Experimental and comparative analyses of maternal age and senescence

Abstract

Senescence is often described as an age-related physiological deterioration accompanied with declining fertility and increasing mortality, and it is believed to be the result of declining forces of natural selection. A manifestation of senescence that has attracted much recent interest is the detrimental effect of increasing maternal age acting on offspring traits. However, uncertainty arises when attempting to describe the prevalence and ubiquity of this third form of ageing and the evolutionary causes for diversity in ageing trajectories. Here I address the following questions: (1) How are maternal age effects distributed across taxa? And (2) Can an evolutionary perspective help us to understand the observed diversity in maternal age effects and demographic senescence? I addressed these through (i) a cross-fostering ageing experiment using a laboratory population of burying beetle, Nicrophorus vespilloides to decouple the separate effects of increasing pre- and postnatal maternal age, whilst accounting for the potential bias of selective disappearance. I found no evidence for maternal age effects or effects deriving from selective disappearance. These results suggest that current theory may be insufficient to account for the true diversity in ageing patterns. (ii) A meta-analytical review of maternal effect senescence to investigate the prevalence and diversity of maternal effect ageing patterns and the performance of an evolutionary model to predict observed patterns. We found taxa-wide evidence for maternal age effects on offspring survival. However the direction of these effects was based on phylogenetic constraints with laboratory and natural-mammal species showing a decline, but natural-bird species showing an ambiguous effect of maternal age. The evolutionary model was shown to improve in performance compared to evolution-agnostic demographic models when describing maternal effect ageing in natural populations. This result suggests an evolutionary cause to maternal effect senescence. (iii) Lastly, I performed a comparative analysis of vital rate selection across the tree of life. Using extensive existing databases of life history data coupled with predictions from two evolutionary theories, I derived correlations between predicted and observed vital rates across multiple animal species. I found that whilst natural selection had weak predictive power when describing patterns of mortality, age-specific fertility patterns showed extensive departures from evolutionary predictions. Additionally, I found that several biological processes were readily contributing to non-conformance of Hamilton-like ageing. Taken together, we provide convincing evidence to suggest that both natural selection and biological processes have helped shape the vast diversity of observed ageing rates that exist across the tree of life.