Causes and consequences of natural variation in maternal thyroid hormones in avian eggs

Mothers have the ability to shape the development of their offspring via various non-genetic pathways. These non-genetic influences can be behavioural, social or physiological, and are referred to as maternal effects. Research on maternal effects in vertebrates has grown significantly in the last two decades. A widely studied pathway for mothers to exert maternal effects is via hormonal signalling, and hormones transferred from the mothers to their offspring are designated as maternal hormones. Research on maternal hormones has mainly focused on steroid hormones, i.e. androgens and glucocorticoids, and there is now ample evidence that hormones of maternal origin can affect offspring phenotype. Other hormones are also transmitted by mothers such as thyroid hormones, which have received much less attention so far, despite their critical role in vertebrates on embryonic development, juvenile growth, metabolic activity and reproduction. Egg-laying species are good models to study maternal hormones as embryos develop in a sealed compartment and rely exclusively on maternal signalling during their development. In addition, it makes it easier to measure and manipulate yolk hormones independently of maternal physiology. In my thesis, I aimed at answering several questions on maternal thyroid hormones in avian eggs: their cost of production and transfer to the eggs, the potential ability of mothers to regulate thyroid hormone deposition in the yolk, their short- and long-term effects, and their interactions with environmental variables. Overall, my thesis sheds light on a crucial hormonal signal that has received little attention in the context of maternal hormones. It should stimulate future research on prenatal thyroid hormones that would tackle essential questions such as the potential adaptive value of variation in prenatal thyroid hormones or the embryonic response to this maternal signalling

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

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

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

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

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 (T-4, the prohormone for the biologically active triiodothyronine, T-3) during egg laying using T-4 implants in females of a wild population of pied flycatchers (Ficedula hypoleuca), and measured the resulting plasma and yolk T-4 and T-3 levels. We found an increase in plasma and yolk T-4 and no change in plasma or yolk T-3 concentration, leading to a decrease in yolk T-3/T-4 ratio in response to the T-4 treatment. The yolk T-3/T-4 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 T-4 to T-3 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 T-4 to T-3 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 T-4 to its biologically active T-3 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

Atracción de otras especies por reproducciones del canto del Pechiazul Luscinia svecica durante la migración otoñal: un test experimental empleando datos de anillamiento

Song playback of a particular avian species is well-known to have the potential to bias the sample of conspecifics that can be captured during mist-netting sessions, with respect to sex, age or body condition. However, the possibility that playback affects heterospecific captures has been less explored and lacks solid experimental evidence. In this study, we used an experimental approach to test whether Bluethroat Luscinia svecica song playback altered the overall number of individuals of other species captured during autumn migration in a wetland in southwestern France. We found that playback increased the capture rates of species that were not the direct target of the playback. This heterospecific attraction effect should be assessed and carefully considered when designing any avian monitoring programme.El uso de reproducciones sonoras de una especie de ave concreta es bien conocido que tiene el potencial de sesgar la muestra de conespecíficos (con relación al sexo, edad o condición corporal) que pueden ser capturados durante las sesiones de anillamiento con redes japonesas. Sin embargo, la posibilidad de que los reclamos sonoros afecten a las capturas de heterospecíficos ha sido menos explorada y carece de evidencias experimentales sólidas. En este estudio testamos experimentalmente si el uso de reclamos de pechiazul Luscinia svecica alteraba el número total de heterospecíficos capturados durante la migración otoñal en una zona húmeda localizada en el suroeste de Francia. Nuestros resultados muestran que el uso de reproductores sonoros incrementa las tasas de capturas de especies que no fueron el objetivo directo del reproductor. Este efecto de atracción por heterospecíficos debería ser evaluado y considerado cuidadosamente a la hora de diseñar cualquier programa de seguimiento de aves

Testing for context-dependent effects of prenatal thyroid hormones on offspring survival and physiology: an experimental temperature manipulation

Maternal effects via hormonal transfer from the mother to the offspring provide a tool to translate environmental cues to the offspring. Experimental manipulations of maternally transferred hormones have yielded increasingly contradictory results, which may be explained by differential effects of hormones under different environmental contexts. Yet context-dependent effects have rarely been experimentally tested. We therefore studied whether maternally transferred thyroid hormones (THs) exert context-dependent effects on offspring survival and physiology by manipulating both egg TH levels and post-hatching nest temperature in wild pied flycatchers (Ficedula hypoleuca) using a full factorial design. We found no clear evidence for context-dependent effects of prenatal THs related to postnatal temperature on growth, survival and potential underlying physiological responses (plasma TH levels, oxidative stress and mitochondrial density). We conclude that future studies should test for other key environmental conditions, such as food availability, to understand potential context-dependent effects of maternally transmitted hormones on offspring, and their role in adapting to changing environments

Testing for context-dependent effects of prenatal thyroid hormones on offspring survival and physiology: an experimental temperature manipulation

Abstract: Maternal effects via hormonal transfer from the mother to the offspring provide a tool to translate environmental cues to the offspring. Experimental manipulations of maternally transferred hormones have yielded increasingly contradictory results, which may be explained by differential effects of hormones under different environmental contexts. Yet context-dependent effects have rarely been experimentally tested. We therefore studied whether maternally transferred thyroid hormones (THs) exert context-dependent effects on offspring survival and physiology by manipulating both egg TH levels and post-hatching nest temperature in wild pied flycatchers (Ficedula hypoleuca) using a full factorial design. We found no clear evidence for context-dependent effects of prenatal THs related to postnatal temperature on growth, survival and potential underlying physiological responses (plasma TH levels, oxidative stress and mitochondrial density). We conclude that future studies should test for other key environmental conditions, such as food availability, to understand potential context-dependent effects of maternally transmitted hormones on offspring, and their role in adapting to changing environments