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

Abstract

1. 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 tobalance 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.3. 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. 4. We modulated somatic state through a lifelong brood size manipulation in wild jackdaws and measured its consequences for age-dependent mortality and reproductive success. 5.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. 6. 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. 7. 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.

Late‐life reproduction in an insect: Terminal investment, reproductive restraint or senescence

“…Conversely, these results, in addition to the observation of a lifehistory priority scheme (Rigby & Moret, 2000), in which longevity is favoured at the expense of reproduction, suggest that T. molitor reproduction late in life is more consistent with the reproductive restraint hypothesis (McNamara et al, 2009). Therefore, our study provides, to our knowledge, the first direct experimental support for this hypothesis, for which only scarce empirical evidence from natural populations (Boonekamp et al, 2020;Elliott et al, 2014;Lecomte et al, 2010;Morin et al, 2016) or indirect experimental support in insects (Cotter et al, 2010;Smith et al, 2014) was previously available.…”

“…On the other hand, reduced late-life reproduction due to reproductive restraint should be associated with maintained somatic protection. Empirical evidence consistent with the reproductive restraint hypothesis is scarce (Boonekamp et al, 2020;Cotter et al, 2010;Elliott et al, 2014;Lecomte et al, 2010;Morin et al, 2016;Smith et al, 2014) and direct experimental evidence is missing.…”

“…On the other hand, reduced late‐life reproduction due to reproductive restraint should be associated with maintained somatic protection. Empirical evidence consistent with the reproductive restraint hypothesis is scarce (Boonekamp et al., 2020; Cotter et al, 2010; Elliott et al., 2014; Lecomte et al., 2010; Morin et al., 2016; Smith et al., 2014) and direct experimental evidence is missing. Experimentally disentangling a terminal investment strategy from the reproductive restraint one or senescence requires to assess the effects of age‐dependent reproductive effort on post‐reproduction survival and age‐related somatic functions (e.g.…”

The sources of sex differences in aging in annual fishes

“…a steeper increase in mortality with age in one sex). These two sources of differential mortality can be best estimated with a Gompertz model of increasing failure time (Bronikowski et al 2011; Boonekamp et al 2020). We fitted a set of models (Colchero et al 2012) to our data from the social treatment, in which shorter male lifespan was detected, and confirmed that Gompertz-family models well approximated observed mortality patterns (Supplementary Table 2).…”

“…We analyzed each population separately as we knew a priori that populations within species differ in lifespan (Blažek et al 2017) and, unlike for survival analysis, they cannot be entered as random effects to BaSTA. Gompertz-family models were chosen to provide the most unambiguous demographic interpretation of the parameters (Bronikowski et al 2011; Boonekamp et al 2020) and a good fit to the datasets. The Gompertz model assumes that aging starts at species-specific age, with one parameter (intercept, Initial mortality rate, IMR ) describing age-independent mortality (baseline mortality) and the second parameter (slope, Rate of Aging, RoA ) describing the increase in mortality with age (Pletcher et al 2000).…”