Poor starts and silver spoons: how diet shapes sex-specific fitness from birth to death

'..methinks I would not grow so fast, Because sweet flowers are slow ...'
(Shakespeare, Richard III, Act II Scene 4)

There is huge variation in the way that organisms live their lives. For example, mayflies famously live and reproduce as adults for only 1 day, while turtles live and reproduce for many decades. However, what is becoming increasingly clear is that males and females from the same species can also exhibit striking variation in these life histories, and may differ in lifespan, growth rate and duration of reproduction.

It is thought that the expression of contrasting life histories by males and females allows each sex to increase their reproductive success. The ultimate reasons for this stem from fundamental differences between the sexes in reproductive investment, with females typically investing more in fewer, larger eggs and males less in their more numerous sperm. The consequences that flow from this basic difference are profound and dictate the contrasting ways in which each sex achieves reproductive success over their whole lifetimes.

For example, males are predicted to compete strongly with each other for access to matings and fertilisations. This can lead to a high risk / high pay off 'live fast die young' strategy that is energetically demanding and hence requires a high carbohydrate (C) diet. On the other hand, females are expected to benefit from adopting a 'live slow die old' strategy contingent on the acquisition of high protein (P) to support high fecundity and promote survival.

Experiments are consistent with this idea but we have surprisingly little insight into the effects on reproductive success of sex-specific responses to diets across the whole lifespan. Nor do we understand how each sex responds differently to diet. Our aim in this research programme is to address these major gaps.

A major problem in achieving the next steps has been a lack of model systems and manipulations for the direct experimental tests that are urgently needed. Fortunately, the fruit fly model system, in combination with recent advances in 'Nutritional Geometry' (diets formulated with precise ratios of C:P) offer powerful tools to address this gap. For example, we can vary diets across the life course in a defined manner, generate large cohorts for high-resolution tests of survival and reproductive success and use genetic and molecular genetic reagents to test effects of manipulating nutrient sensing pathways. In addition, we have evolved populations of flies on different P and C ratios over many generations, which offers a unique opportunity to examine whether these diets favour the success of females versus males, respectively.

Our overarching aim is to identify how and why sex differences in responses to diets occur, as follows:

1. We will test the direct effect on the reproductive success of males and females of varying diets during development and adulthood. We will manipulate diets with varying C:P ratios and test the effect on lifespan and reproductive success for each sex separately.
2. We will investigate the mechanisms associated with the sex-specific responses. In this we will use molecular and genetic tools to measure the impact of altered nutrient sensing pathways on male and female reproductive success.
3. We will measure the reproductive success of males and females from lines with an evolutionary history of exposure to high and low C and P. This will test the idea that the balance of male to female success has evolved. Tests of the expression of nutrient sensing genes will also reveal evolved changes in these underlying pathways.

The work will provide the first direct tests of the consequences and mechanisms underpinning sex differences in responses to diet across the whole life course. The work is expected to result in a major advance in our fundamental understanding of why and how males and females exhibit different life histories.

1. WHO WILL BENEFIT FROM THIS RESEARCH

We anticipate 4 main areas for potential impact:

1. Life history, lifespan and ageing. Sex differences in responses to diet are becoming apparent across the animal kingdom. But - we do not understand the consequences or causes. We have developed lines in which the sexes are predicted to have evolved different responses to dietary components, which allows us now to test key ideas about why this has occurred and how. This will shed light on universally observed, but so far little understood, sex differences in dietary responses.
2. Lifespan, life history and diet. The proposed work will also show how diet can influence lifespan and healthy ageing differently for the sexes. This is a topic of major current research and public interest.
3. The battle of the sexes. The interactions 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 show sex specificity, and this is a topic that catches the public interest.
4. 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 applied partnerships.

The main beneficiaries / recipients 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 sex specific diet responses 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 fruit fly pests in CASE studentships together with Oxford insect technologies (Oxitec) and IAH (Pirbright).
3. General public, schools: We 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 in how animals live their lives.

2. HOW THE MAIN RECIPIENTS NAMED ABOVE WILL BENEFIT:

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.