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Experimentally increased brood size accelerates actuarial senescence and increases subsequent reproductive effort in a wild bird population.

ABSTRACT: The assumption that reproductive effort decreases somatic state, accelerating ageing, is central to our understanding of life-history variation. Maximal reproductive effort early in life is predicted to be maladaptive by accelerating ageing disproportionally, decreasing fitness. Optimality theory predicts that reproductive effort is restrained early in life to balance the fitness contribution of reproduction against the survival cost induced by the reproductive effort. When adaptive, the level of reproductive restraint is predicted to be inversely linked to the remaining life expectancy, potentially resulting in a terminal effort in the last period of reproduction. Experimental tests of the reproductive restraint hypothesis require manipulation of somatic state and subsequent investigation of reproductive effort and residual life span. To our knowledge the available evidence remains inconclusive, and hence reproductive restraint remains to be demonstrated. We modulated somatic state through a lifelong brood size manipulation in wild jackdaws and measured its consequences for age-dependent mortality and reproductive success. The assumption that lifelong increased brood size reduced somatic state was supported: Birds rearing enlarged broods showed subsequent increased rate of actuarial senescence, resulting in reduced residual life span. The treatment induced a reproductive response in later seasons: Egg volume and nestling survival were higher in subsequent seasons in the increased versus reduced broods' treatment group. We detected these increases in egg volume and nestling survival despite the expectation that in the absence of a change in reproductive effort, the reduced somatic state indicated by the increased mortality rate would result in lower reproductive output. This leads us to conclude that the higher reproductive success we observed was the result of higher reproductive effort. Our findings show that reproductive effort negatively covaries with remaining life expectancy, supporting optimality theory and confirming reproductive restraint as a key factor underpinning life-history variation.

SUBMITTER: Boonekamp JJ

PROVIDER: S-EPMC7317873 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Experimentally increased brood size accelerates actuarial senescence and increases subsequent reproductive effort in a wild bird population.

Boonekamp Jelle J JJ Bauch Christina C Verhulst Simon S

The Journal of animal ecology 20200312 6

The assumption that reproductive effort decreases somatic state, accelerating ageing, is central to our understanding of life-history variation. Maximal reproductive effort early in life is predicted to be maladaptive by accelerating ageing disproportionally, decreasing fitness. Optimality theory predicts that reproductive effort is restrained early in life to balance the fitness contribution of reproduction against the survival cost induced by the reproductive effort. When adaptive, the level o ...[more]

PMID: 32037534

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Project description:The concept of actuarial senescence (defined here as the increase in mortality hazards with age) is often confounded with life span duration, which obscures the relative role of age-dependent and age-independent processes in shaping the variation in life span. We use the opportunity afforded by the Species360 database, a collection of individual life span records in captivity, to analyze age-specific mortality patterns in relation to variation in life span. We report evidence of actuarial senescence across 96 mammal species. We identify the life stage (juvenile, prime-age, or senescent) that contributes the most to the observed variation in life span across species. Actuarial senescence only accounted for 35%-50% of the variance in life span across species, depending on the body mass category. We computed the sensitivity and elasticity of life span to five parameters that represent the three stages of the age-specific mortality curve-namely, the duration of the juvenile stage, the mean juvenile mortality, the prime-age (i.e., minimum) adult mortality, the age at the onset of actuarial senescence, and the rate of actuarial senescence. Next, we computed the between-species variance in these five parameters. Combining the two steps, we computed the relative contribution of each of the five parameters to the variance in life span across species. Variation in life span was increasingly driven by the intensity of actuarial senescence and decreasingly driven by prime-age adult mortality from small to large species because of changes in the elasticity of life span to these parameters, even if all the adult survival parameters consistently exhibited a canalization pattern of weaker variability among long-lived species than among short-lived ones. Our work unambiguously demonstrates that life span cannot be used to measure the strength of actuarial senescence, because a substantial and variable proportion of life span variation across mammals is not related to actuarial senescence metrics.

Dataset Information

Experimentally increased brood size accelerates actuarial senescence and increases subsequent reproductive effort in a wild bird population.

Publications

Experimentally increased brood size accelerates actuarial senescence and increases subsequent reproductive effort in a wild bird population.

Similar Datasets

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