Evolutionary ecology of senescence and a reassessment of Williams' 'extrinsic mortality' hypothesis

The evolutionary theory of senescence underpins research in life history evolution and the biology of aging. In 1957 G.C. Williams predicted that higher adult death rates select for earlier senescence and shorter length of life, but pre- adult mortality doesn’t matter to evolution. This was subsequently interpreted as predicting that senescence should be caused by 'extrinsic' sources of mortality. This idea still motivates empirical studies, even though formal, mathematical theory shows it is wrong. It has nonetheless prospered because it offers an intuitive explanation for patterns observed in nature. We review the flaws in Williams' model, explore alternative explanations for comparative patterns that are consistent with the evolutionary theory of senescence and discuss how hypotheses based upon it can be tested. We argue that focussing on how sources of mortality affect ages differently offers greater insight into evolutionary processes

Immunosenescence in wild animals:Meta-analysis and outlook

Immunosenescence, the decline in immune defense with age, is an important mortality source in elderly humans but little is known of immunosenescence in wild animals. We systematically reviewed and meta-analysed evidence for age-related changes in immunity in captive and free-living populations of wild species (321 effect sizes in 62 studies across 44 species of mammals, birds and reptiles). As in humans, senescence was more evident in adaptive (acquired) than innate immune functions. Declines were evident for cell function (antibody response), the relative abundance of naive immune cells and an in vivo measure of overall immune responsiveness (local response to phytohaemagglutinin injection). Inflammatory markers increased with age, similar to chronic inflammation associated with human immunosenescence. Comparisons across taxa and captive vs free-living animals were difficult due to lack of overlap in parameters and species measured. Most studies are cross-sectional, which yields biased estimates of age-effects when immune function co-varies with survival. We therefore suggest longitudinal sampling approaches, and highlight techniques from human cohort studies that can be incorporated into ecological research. We also identify avenues to address predictions from evolutionary theory and the contribution of immunosenescence to age-related increases in disease susceptibility and mortality

Why do female migratory birds arrive later than males?

1 In migratory birds males tend to arrive first on breeding grounds, except in sex-role reversed species. The two most common explanations are the rank advantage hypothesis, in which male–male competition for breeding sites drives stronger selection for early arrival in males than females, and the mate opportunity hypothesis, which relies on sexual selection, as early arrival improves prospects of mate acquisition more for males than for females. 2 To date, theoretical work has focused on selection for early arrival within a single sex, usually male. However, if fitness depends on territory quality, selection for early arrival should operate on both sexes. Here we use two independent modelling approaches to explore the evolution of protandry (male-first arrival) and protogyny (female-first arrival) under the rank advantage and mate opportunity hypotheses. 3 The rank advantage hypothesis, when operating alone, fails to produce consistent patterns of protandry, despite our assumption that males must occupy territories before females. This is because an individual of either sex benefits if it out-competes same-sex competitors. Rather than promoting protandry, the rank advantage mechanism can sometimes result in protogyny. Female–female competition is stronger than male–male competition early in the season, if females compete for a resource (territories occupied by males) that is initially less common than the resource of interest to males (unoccupied territories). 4 Our results support the mate opportunity hypothesis as an explanation of why protandry is the norm in migratory systems. Male-biased adult sex ratios and high levels of sperm competition (modelled as extra-pair young: EPY) both produce protandry as a result of sexual selection. Protogyny is only observed in our models with female-biased sex ratios and low EPY production. 5 We also show that the effects of sex ratio biases are much stronger than those of EPY production, explore the evidence for sex ratio biases and extra-pair paternity in migratory species and suggest future research directions

Tooth microstructure tracks the pace of human life-history evolution

A number of fundamental milestones define the pace at which animals develop, mature, reproduce and age. These include the length of gestation, the age at weaning and at sexual maturity, the number of offspring produced over a lifetime and the length of life itself. Because a time-scale for dental development can be retrieved from the internal structure of teeth and many of these life-history variables tend to be highly correlated, we can discover more than might be imagined about fossil primates and more, in particular, about fossil hominids and our own evolutionary history. Some insights into the evolutionary processes underlying changes in dental development are emerging from a better understanding of the mechanisms controlling enamel and dentine formation. Our own 18–20-year period of growth and development probably evolved quite recently after ca 17 million years of a more ape-like life-history profile