Before senescence: the evolutionary demography of ontogenesis

Abstract

The age-specific mortality curve for many species, including humans, is U-shaped: mortality declines with age in the developing cohort (ontogenescence) before increasing with age (senescence). The field of evolutionary demography has long focused on understanding the evolution of senescence while largely failing to address the evolution of ontogenescence. The current review is the first to gather the few available hypotheses addressing the evolution of ontogenescence, examine the basis and assumptions of each and ask what the phylogenetic extent of ontogenescence may be. Ontogenescence is among the most widespread of life-history traits, occurring in every population for which I have found sufficiently detailed data, in major groups throughout the eukaryotes, across many causes of death and many life-history types. Hypotheses seeking to explain ontogenescence include those based on kin selection, the acquisition of robustness, heterogeneous frailties and life-history optimization. I propose a further hypothesis, arguing that mortality drops with age because most transitions that could trigger the risks caused by genetic and developmental malfunctions are concentrated in early life. Of these hypotheses, only those that frame ontogenescence as an evolutionary by-product rather than an adaptation can explain the tremendous diversity of organisms and environments in which it occurs.

Quantifying Intrinsic and Extrinsic Contributions to Human Longevity: Application of a Two-Process Vitality Model to the Human Mortality Database

“…Adult extrinsic death occurs when a challenge exceeds a measure of deterministic age-dependent vitality 3. Juvenile extrinsic death occurs when a challenge exceeds a deterministic juvenile vitality that, unlike the adult deterministic vitality, begins at zero and increases to reflect increasing robustness associated with declining ontogenescent mortality with age among the very young (Levitis 2011; Levitis and Martínez 2013). For simplicity, all juvenile deaths are denoted as extrinsic.…”

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

“…Except for the characterization of survival rate (21,22), most of these approaches, in particular at physiological, cellular, and molecular levels, use linear models, but monotonic functions may have limited utility for characterizing the complex, nonlinear relationship linking age and phenotypic changes, especially across the entire life span. In fact, most characterizations only take into account senescence or ontogeny, but rarely both, which contributes to fundamental misconceptions about age-related dynamics (21,22). …”

Calculating the Rate of Senescence From Mortality Data: An Analysis of Data From the ERA-EDTA Registry

“…At the beginning of human life, negative senescence is universally observed as a decline in mortality rate caused by processes that are distinct from senescence. It may be the result of a reduction in children's vulnerability during development and growth or of a reduction in a population's vulnerability due to the early death of the frailest children and the selective survival of healthier children (33,34). In the cases of dialysis therapy (35) and kidney transplantation (36), development and growth are impaired in children, although the deficits are partly compensated at a later age.…”