Troubleshooting the potential pitfalls of cross‐fostering

Winney, Isabel; Nakagawa, Shinichi; Hsu, Yu‐Hsun; Burke, Terry; Schroeder, Julia

doi:10.1111/2041-210x.12341

Cited by 28 publications

(43 citation statements)

References 46 publications

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“…Therefore we have reason to be equally confident about the accuracy of our estimates of LRS. iv) Finally, a large proportion of broods was cross-fostered systematically from 2000 onwards (14). These data allow us to differentiate among the effects of the genetic parents, the effects of early social environment, and the effects of parent-offspring interactions after hatching (44).…”

Section: Methodsmentioning

confidence: 99%

“…In contrast, if it were caused by a transgenerational, epigenetically inherited effect, then we would expect the age of the foster parent to have no effect on the annual number of recruits of the focal bird. Therefore we used a dataset of focal birds that had been cross-fostered (14) and for which the age of the cross-fostered parents was known (n = 453 foster mothers, n = 385 foster fathers). We ran two analyses, one for each parental sex, including both the foster and genetic parents' ages to distinguish between the effects of both.…”

Section: Parental Agementioning

confidence: 99%

“…We use these data to demonstrate that parental age has a negative effect on fitness. We complement this study with a long-term cross-fostering experiment (14) that allows us to demonstrate that this effect is not environmentally induced. Our study reveals the hidden consequences of late-life reproduction for the next generation.…”

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confidence: 99%

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Reduced fitness in progeny from old parents in a natural population

Schroeder

Nakagawa

Rees

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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140

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A nongenetic, transgenerational effect of parental age on offspring fitness has been described in many taxa in the laboratory. Such a transgenerational fitness effect will have important influences on population dynamics, population age structure, and the evolution of aging and lifespan. However, effects of parental age on offspring lifetime fitness have never been demonstrated in a natural population. We show that parental age has sex-specific negative effects on lifetime fitness, using data from a pedigreed insular population of wild house sparrows. Birds whose parents were older produced fewer recruits annually than birds with younger parents, and the reduced number of recruits translated into a lifetime fitness difference. Using a long-term cross-fostering experiment, we demonstrate that this parental age effect is unlikely to be the result of changes in the environment but that it potentially is epigenetically inherited. Our study reveals the hidden consequences of late-life reproduction that persist into the next generation.aging | epigenetic | indirect effects | senescence | transgenerational R eproducing at old age is known to incur costs such as an increased risk of polysomy and higher infant and maternal mortality. One potential cost that is hard to estimate occurs when parental age influences the lifespan or fertility of the next generation and beyond. First described by Alexander Graham Bell (1), this negative influence of parental age on offspring fitness [known as the "Lansing effect" (2-6)] has been observed in humans and in many taxa in the laboratory. Such transgenerational effects might have an epigenetic cause and are critical for understanding the evolution of late reproduction and longevity (7-11). However, to our knowledge, an effect of parental age on fitness in the next generation has not yet been shown conclusively in the wild, perhaps because its detection requires an exact knowledge of parental age and of the lifetime fate of offspring, data that are difficult to gather in natural populations (12). We have data from a natural, pedigreed population of passerines, house sparrows (Passer domesticus), in which we know the life history and precise fitness estimates of nearly all individuals (13). We use these data to demonstrate that parental age has a negative effect on fitness. We complement this study with a long-term cross-fostering experiment (14) that allows us to demonstrate that this effect is not environmentally induced. Our study reveals the hidden consequences of late-life reproduction for the next generation. Such transgenerational effects have the potential to help us better understand the evolution of aging and lifespan. ResultsWe found no statistically significant effect of a parent's age at reproduction on its offspring's longevity (Table 1). However, we found significant, sex-specific evidence for a negative effect of the age of the focal individual's parents on its lifetime reproductive success (the number of genetic recruits over a lifetime, LRS; Fig. 1). Sparrow females ...

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Section: Methodsmentioning

confidence: 99%

Section: Parental Agementioning

confidence: 99%

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Reduced fitness in progeny from old parents in a natural population

Schroeder

Nakagawa

Rees

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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140

206

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“…This population has extremely low rates of immigration and emigration, and high resighting probabilities (Simons et al ., ), so the survey has a very limited bias. A large proportion of nestlings were cross‐fostered on the day after hatching (Winney et al ., ). This manipulation increases our power to separate premanipulation maternal effects from additive genetic and post‐manipulation environmental (social brood) effects (Kruuk & Hadfield, ).…”

Section: Methodsmentioning

confidence: 97%

Heritability and social brood effects on personality in juvenile and adult life‐history stages in a wild passerine

Winney

Schroeder

Nakagawa

et al. 2017

J of Evolutionary Biology

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How has evolution led to the variation in behavioural phenotypes (personalities) in a population? Knowledge of whether personality is heritable, and to what degree it is influenced by the social environment, is crucial to understanding its evolutionary significance, yet few estimates are available from natural populations. We tracked three behavioural traits during different life-history stages in a pedigreed population of wild house sparrows. Using a quantitative genetic approach, we demonstrated heritability in adult exploration, and in nestling activity after accounting for fixed effects, but not in adult boldness. We did not detect maternal effects on any traits, but we did detect a social brood effect on nestling activity. Boldness, exploration and nestling activity in this population did not form a behavioural syndrome, suggesting that selection could act independently on these behavioural traits in this species, although we found no consistent support for phenotypic selection on these traits. Our work shows that repeatable behaviours can vary in their heritability and that social context influences personality traits. Future efforts could separate whether personality traits differ in heritability because they have served specific functional roles in the evolution of the phenotype or because our concept of personality and the stability of behaviour needs to be revised.

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“…In contrast, Winney et al. () showed that in house sparrows ( Passer domesticus ), cross‐fostered offspring had higher survival, but attributed this to methodological problems. The partial cross‐fostering design does not allow the consequences of parent–offspring coadaptation on parental fitness to be measured, as all parents rear a mix of related and unrelated offspring.…”

mentioning

confidence: 96%

No evidence for sibling or parent-offspring coadaptation in a wild population of blue tits, despite high power

Thomson

Hadfield

2018

Evolution

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Parent and offspring behaviors are expected to act as both the agents and targets of selection. This may generate parent–offspring coadaptation in which parent and offspring behaviors become genetically correlated in a way that increases inclusive fitness. Cross‐fostering has been used to study parent–offspring coadaptation, with the prediction that offspring raised by non‐relatives, or parents raising non‐relatives, should suffer fitness costs. Using long‐term data from more than 400 partially crossed broods of blue tits ( Cyanistes caeruleus ), we show that there is no difference in mass or survival between crossed and non‐crossed chicks. However, previous studies for which the evidence for parent–offspring coadaptation is strongest compare chicks from fully crossed broods with those from non‐crossed broods. When parent–offspring coadaptation acts at the level of the brood then partial cross‐fostering experiments are not expected to show evidence of coadaptation. To test this, we performed an additional experiment (163 broods) in which clutches were either fully crossed, non‐crossed, or partially crossed. In agreement with the long‐term data, there was no evidence for parent–offspring coadaptation on offspring fitness despite high power. In addition there was no evidence of effects on parental fitness, nor evidence of sibling coadaptation, although the power of these tests was more modest.

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Troubleshooting the potential pitfalls of cross‐fostering

Cited by 28 publications

References 46 publications

Reduced fitness in progeny from old parents in a natural population

Reduced fitness in progeny from old parents in a natural population

Heritability and social brood effects on personality in juvenile and adult life‐history stages in a wild passerine

No evidence for sibling or parent-offspring coadaptation in a wild population of blue tits, despite high power

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