Testing the evolutionary theory of senescence in wild vertebrate and historical human populations

Lead Research Organisation: University of Edinburgh
Department Name: Sch of Biological Sciences

Abstract

Ageing, or senescence, is a central focus of current research across a wide range of biological disciplines, as well as a topic of wider public and governmental concern. Our understanding of the processes responsible for ageing is limited by the paucity of research into the evolution of senescence undertaken in natural settings. Organisms in nature experience an inevitable risk of death from environmental causes, and this leads to a decline in the force of natural selection with age. It is now widely accepted that senescence evolves as a bi-product of this weakening selection. Classical theory predicts that increasing the risk of mortality will result in the evolution of faster senescence rates. However, more recent theory has shown that this prediction is over-simplistic and may not apply outside of the laboratory. Conventional wisdom also states that the weakening force of selection with age allows senescence to evolve via two different genetic mechanisms, known as 'antagonistic pleiotropy' and 'mutation accumulation'. However, the roles that these mechanisms actually play are poorly understood in natural animal populations, including humans. My research will address these two major challenges to our understanding of evolution of senescence. Determining the causes of variation in individual mortality risk and senescence rates in natural populations is required to understand the evolution of senescence. I will use data collected from long-term individual-based studies of four wild vertebrate populations to test the effects of shared genes and environments on variation in adult mortality risk. I will also test for differences in senescence rates associated with sex and environmental quality. In order to test the roles of the two genetic mechanisms thought to be responsible for the evolution of senescence, I will analyse data from wild vertebrate and historical human populations. I will use historical human data sets to provide the first simultaneous tests of both genetic mechanisms of senescence in a natural population. My analyses will produce general, rather than just system-specific, tests of key hypotheses regarding the evolution of senescence in nature. Advancing our understanding of senescence in natural systems will benefit the wide range of biological disciplines involved in research into ageing, including population ecology, evolutionary biology, veterinary and medical sciences, molecular and cell biology and physiology.

Publications

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Milot E (2011) Evidence for evolution in response to natural selection in a contemporary human population. in Proceedings of the National Academy of Sciences of the United States of America

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Monaghan P (2008) The evolutionary ecology of senescence in Functional Ecology

 
Description My work over the course of this postdoctoral fellowship has substantially advanced our understanding of the causes and consequences of individual variation in ageing in wild animal populations. Since starting the fellowship, I have produced 10 peer-reviewed publications (see publication list section) and have several more manuscripts related directly to the aims in the fellowship proposal currently either in review or in preparation. In the work published since the fellowship began, I have presented some of the most compelling evidence to date in support of evolutionary theories of ageing from wild animal populations. I have been to show that, in wild ungulates:
- As predicted by evolutionary theory, variation in ageing rates in annual fitness traits has an additive genetic basis.
- As predicted by the antagonistic pleiotropy theory of ageing, investment in reproduction in early life results in more rapid ageing rates in later life and that this trade-off has a genetic basis.
- Poor environmental conditions in early life exacerbate ageing rates in survival and reproduction in later adulthood.
- As classical evolutionary theory predicts, males show more rapid reproductive senescence than females but - unexpectedly - different reproductive traits senesce at different rates within each sex.
- As predicted by free radical theories of ageing and life history evolution, faster growth in early life is associated with increased levels of oxidative damage, although oxidative damage does not appear to increase with age.

During the fellowship, I was also invited to co-edit and contribute a review to a special themed issue of the journal Functional Ecology on 'the evolutionary ecology of senescence' in 2008. More recently, I was also invited to help produce a unique guide to the application of quantitative genetic analytical techniques for ecologists for Journal of Animal Ecology. I have co-organised a day-long symposium on ageing in wild populations as part of the 2007 European Society for Evolutionary Biology Congress in Uppsala, Sweden. I recently helped set up an organisation that aims to bring together researchers interested studying ageing from across Scottish universities on an annual basis (Scottish Ecological Ageing Research Group), the second annual meeting of which ran successfully in summer 2010.

As the above shows, I have achieved the core aims set out in my original proposal, namely, to test key evolutionary predictions regarding the causes of variation in ageing rates in natural populations. This work, as well as the invited reviews and meetings / conferences I have been involved in over the last three years, have helped to fuel and develop rapidly growing interest in studying senescence within evolutionary ecology.

Some of the work in the original proposal is still ongoing and I expect this will result in publications over the coming year or so. The work proposed on the historical human populations in Quebec has begun to bear fruit after considerable efforts to organise the data set into a manageable database format. Analyses investigating the fitness consequences of inbreeding and the quantitative genetics of fitness in the Isle-aux-Coudres population are now complete and produced a paper in PNAS. Ongoing investigations of senescence in body mass and factors influencing actuarial senescence in several wild ungulate populations (collaborators: J Pemberton, L Kruuk, T Clutton-Brock, T Coulson, J-M Gaillard & M Festa-Bianchet) have resulted in a paper in Ecology.

Finally, the support provided by this postdoctoral fellowship has allowed me to establish new collaborations with researchers working on other systems and in different fields and obtain funding to pursue these new research questions. I am co-investigator on recently funded NERC response mode grant to study ageing in a wild mongoose population and have recently been awarded a BBSRC David Phillips fellowship to follow-on from the NERC postdoctoral fellowship to study the links between early-life experiences and ageing in a wild sheep population.
Exploitation Route Ultimately, they lay groundwork for improved understanding of the causes of individual variability in the ageing process. Ongoing collaborations are actively relating findings and approaches used in the fellowship to domestic ruminant health and management.
Sectors Agriculture, Food and Drink,Environment

URL http://nussey.bio.ed.ac.uk/