The Age-old question: Evolutionary causes & ecological consequences of ageing in the wild

Abstract

Iteroparous animals often express dramatic variation in life-history traits over the course of a lifetime. Understanding the evolutionary causes and ecological consequences of the age-related improvements and declines (i.e. senescence) in fitness-related traits is central to life-history theory. However, the evolution of ageing is highly complex, and poorly understood. Why is there such dramatic variability in ageing patterns not only across species, but also within species across individuals, and even within individuals across traits? In this thesis I investigate the eco-evolutionary dynamics of ageing and senescence, first broadly using a cross-species meta-analysis, and then more narrowly, using 30 years of individual-level life-history data collected on a wild population of superb fairy-wrens (Malurus cyaneus).

Chapter 1 investigates the effect of early-life environmental quality on late-life rates of senescence via a meta-analysis of studies of 14 wild populations of birds and mammals. I found no effect of early-life environment on survival senescence, but reproductive output declined more rapidly when early environmental conditions were poor. This effect of early-life environment on reproductive senescence suggests a gene-by-past-environment interaction, and indicates one mechanism by which senescence rates will vary between individuals living within a single population. I discuss the consequences of this finding for our understanding of the evolution of senescence.

Chapter 2 investigates ageing in a suite of different traits using data from a long-term study of superb fairy-wrens. While I found that survival senescence begins at the age of maturity in both sexes, the onset of senescence in some reproductive traits is substantially later, and in other reproductive traits there is no senescence at all. I suggest eco-evolutionary pathways that may explain why these traits do not age in synchrony in the fairy-wrens. Most notably, I discuss the likely role of sexual selection in driving the evolution of ageing in some traits, and as a corollary, lead to variability in ageing between traits within an individual.

Chapter 3 investigates the age-specific genetic architecture and selection on males' date of moult into breeding plumage each year, a sexually selected trait in the fairy-wrens that apparently defies senescent declines. Female fairy-wrens strongly prefer males that moult earlier in a given year. Notably, moult date continuously improves with age, despite physiological (survival) senescence co-occurring within males. I used quantitative genetic and multivariate selection models to investigate the relative roles of adaptation and constraint driving the evolution of the continuous age-related improvement in moult date.

Chapter 4 investigates broader ecological consequences of ageing, by examining if and how parental and helper ages impact the fitness of the next generation (transgenerational effects of age). I exploited the natural structure of the fairy-wren social system to disentangle germline from environmental effects of paternal age, by estimating paternal age effects in extra-pair sires that provide only genetic material, and cuckolded mates that provide only parental care. Additionally, because fairy-wrens are cooperative breeders, I tested if the ages of helpers also impact chick fitness. I show that ageing in both parents and helpers can influence the fitness of the next generation in complex ways, and that here too sexual selection likely plays a key role in driving some of the observed patterns.

My results highlight the complexity of processes shaping ageing and senescence. Through the lens of life-history theory, I illustrate here how longitudinal individual-based study of wild animal populations are a uniquely powerful tool for investigating the evolution of ageing and senescence in the natural world.