Helpers compensate for age-related declines in parental care and offspring survival in a cooperatively breeding bird

Hammers, Martijn; Kingma, Sjouke A.; Boheemen, Lotte A. van; Sparks, Alexandra M.; Burke, Terry; Dugdale, Hannah L.; Richardson, David S.; Komdeur, Jan

doi:10.32942/osf.io/vgzc7

Cited by 13 publications

(32 citation statements)

References 34 publications

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“…Ages of the group members that act as helpers in the rearing of offspring may also potentially be of importance. The presence [23,24], number [25,26], sex [27,28], behavior [29,30], and relatedness [31] of helpers can all impact the fitness of the young. There is also evidence from several species that helpers become more effective in provisioning young with increased experience.…”

Section: Introductionmentioning

confidence: 99%

Do the ages of parents or helpers affect offspring fitness in a cooperatively breeding bird?

Cooper¹,

Bonnet²,

Cockburn³

et al. 2020

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Age-related changes in either the phenotypes or genotypes of care-givers can impact juvenile performance. However, rarely in wild populations have germline and non-germline transgenerational effects of ageing been separately quantified. In cooperatively breeding animals, in addition to parental ages, the age of ‘helpers’ attending the nest may also impact juvenile performance. Using a wild population of superb fairy-wrens (Malurus cyaneus), we investigated the effects of maternal, paternal, and helper ages on three measures of offspring performance: weight as a nestling, juvenile survival, and recruitment to the breeding population, using up to 4538 offspring over 30 cohorts. A mother’s age at conception negatively affected her offspring’s performance, but mothers with a longer total lifespan had offspring with higher juvenile survival. We distinguished the effects of paternal germline versus paternal environment (for offspring sired extra-pair) as well as the combined effect of paternal germline and environment (for offspring sired within-pair). Neither the ages of the genetic or the cuckolded social father impacted extra-pair offspring performance, however, for offspring sired within-pair, there was a positive effect of paternal age on the juvenile survival. Offspring performance increased most strongly and consistently with the average age of helpers. Our analyses thus revealed multiple associations between offspring fitness components and the ages of the adults around them. These associations appear to be primarily driven by age-related environmental effects, rather than age-related changes in germline.

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Section: Introductionmentioning

confidence: 99%

Do the ages of parents or helpers affect offspring fitness in a cooperatively breeding bird?

Cooper¹,

Bonnet²,

Cockburn³

et al. 2020

Preprint

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“…All data are available in the Dryad depository: https://doi.org/10.5061/dryad.rxwdbrv4s (Hammers et al. 2020)…”

Section: Data Availability Statementmentioning

confidence: 99%

Helpers compensate for age-related declines in parental care and offspring survival in a cooperatively breeding bird

et al. 2021

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Offspring from elderly parents often have lower survival due to parental senescence. In cooperatively breeding species, where offspring care is shared between breeders and helpers, the alloparental care provided by helpers is predicted to mitigate the impact of parental senescence on offspring provisioning and, subsequently, offspring survival. We test this prediction using data from a long‐term study on cooperatively breeding Seychelles warblers (Acrocephalus sechellensis). We find that the nestling provisioning rate of female breeders declines with their age. Further, the total brood provisioning rate and the first‐year survival probability of offspring decline progressively with age of the female breeder, but these declines are mitigated when helpers are present. This effect does not arise because individual helpers provide more care in response to the lower provisioning of older dominant females, but because older female breeders have recruited more helpers, thereby receiving more overall care for their brood. We do not find such effects for male breeders. These results indicate that alloparental care can alleviate the fitness costs of senescence for breeders, which suggests an interplay between age and cooperative breeding.

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“…Senescence has been well documented in the Seychelles warbler (Hammers et al 2015) with age-dependent declines in both survival and reproduction (Hammers et al 2012(Hammers et al , 2013Raj Pant et al 2020). Mothers provide more parental care to the offspring than fathers (Hammers et al 2019) and the amount of provisioning declines with maternal, but not paternal age (Hammers et al 2021). Further, the first-year survival of offspring declines with maternal, but not paternal age (Hammers et al 2021).…”

Section: Introductionmentioning

confidence: 99%

“…For instance, a negative effect of parental age on offspring lifespan has been reported across a range of taxa in both laboratory and field studies ('Lansing effect'; (Plaistow et al 2015;Wylde et al 2019;Monaghan et al 2020), however this effect is not universal (Fox et al 2003;Yilmaz et al 2008;Krishna et al 2012). Age-dependent declines in parental gamete quality (Monaghan & Metcalfe 2019) and declines in parental care (Hammers et al 2021) are predicted to cause reduced fitness in offspring of elderly parents. Indeed, there is increasing evidence in wild populations that elderly parents produce offspring with lower birth weights, reduced neonatal survival and lower recruitment rates (Hadley et al 2006;Descamps et al 2008;Nussey et al 2009;Hoffman et al 2010;Hayward et al 2015;Fay et al 2016;Hammers et al 2021).…”

Section: Introductionmentioning

confidence: 99%

“…Age-dependent declines in parental gamete quality (Monaghan & Metcalfe 2019) and declines in parental care (Hammers et al 2021) are predicted to cause reduced fitness in offspring of elderly parents. Indeed, there is increasing evidence in wild populations that elderly parents produce offspring with lower birth weights, reduced neonatal survival and lower recruitment rates (Hadley et al 2006;Descamps et al 2008;Nussey et al 2009;Hoffman et al 2010;Hayward et al 2015;Fay et al 2016;Hammers et al 2021). However, due to the necessity for long-term longitudinal studies with accurate lifetime reproductive success and survival data, the number of studies that have investigated the impact of parental age on the lifespan and lifetime fitness of offspring in natural populations remains limited (Rödel et al 2009;Bouwhuis et al 2010Bouwhuis et al , 2015Schroeder et al 2015;Reichert et al 2019;Kroeger et al 2020).…”

Section: Introductionmentioning

confidence: 99%

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Sex-dependent effects of parental age on offspring fitness in a cooperatively breeding bird

Sparks¹,

Hammers²,

Komdeur³

et al. 2021

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Parental age can have considerable effects on offspring phenotypes and health. However, intergenerational effects may also have longer-term effects on offspring fitness. Few studies have investigated parental age effects on offspring fitness in natural populations while also testing for sex- and environment-specific effects. Further, longitudinal parental age effects may be masked by population-level processes such as the selective disappearance of poor quality individuals. Here, we used multi-generational data collected on individually marked Seychelles warblers (Acrocephalus sechellensis) to investigate the impact of maternal and paternal age on offspring lifespan and lifetime reproductive success. We found negative effects of maternal age on female offspring lifespan and lifetime reproductive success which was likely driven by within-mother effects. There was no difference in annual reproductive output of females born to older versus younger mothers, suggesting that the differences in offspring lifetime reproductive success are driven by offspring lifespan. In contrast, the lifetime reproductive success of male offspring increased with maternal age, but this was driven by between-mother effects. No within- or between-individual paternal age effects were found for female offspring, but fathers that reached old age produced male offspring with higher lifetime reproductive success. We did not find strong evidence for environment-dependent parental age effects. Our study provides evidence for parental age effects on the lifetime fitness of offspring and shows that such effects can be sex-dependent. These results add to the growing literature indicating the importance of intergenerational effects on long-term offspring performance and highlights that these effects can be an important driver of variation in longevity and fitness in the wild.

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Helpers compensate for age-related declines in parental care and offspring survival in a cooperatively breeding bird

Cited by 13 publications

References 34 publications

Do the ages of parents or helpers affect offspring fitness in a cooperatively breeding bird?

Do the ages of parents or helpers affect offspring fitness in a cooperatively breeding bird?

Helpers compensate for age-related declines in parental care and offspring survival in a cooperatively breeding bird

Sex-dependent effects of parental age on offspring fitness in a cooperatively breeding bird

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