Life-history connections to rates of aging in terrestrial vertebrates

Abstract

The actuarial senescence (i.e., the rate of increase in adult mortality with age) was related to body mass, development period, and age at sexual maturity across 124 taxonomic families of terrestrial vertebrates. Model selection based on Akaike's information criterion values adjusted for small size showed that the rate of aging decreases with increasing body mass, gestation period, age at maturity, and possession of flight. Among families of mammals, actuarial senescence was related to extrinsic mortality rate (standardized regression coefficient = 0.215), gestation period (−0.217), and age at maturity (−0.553). Although rate of aging in birds also was related to the embryo development period, birds grow several times more rapidly than mammals, and therefore, the connection between rate of early development and rate of aging is unclear. The strong vertebrate-wide relationship between rate of aging, or life span, and age at maturity can be explained by density-dependent feedback of adult survival rate on the recruitment of young individuals into the breeding population. Thus, age at maturity seems to reflect extrinsic mortality, which, in turn, influences selection on mechanisms that postpone physiological and actuarial senescence. Because rate of embryo development influences rate of aging independently of the age at maturity, in a statistical sense, the evolutionary diversification of development and aging seem to be connected in both birds and mammals; however, the linking mechanisms are not known.birds | embryo development | mammals | reptiles | sexual maturity M ost biologists accept that the rate of aging has a genetic basis and is under selection (1-3). However, evolutionary adaptations that influence the rate of aging and differentiate potential life span among species are poorly understood. Mechanisms related to the rate of aging that evolve under selection might, or might not, correspond to molecular and biochemical processes of interest to biologists who investigate the aging process in humans and model organisms. These processes include the production of reactive oxygen species (ROS) and control of oxidative damage (4, 5), telomere shortening, which influences cell replication (6-8), various signaling pathways that produce antagonisms between development and aging (9-11), and inflammation responses that produce antagonisms between disease prevention and tissue damage (12). However, other processes, particularly developmental mechanisms that influence the quality of the adult individual, might be brought into play by evolution.Comparative analyses of the rate of aging, or some proxy such as maximum life span, have been used to support various ideas about aging (13-16). For example, the pervasive relationship between life span and body mass was viewed as support for a relationship between metabolism and life span-the so-called rate-of-living hypothesis (17, 18). However, comparative analyses also have been used to test falsifiable hypotheses. In the case of the rate of living hypothesis, for example, th...

Accelerated protein evolution analysis reveals genes and pathways associated with the evolution of mammalian longevity

“…In our analysis, we found many proteins involved in development and growth resulting in functional categories such as muscle development, postsynaptic density, and spermatid development. These results, among others (see Supplementary material for full results), could be interpreted as proteins that were selected for phenotypes that correlate longevity, such as body size or brain size Austad 2009;Ricklefs 2010). Therefore, some of our results may be due to selection on other life history traits apart from longevity.…”

Ecology and mode-of-life explain lifespan variation in birds and mammals

“…[3,5,6]). However, our study is the first, to our knowledge, to demonstrate the general importance of body size in both volant and non-volant species concurrently (as opposed to traditional taxonomic groupings of birds, bats and terrestrial mammals separately).…”

“…Maximum lifespan in vertebrates, for example, ranges from up to 211 years in the bowhead whale (Balaena mysticetus; [1]), down to just eight weeks in the pygmy goby (Eviota sigillata; [2]). Like most other life-history traits, lifespan varies strongly with body size such that large species tend to live longer than smaller species [3][4][5][6]. However, many species have far longer, or indeed shorter, lives than expected given their body mass (figure 1).…”

Constraints and flexibility in mammalian social behaviour: introduction and synthesis

“…Mammals are an excellent taxon in which to investigate constraints and flexibility in social behaviour because they show an extremely broad range of social systems, along with equivalent variation in social complexity, behavioural flexibility, brain size and cognitive abilities [16][17][18][19]. Compared with other taxa whose social behaviour has been well studied, notably birds and social insects, mammals exhibit more interspecific variation in the pace of development (which affects time available for learning), length of the lifespan (which influences options to establish and manage multiple, long-term individualized social relationships in complex networks) and finally, brain size (which modulates behavioural decisions through variable cognitive abilities).…”