Parental breeding age effects on descendants’ longevity interact over 2 generations in matrilines and patrilines

Wylde, Zachariah; Spagopoulou, Foteini; Hooper, Amy K.; Maklakov, Alexei A.; Bonduriansky, Russell

doi:10.1371/journal.pbio.3000556

Cited by 29 publications

(39 citation statements)

References 114 publications

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“…Later, Albert Lansing’s work on parthenogenic rotifers 13,14 (see also 15 ) showed that selection lines propagated through older parents gave rise to shorter-lived offspring and went extinct faster than selection lines using young parents. Subsequent studies have confirmed that offspring of older mothers may have reduced lifespan in a wide range of taxa, including flies 5,16 , nematodes 2 , butterflies 17 , water fleas 18 , birds 19–22 , mice 23 , squirrels 24 and humans 25 . The lifespan reduction in offspring of older parents led Lansing to suggest that age-dependent changes, or an ‘ageing factor’, is passed on to offspring of older parents, shortening the lives of those offspring – now commonly referred to as the Lansing effect.…”

Section: Introductionmentioning

confidence: 95%

Beneficial cumulative effects of old parental age on offspring fitness

Travers

Carlsson

Lind

et al. 2021

Preprint

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Old parental age is commonly associated with negative effects on offspring life-history traits. Such parental effect senescence is predicted to have a cumulative detrimental effect over successive generations. However, old parents may benefit from producing high-quality offspring when these compete for seasonal resources. Thus, old parents may choose to increase investment in their offspring, thereby producing fewer but larger and more competitive progeny. We show that Caenorhabditis elegans hermaphrodites increase parental investment with advancing age, resulting in fitter offspring who reach their reproductive peak earlier. Remarkably, these effects increased over six successive generations of breeding from old parents and were subsequently reversed following a single generation of breeding from a young parent. These results contradict the theory that old parents transfer a cumulative detrimental ageing factor to their offspring. Instead, our findings support the hypothesis that offspring of old parents receive more resources and convert them into increasingly faster life-histories.

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Section: Introductionmentioning

confidence: 95%

Beneficial cumulative effects of old parental age on offspring fitness

Travers

Carlsson

Lind

et al. 2021

Preprint

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“…For example, previous studies have found divergent gene expression in sons and daughters in response to maternal experiences (Constantinof et al., 2019; Metzger & Schulte, 2016), which suggests that maternal experience activates different developmental programmes in sons and daughters. Because the vast majority of studies that have compared parental effects on sons and daughters have focused on maternal effects, rather than both maternal and paternal effects (but see Emborski & Mikheyev, 2019; He et al., 2016; Priest et al., 2002; Wylde et al., 2019), it is often unclear if sex‐specific offspring effects are driven by (a) differences in the magnitude of sons’ versus daughters’ responses to parental environments (e.g. daughters are generally more responsive to parental stress, whether mediated by the mother or the father) or (b) how offspring attend to experiences of their same‐sex versus opposite‐sex parent.…”

Section: Introductionmentioning

confidence: 99%

Sex‐specific plasticity across generations I: Maternal and paternal effects on sons and daughters

Hellmann

Bukhari

Deno

et al. 2020

Journal of Animal Ecology

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1. Intergenerational plasticity or parental effects-when parental environments alter the phenotype of future generations-can influence how organisms cope with environmental change. An intriguing, underexplored possibility is that sex-of both the parent and the offspring-plays an important role in driving the evolution of intergenerational plasticity in both adaptive and non-adaptive ways. 2. Here, we evaluate the potential for sex-specific parental effects in a freshwater population of three-spined sticklebacks Gasterosteus aculeatus by independently and jointly manipulating maternal and paternal experiences and separately evaluating their phenotypic effects in sons versus daughters. We tested the adaptive hypothesis that daughters are more responsive to cues from their mother, whereas sons are more responsive to cues from their father. 3. We exposed mothers, fathers or both parents to visual cues of predation risk and measured offspring antipredator traits and brain gene expression. 4. Predator-exposed fathers produced sons that were more risk-prone, whereas predator-exposed mothers produced more anxious sons and daughters. Furthermore, maternal and paternal effects on offspring survival were non-additive: offspring with a predator-exposed father, but not two predator-exposed parents, had lower survival against live predators. There were also strong sex-specific effects on brain gene expression: exposing mothers versus fathers to predation risk activated different transcriptional profiles in their offspring, and sons and daughters strongly differed in the ways in which their brain gene expression profiles were influenced by parental experience. 5. We found little evidence to support the hypothesis that offspring prioritize their same-sex parent's experience. Parental effects varied with both the sex of the parent and the offspring in complicated and non-additive ways. Failing to account for these sex-specific patterns (e.g. by pooling sons and daughters) would have underestimated the magnitude of parental effects. Altogether, these results draw attention to the potential for sex to influence patterns of intergenerational plasticity and raise new questions about the interface between intergenerational plasticity and sex-specific selective pressures, sexual conflict and sexual selection.

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“…In the past, researchers were mainly focused on the effects of maternal age at breeding on offspring performance, but recently, evidence for paternal age effects is rapidly increasing (Ducatez et al, 2012; Fay et al, 2016; Priest et al, 2002; Saha et al, 2009; Sandin et al, 2016; Schroeder et al, 2015; Wylde, Spagopoulou, Hooper, Maklakov, & Bonduriansky, 2019). Paternal and maternal age effects can be mediated by different factors and vary in their influence on offspring performance (Crean & Bonduriansky, 2014; Curley, Mashoodh, & Champagne, 2011; Immler, Pryke, Birkhead, & Griffith, 2010; Lock, 2012; Wylde et al, 2019). However, studying paternal age effects in natural populations can be even more challenging, due to processes such as extra‐pair copulations or male‐biased dispersal, and would require reliable pedigree datasets.…”

Section: Figurementioning

confidence: 99%

Transgenerational maternal age effects in nature: Lessons learnt from Asian elephants

Spagopoulou

2020

Journal of Animal Ecology

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In Focus Reichert, S., Berger, V., Jackson, J., Chapman, S. N., Htut, W., Mar, K. U., & Lummaa, V. (2019). Maternal age at birth shapes offspring life‐history trajectory across generations in long‐lived Asian elephants. Journal of Animal Ecology, 89, 996–1007. Parental age can have strong effects on offspring life history, but the prevalence and magnitude of such effects in natural populations remain poorly understood. Using a multigenerational dataset of semi‐captive Asian elephants, Reichert et al. (2019) studied the effects of maternal and grandmaternal age on offspring performance and found that offspring from old mothers have lower survival, but higher body condition and reproductive success than offspring from younger mothers. Importantly the observed consequences on survival are long‐lasting and span more than one generation, with grand‐offspring of old grandmothers also showing reduced survival. These findings suggest that persistent transgenerational effects of maternal age on fitness can shape the individual variation in ageing patterns in nature and ultimately the evolution of life histories.

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Parental breeding age effects on descendants’ longevity interact over 2 generations in matrilines and patrilines

Cited by 29 publications

References 114 publications

Beneficial cumulative effects of old parental age on offspring fitness

Beneficial cumulative effects of old parental age on offspring fitness

Sex‐specific plasticity across generations I: Maternal and paternal effects on sons and daughters

Transgenerational maternal age effects in nature: Lessons learnt from Asian elephants

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