Heritable variation in maternally derived yolk androgens, thyroid hormones and immune factors

Ruuskanen, Suvi; Gienapp, Phillip; Groothuis, Ton G. G.; Schaper, Sonja V.; Darras, Veerle; Pereira, Cliff; Vries, de Tity; Visser, Marcel E.

doi:10.1038/hdy.2016.49

Cited by 21 publications

(16 citation statements)

References 49 publications

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“…To our knowledge, individual variation in responses to temperature challenges in circulating THs, the key hormones underlying thermoregulation, or associated molecular pathways (DIOs, receptors) has not been tested. However, there is some evidence on heritability of the mean levels of T3 in eggs (Ruuskanen et al, 2016b), suggesting scope for microevolutionary responses of THs to climate change. Interestingly, endocrine responses to thermal stress have been shown to vary among poultry breeds, potentially suggestive of genetic variation in temperature tolerance (Xie et al, 2018).…”

Section: Climate Change Microevolution In Thermoregulation and Its Umentioning

confidence: 99%

Endocrinology of thermoregulation in birds in a changing climate

Ruuskanen¹,

Hsu²,

Nord³

2019

Preprint

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The ability to maintain a (relatively) stable body temperature in a wide range of thermal environments 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 a compact 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 in 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. mitochondria 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 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.

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Section: Climate Change Microevolution In Thermoregulation and Its Umentioning

confidence: 99%

Endocrinology of thermoregulation in birds in a changing climate

Ruuskanen¹,

Hsu²,

Nord³

2019

Preprint

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“…Several lines of evidence suggest heritability of and natural selection on yolk hormone concentrations. Field and laboratory studies with wild birds showed that yolk androgen concentrations are heritable and under natural selection (Ruuskanen et al, ; Tschirren, Sendecka, Groothuis, Gustafsson, & Doligez, ); directional selection for high or low yolk androgen concentrations in domesticated Japanese quail ( Coturnix japonica ) yielded rapid divergence of titers within a few generations (Okuliarova, Groothuis, Škrobánek, & Zeman, ) and indicates matrilineal inheritance (Tschirren et al, ) ; and artificial selection for behavioral traits such as bold and shy personalities in Great tits ( Parus major ) resulted in increasing, respectively, decreasing yolk androgen concentrations over the laying sequence (Groothuis, Carere, Lipar, Drent, & Schwabl, ). These results prompt us to propose that differential environments operating in urban versus rural populations lead to coupled changes in yolk androgen concentrations and behavior, the mechanistic link being the wide‐spread and well‐established organizational actions of steroid hormones on brain function during development of vertebrates (Adkins‐Regan, ; Fowden & Forhead, ; McCarthy, ; O'Connor & Barrett, ).…”

Section: Discussionmentioning

confidence: 99%

Maternal effects and urbanization: Variation of yolk androgens and immunoglobulin in city and forest blackbirds

Partecke

Hegyi

Fitze

et al. 2020

Ecology and Evolution

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Wildlife inhabiting urban environments exhibit drastic changes in morphology, physiology, and behavior. It has often been argued that these phenotypic responses could be the result of micro‐evolutionary changes following the urbanization process. However, other mechanisms such as phenotypic plasticity, maternal effects, and developmental plasticity could be involved as well. To address maternal effects as potential mechanisms, we compared maternal hormone and antibody concentrations in eggs between city and forest populations of European blackbirds (Turdus merula), a widely distributed species for which previous research demonstrated differences in behavioral and physiological traits. We measured egg and yolk mass, yolk concentrations of androgens (androstenedione [A4], testosterone [T], 5α‐dihydrotestosterone [5α‐DHT], and immunoglobulins [IgY]) and related them to population, clutch size, laying order, embryo sex, and progress of breeding season. We show (a) earlier onset of laying in the city than forest population, but similar egg and clutch size; (b) higher overall yolk androgen concentrations in the forest than the city population (sex‐dependent for T); (c) greater among‐female variation of yolk T and 5α‐DHT concentrations in the forest than city population, but similar within‐clutch variation; (d) similar IgY concentrations with a seasonal decline in both populations; and (e) population‐specific positive (city) or negative (forest) association of yolk A4 and T with IgY concentrations. Our results are consistent with the hypotheses that hormone‐mediated maternal effects contribute to differences in behavioral and physiological traits between city and forest individuals and that yolk androgen and immunoglobulin levels can exhibit population‐specific relationships rather than trade‐off against each other.

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“…The first option may not be likely as a recent study showed no evidence that early exposure to experimentally elevated T in the egg results in elevated yolk T of the eggs produced by these females (Müller et al., ). The second option may be possible as yolk androgens, also in this species, show genetic heritability (Ruuskanen et al., ; Tschirren et al., ) and affect various personality traits (Daisley et al., ; Partecke & Schwabl, ; Ruuskanen & Laaksonen, ; Tobler & Sandell, ; van Oers et al., ; Vergauwen et al., ; see e.g. Marasco et al., for potential underlying mechanisms).…”

Section: Discussionmentioning

confidence: 99%

Maternal egg hormones in the mating context: The effect of pair personality

et al. 2017

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Abstract1. Animal personality traits emerge developmentally from the interaction of genetic and early environmental factors. Maternal hormones, such as androgens (testosterone, T and androstenedione, A4), transferred to embryos and egg yolks may simultaneously organize multiple behavioural and physiological traits. Although previous studies demonstrated an association between the mother's personality and yolk androgen levels, the independent effects of the male partner's personality and pair combination remains unknown.2. We test this association using an ecological model species for personality research, the great tit (Parus major) using multiple approaches: (1) a wild population, (2) a randomly mated captive population and (3) an experimental study with (dis)assortatively mated pairs from lines selected for fast exploration/boldness or slow exploration/shyness.3. Egg androgen concentrations were associated with variation in female personality traits, and the experimental data suggested that this is independent of male personality: Experimental females from the slow-shy line tended to have higher egg T concentrations than females from the fast-bold line, with no effect of male personality. Shy females from the wild population had higher egg A4 concentration than bold females. However, in the correlative data yolk hormones were linked with male personality, as well as the interaction between female and male traits: Male handling responsiveness correlated negatively with egg A4 concentration in wild birds. In randomly mated birds, pairs that were mated assortatively for personality had lower egg T concentrations than disassortatively mated pairs.4. Given that egg androgens are known mediators of avian personality, our results suggest that maternal hormones might contribute to the heritability of personality, may be sensitive to the social context of mating, and act as key drivers of individual differences. K E Y W O R D Savian, behavioural syndrome, maternal effects, Parus major, plasticity, testosteroneThis is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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Heritable variation in maternally derived yolk androgens, thyroid hormones and immune factors

Cited by 21 publications

References 49 publications

Endocrinology of thermoregulation in birds in a changing climate

Endocrinology of thermoregulation in birds in a changing climate

Maternal effects and urbanization: Variation of yolk androgens and immunoglobulin in city and forest blackbirds

Maternal egg hormones in the mating context: The effect of pair personality

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