Abstract
Declines in survival and performance with advancing age (senescence) have been widely documented in natural populations, but whether patterns of senescence across traits reflect a common underlying process of biological ageing remains unclear. Senescence is typically characterized via assessments of the rate of change in mortality with age (actuarial senescence) or the rate of change in phenotypic performance with age (phenotypic senescence). Although both phenomena are considered indicative of underlying declines in somatic integrity, whether actuarial and phenotypic senescence rates are actually correlated has yet to be established. Here we present evidence of both actuarial and phenotypic senescence from a decade‐long longitudinal field study of wild insects. By tagging every individual and using continuous video monitoring with a network of up to 140 video cameras, we were able to record survival and behavioral data on an entire adult population of field crickets. This reveals that both actuarial and phenotypic senescence vary substantially across 10 annual generations. This variation allows us to identify a strong correlation between actuarial and phenotypic measures of senescence. Our study demonstrates age‐related phenotypic declines reflected in population level mortality rates and reveals that observations of senescence in a single year may not be representative of a general pattern.
Highlights
There is a broad consensus that senescence, “the age-related decline in fitness traits that arises due to internal physiological deterioration” (Rose 1991), is widespread in natural populations
This conclusion has largely been reached on the basis of measurements of demographic variables, usually longevity and fecundity, there are a growing number of studies in which phenotypic traits are measured across individual lifespans (Nussey et al 2013)
Beyond the functional explanations for asynchrony of senescence, there are statistical factors that may lead to a mismatch between actuarial and phenotypic measures of senescence, even when they would be influenced by physiological deterioration
Summary
There is a broad consensus that senescence, “the age-related decline in fitness traits that arises due to internal physiological deterioration” (Rose 1991), is widespread in natural populations This conclusion has largely been reached on the basis of measurements of demographic variables, usually longevity and fecundity, there are a growing number of studies in which phenotypic traits are measured across individual lifespans (Nussey et al 2013). Actuarial senescence is expected to be correlated with phenotypic senescence based on the assumption that physiological declines associated with ageing increase individual frailty (how likely negative environmental factors are to cause mortality in the individual). This relationship could be altered by the influence of selective disappearance and by environmental factors which affect physiological trait expression and survival differently. Empirical tests of the relationship between actuarial and phenotypic ageing trajectories will elucidate the extent to which cross-sectional demographic and longitudinal phenotypic measures of senescence provide information on a common underlying process of biological ageing
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