Transgenerational effects of parental age on fitness.

Lead Research Organisation: University of Sheffield
Department Name: Animal and Plant Sciences

Abstract

Why do organisms age? This is one of the big, unsolved questions in biology, because it is unclear how a process that ultimately decreases fitness can persist evolutionarily, and why species do not evolve to live longer. Many theories have been put forward to explain from an evolutionary perspective why organisms change with age, but it is likely that many factors contribute to the phenomenon. One factor that can strongly affect selection pressure for longevity has, however, not received much attention: the transgenerational effects of senescence. Epigenetic effects can strongly affect the predicted outcome of certain evolutionary models. One such epigenetic and trans-generational factor that affects fitness is maternal age. It has been known for nearly a century that a mother's age can affect her offspring's, and potentially even her grand-offspring's, fitness. However, all the relevant studies have been done in the laboratory. Therefore, it is unknown whether this effect of maternal age operates in wild populations, and whether it can contribute to our understanding of the evolution of longevity.
We propose to study the effects of parental and grand-parental age on their offspring's lifespan, reproductive success, physiology and genetics in a wild population of house sparrows. We have data available from a uniquely suited, long-term study of house sparrows in which to examine these topics in detail. Only in a closed population such as the one that we have is it possible to accurately estimate lifespan, fitness and parentage, which are all prerequisites for the longitudinal study of parental age on individual fitness. In addition, we will use focused experiments with captive birds to cement our hypotheses, and individual-based simulation models to explore quantitatively the implications of maternal age effects on the evolution of longevity.
We expect the epigenetic effects of maternal age on offspring fitness to have important consequences on the demography of a population, and in turn also on the balance of the classic trade-off between reproduction and survival. Ultimately, these effects will strongly affect the selection pressures acting on longevity itself, and should lead to novel theories of the evolution of longevity.

Planned Impact

Non-academic beneficiaries:

The question of why most organisms are not immortal is probably as old as the human race, and with the shift in demography towards ageing populations in western countries, its political and societal relevance is more pronounced than ever. We propose to investigate the function and mechanism behind transgenerational senescence - where the age of the parents at birth negatively affects the life of their offspring. This will improve our understanding of the phenomenon of reproductive senescence, menopause and the evolution of lifespan.
The study will also provide practical information on what to study next in the quest for a remedy against the phenotypic consequences of ageing, especially for reproductive biology. On average, couples have their first child more than ten years later in life now than just a few decades ago. This increase in age at first reproduction has come at a cost: higher chances of miscarriage and infertility of aged gametes, both male and female, to name just a few. The remedies of assisted fertilisation are complex and expensive. Our project will potentially start to pin down the mechanisms leading to decreased fertility at old age and provide a starting point for future research geared towards the alleviation of these problems.
Endangered animal species may profit more immediately from our research. Species on the brink of extinction are often maintained in complicated breeding programmes in zoos, where individuals are ideally mated with each other according to their pedigree-determined relatedness in order to preserve genetic diversity. Our research points to a factor that has not yet been incorporated in those models: if not accounted for, effects of parental age could diminish these efforts if offspring from older parents have a lower reproductive value. A similar case can be made for the breeding of domesticated animals, including agricultural species and racehorses.
Finally, non-academics, ornithologists and naturalists take a substantial interest in the fate of house sparrows in the UK. House sparrows are currently in sharp decline in the UK, and more so in urban areas. The health of farmland bird populations more generally has been used by the UK government as an index of environmental sustainability. Our proposed research will explore the fitness, and therefore also the demographic consequences of an ageing population in house sparrows, which will garner interest and enable outreach activities across the public more broadly.

Publications

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Hsu YH (2014) Costly infidelity: low lifetime fitness of extra-pair offspring in a passerine bird. in Evolution; international journal of organic evolution

 
Description We have published numerous papers describing the results of the study but some of the key ones are still in progress, and those and their findings will be reported in due course.
Exploitation Route They will stimulate further scientific discovery.
Sectors Environment

 
Description We engaged with the Berlin zoo in particular as planned in our pathways to impact. This involved a useful exchange of knowledge on the potential effect of ageing on the quality of the offspring of endangered captive animas. It became apparent that taking this further to the point of being useful will require substantial collation and analysis of data beyond the scope of the activity supported within the grant. We are hoping however that the captive breeding community will pick up on this and take the work forward, to the potential benefit of their operations and conservation science.
First Year Of Impact 2015
Sector Environment
Impact Types Cultural