Award details

Male ageing and the ejaculate: composition, competition and conflict

Reference	BB/K014544/1
Principal Investigator / Supervisor	Dr Stuart Wigby
Co-Investigators / Co-Supervisors
Institution	University of Oxford
Department	Zoology
Funding type	Research
Value (£)	1,075,911
Status	Completed
Type	Fellowships
Start date	31/03/2014
End date	31/01/2021
Duration	82 months

Abstract

Our understanding of the biology of ageing is rapidly advancing. However, the biology and evolutionary consequences of male reproductive ageing remain relatively poorly understood. This is an important omission given that male reproductive activity has wide evolutionary consequences in many species, and that - from a human perspective - there is a strong trend for delayed fatherhood. Using Drosophila melanogaster, a model organism for ageing research and for ejaculate research, I will 1) investigate how ageing affects the male ejaculate and variables that influence the rate of ejaculate ageing and 2) test the consequences, for sexual selection and sexual conflict, of male ageing of the ejaculate. In part 1, I will test how the composition of the ejaculate changes with male age by quantifying sperm production and the seminal proteome within males throughout lifespan, and how this relates to the ejaculate components transferred to females at mating. I will assess how male condition, mating history, and interventions that extend lifespan, impact the rate of ejaculate ageing. I will use the information from Part 1, evolutionary theory, and knowledge about the proximate function of sperm and seminal proteins, to make predictions about how ejaculate ageing should influence sexual selection and conflict. In Part 2 I will test these predictions by assaying the effect of ejaculate ageing on female fecundity, fertility and fitness, and on the post-mating competitiveness of males. I will use genetic tools to reveal which specific ejaculate components are important in mediating the ejaculate ageing effects. The work will drive ejaculate research forward into the proteomic era, and will integrate this with functional genetics, molecular biology, gerontology and evolutionary ecology to provide a new level of understanding of the reproductive consequences of ageing and their impact upon inter- and intra-sexual dynamics.

Summary

Parents are becoming older. In the UK, the US and other developed countries, there is a trend for people to have children later, and with this trend comes a suite of potential difficulties. For women, many of these difficulties are relatively well known: there is a time limit imposed by the menopause, fertility declines with age and there are increased chances of genetic disorders in the children of older mothers. But less well known is that males also have a "biological clock"; sperm quality and fertility declines with age and the probability of certain genetic disorders in children of older men is also increased. These impacts of ageing don't just apply to humans but are likely ubiquitous across the animal kingdom. There is currently lots of research, in model organisms such as flies and mice, to help us understand the basic biology and evolution of ageing, the genes and molecules that cause it, and how we might develop interventions to slow ageing and promote health in people. Along with this type of research often comes insights into female reproductive ageing. This is because reproductive ageing in females is obvious: females often produce fewer offspring as they age and this is easy to quantify. Male reproductive ageing is, however, more cryptic. Male offspring-production occurs via females, so it is experimentally more challenging to measure. Moreover, there are several reasons why males might fail reproductively. For example, it could be because they don't mate, because they don't make effective sperm or seminal fluids, or because they fail to transfer ejaculates to females if they do mate. However, using the fruit fly, Drosophila melanogaster, it is now possible to measure many aspects of the semen, and new "proteomic" techniques mean that we can quantify the overall composition of the male ejaculate. Now is the ideal time to utilise these techniques, and our extensive and increasing knowledge about the biology of ageing in this species, to test how ageingimpacts the male ejaculate and to explore the consequences of ejaculate ageing. This is what my project aims to do. In the first part, I will characterise how the ejaculate changes as males age. Do males produce fewer sperm or less seminal fluid, as they get older? Does the composition of the semen change? How much do they transfer to females? I will investigate how various important factors influence ejaculates in ageing males, such as nutrition, health and mating activity. I will also test whether interventions that increase lifespan, such as dietary restriction (a reduction in food intake without starvation), or the manipulation of genes involved in nutrient-sensing pathways, can lead to healthier ejaculates in ageing males. Combining the information gleaned from these experiments with evolutionary theory I will make predictions about how male ejaculate ageing should affect female fertility and reproductive success, and the outcome of sperm competition between males. In the second part of the project I will test evolutionary theories, to tell us how male ageing affects the adaptive reproductive decisions of males and females. For example, are females better off mating with young or old males? Does the sperm-competitive ability of males change as they age? By genetically manipulating male reproductive proteins I will be able to uncover the genes that causes such age-related changes. The goal of the project is to reveal the importance of age-related changes in the ejaculate, whether anything can be done to ameliorate negative effects of ejaculate ageing, and to help explain the age-mediated reproductive decisions that males and female make.

Impact Summary

The project proposed here will increase our understanding of the mechanisms underlying ejaculate ageing - and the consequences of ejaculate ageing - in an evolutionary context. It is a topic of wide interest to scientists and the public alike. The integrative approach of the research, combining the proteomics of ejaculate traits and the genetics of lifespan regulation with the evolutionary ecology of reproductive decisions, ensures that the results will have broad appeal and will impact research areas including gerontology, molecular biology and genetics, proteomics, neuroscience, animal behaviour and reproductive biology. Outside of specialist academics in the same field, the main beneficiaries are likely to be in the public health sector and in insect pest control. My research will contribute to our understanding of the basic processes underlying reproductive ageing in model organisms commonly used to study evolutionarily conserved ageing processes. The potential economic and health benefits of clinical interventions that prevent age-related declines in fertility are substantial. Ultimately, the research might inform the best avenues for research aimed at producing human treatments to reduce age-related male fertility problems and disorders that affect the children of older fathers. The Drosophila accessory gland is currently being developed as a model for the study of the human prostate by the Wilson lab, one of my project partners. My collaboration with Clive Wilson's lab will ensure that relevance of my work to human reproduction will be capitalized upon. The research will also be of interest to researchers who are trying to develop new or more effective ways of controlling insect pests or disease vectors. Techniques to manipulate the fertility of pest species are at the forefront of research in this field. Understanding the mechanisms and evolutionary consequences of ejaculate ageing in insects is therefore of considerable importance. Thus my research will potentially benefit pest-control technology companies and their users: people who consume insect pest-infected food or materials. As detailed in the Impact Plan I will engage with applied insect pest control researchers to exchange knowledge and realise the potential applied benefits of my findings. Furthermore I will implement several strategies to advertise my work: via the internet (webpage, social media and public understanding of science activities) and via the University of Oxford press office, to facilitate media publicity. In addition to presenting my research at a broad range of conferences, I will publish in open access journals (PLoS, and BMC) where possible to maximise access to my research output.

Committee	Research Committee A (Animal disease, health and welfare)
Research Topics	Ageing
Research Priority	X – Research Priority information not available
Research Initiative	Fellowship - David Phillips Fellowship (DF) [1995-2015]
Funding Scheme	X – not Funded via a specific Funding Scheme

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