Long-term fitness consequences of early environment in a long-lived ungulate

Abstract

Cohort effects can be a major source of heterogeneity and play an important role in population dynamics. Silver-spoon effects, when environmental quality at birth improves future performance regardless of the adult environment, can induce strong lagged responses on population growth. Alternatively, the external predictive adaptive response (PAR) hypothesis predicts that organisms will adjust their developmental trajectory and physiology during early life in anticipation of expected adult conditions but has rarely been assessed in wild species. We used over 40 years of detailed individual monitoring of bighorn ewes (Ovis canadensis) to quantify longterm cohort effects on survival and reproduction. We then tested both the silver-spoon and the PAR hypotheses. Cohort effects involved a strong interaction between birth and current environments: reproduction and survival were lowest for ewes that were born and lived at high population densities. This interaction, however, does not support the PAR hypothesis because individuals with matching high-density birth and adult environments had reduced fitness. Instead, individuals born at high density had overall lower lifetime fitness suggesting a silver-spoon effect. Early-life conditions can induce long-term changes in fitness components, and their effects on cohort fitness vary according to adult environment.

Delayed spring onset drives declines in abundance and recruitment in a mountain ungulate

“…, Martin and Festa‐Bianchet , , Pigeon et al. ), and high densities can increase the risk of population declines in relation to extreme weather events (Portier et al. , Coulson et al.…”

Long‐term studies of bighorn sheep and mountain goats reveal fitness costs of reproduction

“…Lactating mountain goats spent more time grazing and more time ruminating while lying compared to non‐lactating females (Hamel & Côté, ). Mass, however, was not the sole determinant of reproductive potential, as cohort effects on reproductive success remained substantial even after differences in mass were accounted for, generating positive correlations between survival and reproduction (Pigeon, Festa‐Bianchet, & Pelletier, ). Early environmental conditions also affected variation in female reproductive potential of cohorts of both species (Hamel et al ).…”

Trophy hunting mediates sex‐specific associations between early‐life environmental conditions and adult mortality in bighorn sheep

“…However, the slope of the relationship between early environment and age at first reproduction did not vary much when accounting for individual yearling mass (−0.29 ± 0.05 vs. −0.33 ± 0.05). In this population, females born at low density are at a reproductive advantage compared to those born at high density (Pigeon et al., ). Overall, these results support the existence of silver‐spoon effects in females.…”

“…Contrary to what the external PAR hypothesis predicts, we found no interaction between early and current environmental conditions on mortality risk in either sex. In addition, the external PAR does not hold for annual reproductive success in female bighorn sheep (Pigeon et al., ). There is an overall lack of support for the external PAR in long‐lived species (humans: Hayward, Rickard, & Lummaa, ; roe deer: Douhard et al., ; baboons: Lea, Altmann, Alberts, & Tung, ; mountain goats: Panagakis, Hamel, & Côté, ), as well as in a range of other organisms (Briga, Koetsier, Boonekamp, Jimeno, & Verhulst, ; Uller, Nakagawa, & English, ).…”

“…We take advantage of a detailed long‐term monitoring of wild bighorn sheep ( Ovis canadensis ) to evaluate whether and how early environment influences adult mortality in females and males. In this population, the effects of population density in the year of birth on life span of females have been described (Pigeon, Festa‐Bianchet, & Pelletier, ; Pigeon & Pelletier, ). However, a comparison of the effects of early environment (sensu Lindström, ) on adult mortality in either sex has not been made.…”