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.

Fig. 1.

Relationship between the rate of aging (ω) and gestation period (GP) in mammals analyzed at the levels of species, family, and order. Regression equations at each level are: order (F_1,13 = 29.5, P < 0.0001, r² = 0.694), ω = 0.040 (± 0.176 SE) − 0.463 (0.085) GP; family (F_1,50 = 48.0, P < 0.0001, r² = 0.490), ω = 0.027 (0.147) – 0.489 (0.071) GP; species (F_1,158 = 100.5, P < 0.0001, r² = 0.389), ω = 0.088 (0.110) – 0.512 (0.051) GP.

Fig. 2.

Species-level relationships between potential life span (1/ω, in years) and lengths of the embryo, postnatal growth, and prereproductive periods as a function of body mass in birds (open symbols) and mammals (solid symbols). The relationship between birds and mammals with respect to the rate of aging most closely matches that with respect to age at sexual maturity.

Fig. 3.

Family-level relationships between the rate of aging (ω) and the embryo development period (Left) and age at maturity (Right). The relationships for each of the classes match well with respect to age at maturity; crocodilians and tortoises are outliers among the reptiles, because they have relatively high rates of aging for their ages at maturity.

Fig. 4.

Distribution of the ages at sexual maturity relative to postnatal growth rate. Black bars represent the relative numbers of species that become sexually mature at different times relative to their postnatal growth. Growth curves in the background are Gompertz functions that describe mass at time t as W(t) = Aexp[−bexp(−kt)], where A is the asymptote of the growth curve, k is the growth-rate constant (1/time), and b is ln[A/W(0)]. The curves have asymptotes of 100 units and initial masses [W(0)] of 2, 4, 6, 8, and 10 units, and they are plotted as a function of relative time (kt). When W(0) = 2, for example, 50% of the asymptote is reached at kt = 1.7, 90% at kt = 3.6, and 95% at kt = 4.3. The relative time at sexual maturity for each species is the product of the species’ growth-rate constant (k; [1/days]) and age at sexual maturity (days), resulting in a dimensionless number. Because birds grow very rapidly compared with mammals, most species of bird mature well after reaching full size, whereas many species of mammal mature well below their eventual adult mass.

Fig. 5.

(Left) Annual fecundity (B) increases linearly in relation to annual mortality (1 − S) in samples of avian and mammalian life histories. Data for birds are from (birds I) Saether and Bakke (60) (50 species; female offspring per female) and (birds II) Ricklefs (49) (34 species; offspring per pair), and data for mammals are from Millar and Zammuto (61) (29 species; litter size). The slopes of the relationships passed through the origin were 3.34 (± 0.25 SE), 5.68 (± 0.37 SE; M < 0.8), and 11.34 (± 0.80 SE), respectively. (Right) The relationship between age at maturity (a) and −1/ln(S). The straight lines show the expected relationship between age at maturity and expected adult life span for different ratios of annual fecundity to annual adult mortality (B/M) in a stable population (Eq. 1). The slopes of the linear relationships [log(B/M)] were 0.519 (± 0.028 SE), 0.477 (± 0.024 SE), and 0.674 (± 0.028 SE), respectively. (Appendix S3 has further details.

Fig. 6.

The rate of actuarial senescence (ω) in mammals as a function of body mass (Left) and age at maturity (Right). Whereas bats (Chiroptera) and primates age slowly for their size, their rate of aging falls into line with other mammals relative to the age at maturity. Note: If you cannot distinguish the colors in this figure and would like more information, please contact the author.