An official website of the United States government
Abstract Parental age at offspring conception often influences offspring longevity, but the mechanisms underlying this link are poorly understood. One mechanism that may be important is telomeres, highly conserved, repetitive sections of non‐coding DNA that form protective caps at chromosome ends and are often positively associated with longevity. Here, the potential pathways by which the age of the parents at the time of conception may impact offspring telomeres are described first, including direct effects on parental gamete telomeres and indirect effects on offspring telomere loss during pre‐ or post‐natal development. Then a surge of recent studies demonstrating the effects of parental age on offspring telomeres in diverse taxa are reviewed. In doing so, important areas for future research and experimental approaches that will enhance the understanding of how and when these effects likely occur are highlighted. It is concluded by considering the potential evolutionary consequences of parental age on offspring telomeres.
more »
« less
Stressors interact across generations to influence offspring telomeres and survival
Parental stress often has long-term consequences for offspring. However, the mechanisms underlying these effects and how they are shaped by conditions offspring subsequently experience are poorly understood. Telomeres, which often shorten in response to stress and predict longevity, may contribute to, and/or reflect these cross-generational effects. Traditionally, parental stress is expected to have negative effects on offspring telomeres, but experimental studies in captive animals suggest that these effects may depend on the subsequent conditions that offspring experience. Yet, the degree to which parental stress influences and interacts with stress experienced by offspring to affect offspring telomeres and survival in free-living organisms is unknown. To assess this, we experimentally manipulated the stress exposure of free-living parent and offspring house sparrows ( Passer domesticus ). We found a weak, initial, negative effect of parental stress on offspring telomeres, but this effect was no longer evident at the end of post-natal development. Instead, the effects of parental stress depended on the natural sources of stress that offspring experienced during post-natal development whereby some outcomes were improved under more stressful rearing conditions. Thus, the effects of parental stress on offspring telomeres and survival are context-dependent and may involve compensatory mechanisms of potential benefit under some circumstances.
more »
« less
- Award ID(s):
- 1656212
- PAR ID:
- 10358061
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 289
- Issue:
- 1982
- ISSN:
- 0962-8452
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
null (Ed.)Parental age can affect offspring telomere length through heritable and epigenetic-like effects, but at what stage during development these effects are established is not well known. To address this, we conducted a cross-fostering experiment in common gulls (Larus canus) that enabled us distinguish between pre-and post-natal parental age effects on offspring telomere length. Whole clutches were exchanged after clutch completion within and between parental age classes (young and old) and blood samples were collected from chicks at hatching and during the fastest growth phase (11 days later) to measure telomeres. Neither the ages of the natal nor the foster parents predicted the telomere length or the change in telomere lengths of their chicks. Telomere length (TL) was repeatable within chicks, but increased across development (repeatability = 0.55, intraclass correlation coefficient within sampling events 0.934). Telomere length and the change in telomere length were not predicted by post-natal growth rate. Taken together, these findings suggest that in common gulls, telomere length during early life is not influenced by parental age or growth rate, which may indicate that protective mechanisms buffer telomeres from external conditions during development in this relatively long-lived species.more » « less
-
Understanding the relationship between the environment parents experience during reproduction and the environment embryos experience in the nest is essential for determining the intergenerational responses of populations to novel environmental conditions. Thermal stress has become commonplace for organisms inhabiting areas affected by rising temperatures. Exposure to body temperatures that approach, but do not exceed, upper thermal limits often induces adverse effects in organisms, but the propensity for these temperatures to have intergenerational consequences has not been explored in depth. Here, we quantified the effects of thermal stress on the reproductive physiology and development of brown anoles (Anolis sagrei) when thermal stress is experienced by mothers and by eggs during incubation.Mothers exposed to thermal stress produced smaller eggs and smaller offspring with reduced growth rates, while egg stress reduced developmental time and offspring mass. Hatchling survival and growth were negatively affected by thermal stress experienced by mothers but not by thermal stress experienced as eggs. We found mixed evidence for an additive effect of thermal stress on offspring; rather, thermal stress had specific (and most often negative) effects on different components of offspring phenotypes and fitness proxies when experienced either by mothers or by eggs. Stressful body temperatures therefore can function in a similar manner to other types of maternal effects in reptiles; however, this maternal effect has predominantly negative consequences on offspring.more » « less
-
ABSTRACT In the face of challenges, animals must balance investments in reproductive effort versus their own survival. Physiologically, this trade-off may be mediated by glucocorticoid release by the hypothalamic–pituitary–adrenal axis and prolactin release from the pituitary to maintain parental care. The degree to which animals react to and recover from stressors likely affects maintenance of parental behavior and, ultimately, fitness. However, less is known about how gaining parental experience may alter hormonal stress responses and their underlying neuroendocrine mechanisms. To address this gap, we measured the corticosterone (CORT) and prolactin (PRL) stress response in individuals of both sexes of the biparental rock dove (Columba livia) that had never raised chicks versus birds that had fledged at least one chick. We measured both CORT and PRL at baseline and after an acute stressor (30 min restraint). We also measured negative feedback ability by administering dexamethasone, a synthetic glucocorticoid that suppresses CORT release, and measured CORT and PRL after 60 min. All hormones were measured when birds were not actively nesting to assess whether effects of parental experience extend beyond the breeding bout. Experienced birds had lower stress-induced and negative-feedback CORT, and higher stress-induced PRL than inexperienced birds. In a separate experiment, we measured glucocorticoid receptor subtype expression in the hippocampus, a key site of negative feedback regulation. Experienced birds showed higher glucocorticoid receptor expression than inexperienced controls, which may mediate their ability to attenuate CORT release. Together, these results shed light on potential mechanisms by which gaining experience may improve parental performance and fitness.more » « less
-
ABSTRACT It has long been recognized that the environment experienced by parents can influence the traits of offspring (i.e. ‘parental effects’). Much research has explored whether mothers respond to predictable shifts in environmental signals by modifying offspring phenotypes to best match future conditions. Many organisms experience conditions that theory predicts should favor the evolution of such ‘anticipatory parental effects’, but such predictions have received limited empirical support. ‘Condition transfer effects’ are an alternative to anticipatory effects that occur when the environment experienced by parents during development influences offspring fitness. Condition transfer effects occur when parents that experience high-quality conditions produce offspring that exhibit higher fitness irrespective of the environmental conditions in the offspring generation. Condition transfer effects are not driven by external signals but are instead a byproduct of past environmental quality. They are also likely adaptive but have received far less attention than anticipatory effects. Here, we review the generality of condition transfer effects and show that they are much more widespread than is currently appreciated. Condition transfer effects are observed across taxa and are commonly associated with experimental manipulations of resource conditions experienced by parents. Our Review calls for increased research into condition transfer effects when considering the role of parental effects in ecology and evolution.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rspb.2022.0868
