Daniel H. Nussey

The evolutionary ecology of individual phenotypic plasticity in wild populations

The ability of individual organisms to alter morphological and life‐history traits in response to the conditions they experience is an example of phenotypic plasticity which is fundamental to any populations ability to deal with short‐term environmental change. We currently know little about the prevalence, and evolutionary and ecological causes and consequences of variation in life history plasticity in the wild. Here we outline an analytical framework, utilizing the reaction norm concept and random regression statistical models, to assess the between‐individual variation in life history plasticity that may underlie population level responses to the environment at both phenotypic and genetic levels. We discuss applications of this framework to date in wild vertebrate populations, and illustrate how natural selection and ecological constraint may alter a populations response to the environment through their effects at the individual level. Finally, we present future directions and challenges for research into individual plasticity.

Environmental conditions in early life influence ageing rates in a wild population of red deer

Summary The process of ageing, or senescence, is an important focus of current research, but our knowledge of the factors influencing ageing rates in naturally occurring populations remains poor [1]. A growing number of studies of wild vertebrate and human populations has shown that environmental conditions early in life can have long-term effects on fitness-correlated traits [2,3]. However, the consequences of early-life environment for ageing rates remain unknown [4]. Using data collected over 35 years from a wild population of red deer ( Cervus elaphus ), we show that females experiencing high levels of resource competition during early life showed faster rates of senescence as adults. Our results suggest that rather than inducing adaptive shifts in developmental trajectories, harsh early-life conditions may constrain development and ultimately exacerbate the ageing process.

Evidence for a genetic basis of aging in two wild vertebrate populations

Aging, or senescence, defined as a decline in physiological function with age, has long been a focus of research interest for evolutionary biologists. How has natural selection failed to remove genetic effects responsible for such reduced fitness among older individuals? Current evolutionary theory explains this phenomenon by showing that, as a result of the risk of death from environmental causes that individuals experience, the force of selection inevitably weakens with age. This in turn means that genetic mutations having detrimental effects that are only felt late in life might persist in a population. Although widely accepted, this theory rests on the assumption that there is genetic variation for aging in natural systems, or (equivalently), that genotype-by-age interactions (GxA) occur for fitness. To date, empirical support for this assumption has come almost entirely from laboratory studies on invertebrate systems, most notably Drosophila and C. elegans, whereas tests of genetic variation for aging are largely lacking from natural populations. By using data from two wild mammal populations, we perform quantitative genetic analyses of fitness and provide the first evidence for a genetic basis of senescence to come from a study in the natural environment. We find evidence that genetic differences among individuals cause variation in their rates of aging and that additive genetic variance for fitness increases with age, as predicted by the evolutionary theory of senescence.

Testing for genetic trade-offs between early- and late-life reproduction in a wild red deer population

The antagonistic pleiotropy (AP) theory of ageing predicts genetically based trade-offs between investment in reproduction in early life and survival and performance in later life. Laboratory-based research has shown that such genetic trade-offs exist, but little is currently known about their prevalence in natural populations. We used random regression ‘animal model’ techniques to test the genetic basis of trade-offs between early-life fecundity (ELF) and maternal performance in late life in a wild population of red deer (Cervus elaphus) on the Isle of Rum, Scotland. Significant genetic variation for both ageing rates in a key maternal performance measure (offspring birth weight) and ELF was present in this population. We found some evidence for a negative genetic covariance between the rate of ageing in offspring birth weight and ELF, and also for a negative environmental covariance. Our results suggest rare support for the AP theory of ageing from a wild population.

Constraints on plastic responses to climate variation in red deer

Influences of climate on life history traits in natural populations are well documented. However, the implications of between-individual variation in phenotypic plasticity underlying observed trait–environment relationships are rarely considered due to the large, long-term datasets required for such analysis. Studies typically present correlations of annual trait means with climate or assume that individual phenotypic responses are constant. Here, we examine this additional level of variation and show that, in a red deer population on the Isle of Rum, Scotland, changes in climate generate changes in phenotype only amongst individuals who have experienced favourable ecological conditions. Examination of relationships between offspring birth weight and spring temperature within the lifetimes of individual females revealed that the tendency to respond to climate declined as the population density experienced early in life increased. The presence of such systematic variation in individual plasticity is rarely documented in the wild, and has important implications for our understanding of the environmental dependencies of traits under varying ecological conditions.