Asynchrony of senescence among phenotypic traits in a wild mammal population

Abstract

The degree to which changes in lifespan are coupled to changes in senescence in different physiological systems and phenotypic traits is a central question in biogerontology. It is underpinned by deeper biological questions about whether or not senescence is a synchronised process, or whether levels of synchrony depend on species or environmental context. Understanding how natural selection shapes patterns of synchrony in senescence across physiological systems and phenotypic traits demands the longitudinal study of many phenotypes under natural conditions. Here, we examine the patterns of age-related variation in late adulthood in a wild population of Soay sheep (Ovis aries) that have been the subject of individual-based monitoring for thirty years. We examined twenty different phenotypic traits in both males and females, encompassing vital rates (survival and fecundity), maternal reproductive performance (offspring birth weight, birth date and survival), male rutting behaviour, home range measures, parasite burdens, and body mass. We initially quantified age-related variation in each trait having controlled for annual variation in the environment, among-individual variation and selective disappearance effects. We then standardised our age-specific trait means and tested whether age trajectories could be meaningfully grouped according to sex or the type of trait. Whilst most traits showed age-related declines in later life, we found striking levels of asynchrony both within and between the sexes. Of particular note, female fecundity and reproductive performance declined with age, but male annual reproductive success did not. We also discovered that whilst home range size and quality decline with age in females, home range size increases with age in males. Our findings highlight the complexity of phenotypic ageing under natural conditions and, along with emerging data from other wild populations and laboratory models, suggest that the long-standing hypothesis within evolutionary biology that fitness-related traits should senesce in a synchronous manner is seriously flawed.

Age-Related Changes in Locomotor Performance Reveal a Similar Pattern forCaenorhabditis elegans,Mus domesticus,Canis familiaris,Equus caballus, andHomo sapiens

“…For example, in C elegans, the difference in locomotor activity peak age between voluntary activity and forced electrotactic conditions might be related to a wide variability of aging effects on muscular and neuronal structures (12). Such an asynchrony among phenotypic traits has already been described for several species in both laboratory and natural conditions (17,49).…”

“…Because locomotion is a highly integrated trait (2,3), differences in the age at peak performance among different types of performance might be related to functional or structural differences in senescence of physiological traits (49). For example, in C elegans, the difference in locomotor activity peak age between voluntary activity and forced electrotactic conditions might be related to a wide variability of aging effects on muscular and neuronal structures (12).…”

The Evolution of Lifespan and Age-Dependent Cancer Risk

“…This perspective helps explain why animals rarely have cancer in the wild, since many animals simply do not survive to the age when cancer becomes a risk factor (Figure 2C). Senescence appears to be common in some groups of wild animals [38,39], however cancer demography data are lacking from wild populations and more research is needed to elucidate if cancer rates are higher in aged wild animals. It is also unclear how senescence in wild populations affects the overall odds of reproductive success, which is the key regulator of the age-dependent strength of germline selection.…”

Genes of susceptibility to early neurodegenerative changes in the rat retina and brain: analysis by means of congenic strains

“…Studying ageing is a challenging task because of the complexity of the aging process and the asynchrony of senescence that was documented in humans, laboratory models, and wild animals [32–34] as well as among phenotypic traits of a natural population [35]. The aging population is diverse genetically and is heterogeneous in terms of diseases and comorbidities.…”