highlighted as a potential mechanism to respond to various environmental and anthropogenic changes across taxa. Transgenerational effects may be mediated via multiple mechanisms, such as transfer of maternal hormones to eggs/foetus. However, sources of variation in hormone transfer are poorly understood in fish, and thus the first step is to characterise whether environmental challenges alter transfer of maternal hormones to eggs. To this end, we explored the population variation and environmental variation (in response to temperature and endocrine disrupting copper) in maternal thyroid hormone (TH), transfer to offspring in a common fish model species, the three-spined stickleback (Gasterosteus aculeatus) using multiple approaches: (i) We compared ovarian TH levels among six populations across a wide geographical range in the Baltic Sea, including two populations at high water temperature areas (discharge water areas of nuclear power plants) and we experimentally exposed fish to (ii) environmentally relevant heat stress and (iii) copper for 7 days. We found that populations did not differ in intraovarian TH levels, and short-term heat stress did not influence intraovarian TH levels. However, copper exposure increased both T4 and T3 levels in ovaries. The next step would be to evaluate if such alterations would lead to changes in offspring phenotype

Testing different forms of regulation of yolk thyroid hormone transfer in pied flycatchers

Hormones transferred from mothers to their offspring are considered a maternal tool to prepare progeny for expected environmental conditions, increasing maternal and offspring fitness. To flexibly influence offspring, mothers should be able to transmit the hormonal signals independent of their own hormonal status. However, the ability to regulate hormone transfer to the next generation is under debate. We studied the transfer of thyroid hormones (THs) to eggs in a bird model. We elevated thyroxine (T4, the prohormone for the biologically active triiodothyronine, T3) during egg laying using T4 implants in females of a wild population of pied flycatchers (Ficedula hypoleuca), and measured the resulting plasma and yolk T4 and T3 levels. We found an increase in plasma and yolk T4 and no change in plasma or yolk T3 concentration, leading to a decrease in yolk T3/T4 ratio in response to the T4 treatment. The yolk T3/T4 ratio was similar to the plasma ratio in females during the yolking phase. This suggests that mothers are not able to regulate TH transfer to yolk but may regulate the T4 to T3 conversion to avoid potential costs of elevated exposure to the active hormone to herself and to her progeny. The absence of regulation in hormone transfer to eggs is in contrast to our predictions. Future studies on deiodinase activity that converts T4 to T3 in maternal and embryonic tissues may help our understanding of how mothers regulate circulating THs during breeding, as well as the embryos' role in converting maternal T4 to its biologically active T3 form during development

Manipulation of prenatal thyroid hormones does not affect growth or physiology in nestling Pied flycatchers

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

Endocrinology of thermoregulation in birds in a changing climate

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

Is maternal thyroid hormone deposition subject to a trade-off between self and egg because of iodine? An experimental study in rock pigeon

Maternal hormones constitute a key signalling pathway for mothers to shape offspring phenotype and fitness. Thyroid hormones (THs; triiodothyronine, T-3; and thyroxine, T-4) are metabolic hormones known to play crucial roles in embryonic development and survival in all vertebrates. During early developmental stages, embryos exclusively rely on exposure to maternal THs, and maternal hypothyroidism can cause severe embryonic maldevelopment. The TH molecule includes iodine, an element that cannot be synthesised by the organism. Therefore, TH production may become costly when environmental iodine availability is low. This may yield a trade-off for breeding females between allocating the hormones to self or to their eggs, potentially to the extent that it even influences the number of laid eggs. In this study, we investigated whether low dietary iodine may limit TH production and transfer to the eggs in a captive population of rock pigeons (Columba livia). We provided breeding females with an iodine-restricted (I-) diet or iodine-supplemented (1+) diet and measured the resulting circulating and yolk iodine and TH concentrations and the number of eggs laid. Our iodine-restricted diet successfully decreased both circulating and yolk iodine concentrations compared with the supplemented diet, but not circulating or yolk THs. This indicates that mothers may not be able to independently regulate hormone exposure for self and their embryos. However, egg production was clearly reduced in the I- group, with fewer females laying eggs. This result shows that restricted availability of iodine does induce a cost in terms of egg production. Whether females reduced egg production to preserve THs for themselves or to prevent embryos from exposure to low iodine and/or THs is as yet unclear

Born to be young? : Prenatal thyroid hormones increase early-life telomere length in wild collared flycatchers

Acknowledgements: We are grateful to many students and Szymek Drobniak for their help in the field, to three anonymous reviewers for their constructive feedback and to Pat Monaghan for providing access to TRF facilities. Funding: The project was funded by a Marie Sklodowska-Curie Postdoctoral Fellowship (#658085) and a ‘Turku Collegium for Science and Medicine’ Fellowship to AS, and an Academy of Finland grant (# 286278) to SR.Peer reviewedPostprin