A future food boom rescues the negative effects of early-life adversity on adult lifespan in a small mammal

Abstract

Early-life adversity, even when transient, can have lasting effects on individual phenotypes and reduce lifespan across species. If these effects can be mitigated by a high-quality later-life environment, then differences in future resources may explain variable resilience to early-life adversity. Using data from over 1000 wild North American red squirrels, we tested the hypothesis that the costs of early-life adversity for adult lifespan could be offset by later-life food abundance. We identified six adversities that reduced juvenile survival in the first year of life, though only one-birth date-had continued independent effects on adult lifespan. We then built a weighted early-life adversity (wELA) index integrating the sum of adversities and their effect sizes. Greater weighted early-life adversity predicted shorter adult lifespans in males and females, but a naturally occurring food boom in the second year of life ameliorated this effect. Experimental food supplementation did not replicate this pattern, despite increasing lifespan, indicating that the buffering effect of a future food boom may hinge on more than an increase in available calories. Our results suggest a non-deterministic role of early-life conditions for later-life phenotype, highlighting the importance of evaluating the consequences of early-life adversity in the context of an animal's entire life course.

Keywords: early-life adversity; longevity; mammal.

Figure 1.

Harsh conditions in the first year of life independently predict poor juvenile survival and reduced adult lifespan. (a) Six of the eight potential early-life adversities, and their interactions, were associated with a reduced likelihood of juvenile overwinter survival (i.e. survival past the first 200 days of life). (b) Birth date was the only factor to demonstrate a continued effect on adult lifespan for those individuals that survived their first winter. Forest plots reflect results of generalized linear mixed-effects models (a: binomial, b: Poisson) testing which early-life factors predict juvenile overwinter survival (N = 3699 squirrels) and total adult lifespan (N = 885 squirrels). Purple bars denote factors that significantly (p < 0.05) negatively correlate with survival; green bars denote factors that significantly positively correlate with survival; grey bars denote non-significant factors. SU, study area/grid named Sulphur.

Figure 2.

A second-year food boom mitigates the costs of early-life adversity for adult lifespan. Squirrels that experienced harsher conditions in their first year of life lived shorter lives (electronic supplementary material, table S2). For squirrels that did not experience a food boom event (i.e. spruce mast) in their second year of life, greater weighted early-life adversity (wELA) led to steeper declines in adult lifespan. For squirrels that did encounter a second-year food boom, greater wELA was instead associated with increased adult lifespan. Plot depicts partial residuals from a generalized linear mixed-effects model (Poisson; N = 885 squirrels).

Figure 3.

Experimental food supplementation extends lifespan but does not alter the relationship between early-life adversity and longevity. On the experimental study area, squirrels that received peanut butter at the centre of their territories lived longer adult lives than those that did not receive a bucket (electronic supplementary material, table S3), but supplemental food did not modify the relationship between wELA and adult lifespan. Plot depicts partial residuals from a generalized linear-mixed effects model (Poisson; N = 259 squirrels).