Do Early-Life Conditions Drive Variation in Senescence of Female Bighorn Sheep?

Abstract

The rate of senescence may vary among individuals of a species according to individual life histories and environmental conditions. According to the principle of allocation, changes in mortality driven by environmental conditions influence how organisms allocate resources among costly functions. In several vertebrates, environmental conditions during early life impose trade-offs in allocation between early reproduction and maintenance. The effects of conditions experienced during early life on senescence, however, remain poorly documented in wild populations. We examined how several early-life environmental conditions affected reproductive and survival senescence in wild bighorn sheep. We found long-term effects of high population density at birth, precipitations during the winter before birth, and temperature during the winter following birth that decreased survival after 7 years of age. High temperature during the first summer and autumn of life and high Pacific decadal oscillation decreased reproductive success at old ages. However, harsh early-life environment did not influence the rate of senescence in either survival or reproduction. Contrary to our expectation, we found no trade-off between reproductive allocation prior to senescence and senescence. Our results do show that early-life environmental conditions are important drivers of later survival and reproductive success and contribute to intra-specific variation in late-life fitness, but not aging patterns. These conditions should therefore be considered when studying the mechanisms of senescence and the determinants of variation in both survival and reproductive senescence at older ages.

Different proxies, different stories? Imperfect correlations and different determinants of fitness in bighorn sheep

“…We considered some determinants over the entire adulthood (≥2 years old) of an individual and at birth since early‐life conditions have long‐lasting effects on fitness in bighorn sheep (Pigeon & Pelletier, 2018 ). For individual traits, we used age at first reproduction, longevity, body mass at weaning and as a yearling since they are known to affect lifetime reproductive success in large mammals (Festa‐Bianchet et al, 2019 ; Pigeon et al, 2021 ; Pigeon & Pelletier, 2018 ; Zedrosser et al, 2013 ). Using repeated measurements of sheep mass during the growing season, we adjusted body mass at weaning and yearling mass to September 15 using mixed models (Martin & Pelletier, 2011 ).…”

Trait-dependent associations between early- and late-life reproduction in a wild mammal

“…Life-history theory of ageing predicts that these declines may reflect a delayed cost of investment in reproduction, with females that breed successfully in the first few years of life allocating relatively less to somatic maintenance and consequently suffering more rapid senescence [9]. This pattern has been observed in some wild vertebrate study systems [20,25,26], but not in others [18,19,21]. Our results suggest that the detectability of long-term costs of early-life reproductive allocation may depend on the reproductive trait being investigated, which may help explain the mixed evidence from field studies to date.…”

“…While there is widespread evidence that reproductive traits show senescent declines in wild vertebrates [13,14], there is also increasing evidence of asynchrony of senescence among reproductive traits within populations [3,15,16]. While early-late trade-offs are well documented in laboratory model organisms [17], evidence from natural systems remains mixed [18][19][20][21] as heterogeneity among individuals in resource acquisition and selective disappearance can mask both trade-offs and ageing patterns [22][23][24]. Recent studies confirm that where longitudinal lifelong data are available and appropriate statistical controls are used to account for heterogeneity, earlylate trade-offs can be detected in wild populations [11,25,26].…”

Editorial: Mechanisms and Pathways Contributing to the Diversity of Aging Across the Tree of Life

“…This opened the door to studies examining the eco-evolutionary aspects of senescence in the wild. In our Research Topic, the study by Pigeon and others (Pigeon et al, 2021) on bighorn sheep is an excellent example of this work. Their study asks whether patterns of senescence in reproduction and survival may be influenced by environmental conditions during early development.…”