Senescence is the deterioration of physiological function with age. Understanding the reasons why individuals differ in when and how they senesce is an increasingly important challenge in modern biology, as human populations age and we seek to slow or alleviate the physiological declines that typically accompany old age. There is now very good evidence that birds and mammals show senescence in natural environments and detailed longitudinal studies of wild animals, like the Soay sheep project on St Kilda, provide potentially important systems to test how and why individuals vary in their ageing trajectories.
Research on the Soay sheep has clearly demonstrated that, like many other wild populations of mammals and birds, traits closely associated with fitness tend to increase initially through early life (in Soays, up to 2 years), then plateau through prime adulthood (2-6 years old), followed by clear senescent declines thereafter. The application of capture-mark-recapture models has demonstrated declines in the survival probability after 6 years of age in both males and females (Cathchpole et al, 2000; see figure below). Studies of female reproductive performance have found declines in the birth weight of lambs and their probability of surviving their first winter as females grow old (Clutton-Brock et al. 1992). The number of offspring sired by males also declines after 5-6 years of age (Robinson et al. 2006). As they grow old, female sheep appear to suffer higher levels of infection by parasitic worms, measured as egg counts from faecal samples (see figure below), and their lambs likewise have higher worm burdens than offspring born to younger mothers (Hayward et al. 2009, 2010). The net effect, for females at least, is a progressive decline in annual fitness from around 6 years of age onwards, as illustrated in the figure below (from Wilson et al. 2008). It is important to note that the proportion of females in the Village Bay study area the senescent age bracket (7 years old or more) is actually quite substantial. In the figure below this is shown in the green bars: geriatrics tend to make up 10-20% of the female population.
Ageing in female Soay Sheep. Bottom: Proportion of female population in different age classes; Top right, Survival probability as a function of age (from Catchpole et al. 2000); Top left: Parasite burden increases in old age in females (black dots) and males (white dots, from Hayward et al. 2009).
Having clearly demonstrated that age-related declines in fitness occur in wild Soay sheep, more recent research has tried to tackle the more challenging questions of how genes and earlier environmental conditions contribute to the rate and onset of the ageing process, and to try to understand the underlying physiological processes responsible for reduced fitness in older animals. A study led by Alastair Wilson used quantitative genetic analyses to provide evidence that variation in ageing rates in female sheep was at least partially explained by genetic causes (Wilson et al. 2007). This was one of the first studies to show this in a wild vertebrate. Subsequent studies have also suggested that past experience can play an important role in when and how quickly an individual goes into decline. A recent study, by Dan Nussey and colleagues, suggests that elderly females lose around a kilogram across the two summers before they die – but exactly how old the animal is has no bearing on this weight loss (Nussey et al., 2011). This suggests that there is considerable variation in exactly when an individual sheep starts to show serious physiological decline, although the genetic and environmental factors responsible for this variation have yet to be identified. Work by Adam Hayward and others has shown that the rate of increase in parasite level with age was exacerbated if females had experienced poorer environmental conditions earlier in their lives (Hayward et al. 2009). Ongoing work is now aimed at understanding what drives these changes in parasite levels with age, and preliminary immunological work suggests profound changes in the immune state of individuals are occurring as they age (Nussey et al. 2012 – see also Parasites & Immunity section).
There are still a great many unanswered questions when it comes to understanding why individual sheep vary so much in the onset and rate of their decline with age, and how important such variation might be for population dynamics. Ongoing work will delve deeper into the physiological processes involved – including measuring a range of immunological markers, studying telomere length and also oxidative stress. The Soay sheep population on St Kilda has incredible potential to unlock the reasons for variation in lifespan and senescence patterns in mammals experiencing complex environmental conditions – and we expect more exciting results to emerge soon!
Catchpole E.A., Morgan B.J.T., Coulson T.N., Freeman S.N. & Albon S.D. (2000). Factors influencing Soay sheep survival. Journal of the Royal Statistical Society Series C, 49, 453-472.
Clutton-Brock, T.H., Price, O.F., Albon, S.D. & Jewell, P.A. (1992) Early development and population fluctuations in Soay sheep. Journal of Animal Ecology, 61, 381-396.
Hayward, A.D., Wilson, A.J., Pilkington, J.G., Pemberton, J.M. & Kruuk, L.E.B. (2009) Ageing in a variable habitat: environmental stress affects senescence in parasite resistance in St Kilda Soay sheep. Proceedings of the Royal Society of London B, 276, 3477-3485.
Hayward A.D., Pilkington J.G., Pemberton J.M. & Kruuk L.E.B. (2010). Maternal effects and early-life performance are associated with parasite resistance across life in free-living Soay sheep. Parasitology, 137, 1261-1273.
Nussey, D.H., Coulson, T., Delorme, D., Clutton-Brock, T.H., Pemberton, J.M., Festa-Bianchet, M. & Gaillard, J.-M. (2011) Patterns of body mass senescence and selective disappearance differ among three species of free-living ungulates. Ecology, 92, 1936-1947.
Nussey D.H., Watt K., Pilkington J.G., Zamoyska R. & McNeilly T.N. (2012). Age-related variation in immunity in a wild mammal population. Aging Cell, 11, 178-180.
Robinson, M.R., Pilkington, J.G., Clutton-Brock, T.H., Pemberton, J.M. & Kruuk, L.E.B. (2006) Live fast, die young: trade-offs between fitness components and sexually antagonistic selection on weaponry in Soay sheep. Evolution, 60, 2168-2181.
Wilson, A.J., Nussey, D.H., Pemberton, J.M., Pilkington, J.G., Morris, A., Pelletier, F., Clutton-Brock, T.H. & Kruuk, L.E.B. (2007) Evidence for a genetic basis of ageing in two wild vertebrate populations. Current Biology, 17, 2136-2142.