ALL'S FAIR WHEN LOVE IS WAR: THE EVOLUTION OF LIFESPAN AND AGEING UNDER SEXUAL CONFLICT.

Lead Research Organisation: University of East Anglia
Department Name: Biological Sciences

Abstract

In 1992 John Gray wrote a now famous book 'Men are from Mars, Women are from Venus' (Harper Collins). In this he illustrated the many differences between males and females using the book title as the central metaphor. He imagined that the sexes are so different that one might as well consider them as originating from different planets.

One of the main ideas in the book is that men and women assess or 'score' the currency of their relationship - but that they score according to different scales! This is evident, Gray suggests, when the amount of give and take within a relationship is not assessed or scored equitably. This can lead to a perceived or actual imbalance in the relationship, leading to resentment and so on. Overall, the ideas in this book proved to be a popular way of thinking about how relationships work - or not - in terms of sex differences.

Whatever one thinks about the book and its legacy, the central ideas described above accord surprisingly well with evidence drawn from plants and animals. It was realised in the 1970s, for example, that rather than being co-operative ventures, the interactions between the sexes over reproduction are often characterized by conflict rather than co-operation. Hence the sexes often 'disagree' about how much energy and resources to invest in reproduction and how often to make that investment.

A good example is evolutionary disagreements over how often to mate. Males often gain from mating frequently and females often do not. Furthermore, females often suffer significantly reduced lifespan from mating too frequently (an effect that we now know is also true in humans). Such lifespan reduction arising from mating frequently is not incurred to anything like the same degree in males.

It has recently been realised that these sexual interactions, i.e. the effect of males on female lifespan and vice versa, could actually underlie an important and long-standing puzzle: why it is that males and females often have very different longevity. For example, human females generally live at least 4 years longer than men. Such sex differences are also extremely common in the animal world, and can occur in either direction.

In experimental settings the way that lifespan is measured, and longevity 'genes' identified, is often to use non-reproductive individuals, or those that are mated early in life and then kept away from the other sex. Such tests are therefore missing something important - the effects of regular exposure to the other sex.

It is now believed that the 'sexual conflicts' of the sort described by Gray and earlier considered by evolutionary biologists such as Geoff Parker, Richard Dawkins and Bill Rice can go a long way to explaining sex differences in lifespan and ageing by considering the effects of one sex upon the other.

The central aim of the research proposed here is to evaluate this idea and to examine the underlying genetic basis of the differences in these necessary, but sometimes dangerous, liaisons between the sexes.

The work is important because it will be the first full test of these ideas and the first to probe the genomic basis of sex differences caused by sexual conflict. Our proof of principle data gathered for this proposal show that the methods proposed can identify novel ageing genes. The work is also useful because these ideas can also be fed directly into husbandry practices for pest control in the applied sector.

Overall this is an exciting and novel project that will test whether sexual conflict can lead to increased ageing and will identify the underlying genes that are responsible.

Planned Impact

The School of Biological Sciences at UEA is committed to raising the economic and societal impact of its research (for further details, see Pathways to Impact).

1. WHO WILL BENEFIT FROM THIS RESEARCH

We anticipate 4 main areas for potential impact:
1. Lifespan and ageing. Human females generally outlive males, and such sex differences (though not necessarily in this direction) are known all across the animal kingdom. Experimental studies of ageing however, often measure lifespan and ageing in largely non-reproductive individuals separated from the other sex. Much of our understanding of ageing genes detected by such studies therefore overlooks a vitally missing ingredient. Interactions between males and females will have a huge impact on lifespan. Males can cause a reduction in female lifespan through the actions of the seminal fluid proteins they pass during mating. Therefore to address a huge gap in our understanding we need to test the effect of each sex upon the rate of ageing of the other. This will shed light on universally observed, but little understood, sex differences in ageing and lifespan.
2. The battle of the sexes. The interplay between males and females is a powerful evolutionary force. Such interactions can be co-operative or conflicting. There is intuitive appeal in the study of adaptations that are good for males and bad for females, and vice versa and this is a topic that catches the public interest.
3. Husbandry practices for insect control: There is an applied context of this research in terms of the husbandry of insect pests that are mass reared for control. This is being explored through the applied partnerships described above, and also in a new NERC quota studentship (supervisor TC).
4. Communication between signals and receivers: The way in which signals are generated and received is a topic of broad importance and also of public interest.

The main beneficiaries are:
1. Academia: we aim to maximise impact of the research through open access papers, reviews, commentaries, lab research web sites etc. For this project, we plan a research blog to which the research team and particularly the PDRA would contribute.
2. Private sector: we are investigating the potential for conflicts of interest to impact upon husbandry and rearing regimes of insects used for pest control. We have already developed in the private sector the application of knowledge to fruitfly pests in two NERC-funded CASE studentships together with Oxford insect technologies (Oxitec). We plan to further increase impact by contributing to the next Fruit flies of Economic Importance conference in 2014 (in Bangkok, Thailand) and offer a poster (DS) outlining fundamental principles of relevance to control, drawn from the non-pest fruitfly model systems.
3. General public, schools: We have recently devised new exhibition materials for open days and visit days at UEA. We are also developing teaching resources for use in the Teacher Scientist Network (TSN) scheme. Together with our engagement Director in the School, we are tailoring these resources to the National Science Curriculum, for taking into schools via the TSN. We plan to base these around the concepts of sex differences and lifespan.

2. HOW WILL THEY BENEFIT FROM THIS RESEARCH
The beneficiaries named above will benefit through:

1. Increased economic competitiveness of UK plc through increased visibility of research outputs and increased engagement with the private sector.
2. Enhanced effectiveness in the transmission of research findings through the academic community.
3. Increased learning and awareness (through school visits) of the opportunities, relevance and range career choices available through academia.
4. An increased range of career options through training in media, communication, business and private sector practices, which could be employed in a range of employment sectors.

Publications

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Brockhurst MA (2014) Running with the Red Queen: the role of biotic conflicts in evolution. in Proceedings. Biological sciences

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Chapman T (2015) The Evolution of Sexuality

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Duxbury EML (2020) Sex-Specific Responses of Life Span and Fitness to Variation in Developmental Versus Adult Diets in Drosophila melanogaster. in The journals of gerontology. Series A, Biological sciences and medical sciences

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Fricke C (2017) Variation in the post-mating fitness landscape in fruit flies. in Journal of evolutionary biology

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Maklakov AA (2019) Evolution of ageing as a tangle of trade-offs: energy versus function. in Proceedings. Biological sciences

 
Description We have explored the extent to which differences in lifespan between males and females are due to sexual conflict. This research shows that the differences between the lifespan of males and females can evolve and can be modified by the degree of competition between the sexes. Female lifespan is much more affected by exposure to males than vice versa. The research offers new insight into the elusive explanations for why, across many different species, the sexes show characteristic differences in the length of life. The analysis of gene expression differences is also providing insight into the underlying mechanisms of these differences.

Key outcomes arising from this work are the following:

Rostant WR, Fowler EK & Chapman T. (2020) Sexual conflict theory: concepts and empirical tests. The SAGE Handbook of Evolutionary Psychology, edited by Todd Shackelford, in press.

Rostant, WR, Mason, JS, West, N, Smedley, R & Chapman, T. Sex differences in reproductive costs alter lifespan, morality and ageing rate. For submission to Aging Cell.

Rostant WR, Mohorianu I, Fricke C, Mason, JS, Fowler E & Chapman T. Genomic basis of ecological adaptation to divergent nutritional environments. For submission to Evolution Letters.

Further application for funding to BBSRCX is also planned.
Exploitation Route Further experimentation, testing for generality of mechanisms in the wider study of ageing across different animals.
Sectors Agriculture, Food and Drink,Environment,Healthcare

 
Description BBSRC DTP studentship to T Chapman and W Haerty on sexual detection - social responses in fruitflies
Amount £100,000 (GBP)
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 10/2019 
End 09/2023
 
Description NERC standard research grant
Amount £537,000 (GBP)
Funding ID NE/R010056/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 04/2018 
End 03/2021
 
Description Poor starts and silver spoons: how diet shapes sex-specific fitness from birth to death
Amount £436,257 (GBP)
Funding ID NE/R010056/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 04/2018 
End 03/2021
 
Description Social evolution and the evolution of ageing: testing the hypotheses
Amount £603,481 (GBP)
Funding ID NE/R000875/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 10/2017 
End 10/2020
 
Description The cost of longevity: transgenerational consequences of parental lifespan extension for offspring fitness
Amount £468,069 (GBP)
Funding ID BB/R017387/1 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 07/2018 
End 06/2021