Evolution in eternal triangles: a dynamic landscape for driving rapid changes in reproduction

The interplay between males and females over reproduction can ultimately lead to the evolution of spectacular diversity in reproductive behaviour, morphology and physiology. This can range from the stunning peacock's tail to elaborate and bizzare penis morphology. The interactions are particularly strong when females mate with multiple males (polyandry) and when there is internal fertilization and sperm storage for long periods within females. This is because there are then frequent, intense and continuing competitions between males for matings and for fertilizations even after matings have occurred.

In the last few decades it has been realized that interactions between females and males can often be antagonistic rather than co-operative. This 'sexual conflict' occurs because each sex can increase their reproductive success in a way that can result in the expression of costs in the other sex. It is often the case, for example, that males but not females increase their reproductive success through increasing their mating frequency.

When this happens, changes in one sex lead to counter changes in the other, as in an arms race. This continual back and forth between males and females, otherwise known as 'antagonistic coevolution', is a widespread and potent force for driving evolutionary change. Because its effects are focussed on changes to reproductive genes it can lead to reproductive incompatibilities. This can then lead to the creation of new species.

Therefore, sexual conflict is important because it represents a potent and eternal fuel for generating biodiversity through increasing variation in genes and ultimately the number of species.

Sexual conflict should be particularly strong when relatively minor differences in phenomena such as how often to mate result in large effects on the reproductive success of males in comparison to females. This will be particularly intense in the typical situation in which more than one male is involved in a reproductive bout with a single female (the 'eternal triangle' where one females mates with two or more males in series). Hence there can often be three- (or more) way 'disagreements' about reproductive decisions such as how often to mate, since the interests of the two males are served by very different outcomes. For example, the first male to mate would benefit if females never mated again.

Although we currently have predictions, we lack actual measurements of the extent of these evolutionary disagreements and we also lack any understanding of the underlying mechanisms. This is therefore an important gap to fill.

Our first aim is therefore to work with the fruitfly and measure for the first time the magnitude of disagreements in (i) normal flies and (ii) in those in which the 'sex peptide (SP)' pathway - which we know mediates sexual conflict - has been manipulated in both sexes. We will use natural and engineered versions of SP pathway genes, to fully pin down their causal effects.

Our supporting background work shows that in principle this is a valid and promising way to proceed. Our work provides proof of principle (a) that there are differences in reproductive success for normal males and females within eternal triangles, and (b) that inactivation of sex peptide receptor (SPR) in females significantly alters the patterns seen, party through changes in how the sperm of different males are stored and used for fertilisation. The latter could increase the chance of reproductive failure for males. Our second aim is therefore to test how sexual conflict within the eternal triangle could lead to reproductive isolation via a break down in competitions between sperm.

Overall, the research work will show the extent, basis and significance of evolutionary disagreements over reproductive decisions in males and females that can drive evolutionary change, and their potential contribution to reproductive isolation and the generation of biodiversity.

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:

(i) The battle of the sexes. The interplay between males and females is powerful in evolutionary terms. Such interactions can be mutualistic, with both males and females benefitting, or selfish, with one sex benefitting at the expense of the other. There is intuitive and public appeal in the study of adaptations that are good for males and bad for females, and vice versa.
(ii) Husbandry practices for insect control: There is an applied context of this research in terms of increasing the reproductive performance of insect pests that are mass reared for control.
(iii) Communication between signals and receivers: The way in which signals are generated and received or misunderstood is a topic of broad importance and also of public interest.
(iv) Sperm competition dynamics: The proposed work aims to examine the dynamics of the sperm in storage inside females using 'glow in the dark' sperm. These provide visually arresting images that we have already used on public visit days.

The main beneficiaries with whom we aim to maximise the impacts of the research above are:

1. Academia: we aim to maximise impact of the research described above 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 aim to investigate the potential for conflicts of interest to impact upon husbandry and rearing regimes of insects used for pest control. For instance, sexual conflicts that can disrupt the normal fertility patterns for males are of obvious concern if the aim is to breed maximally fertile pest insects for release in sterile insect programmes. We are already developing in the private sector the application of knowledge to fruitfly pests in a NERC-funded CASE studentship together with Oxford insect technologies (Oxitec). We plan to further increase impact by attending the next Fruit flies of Economic Importance conference in 2014 (in Bangkok, Thailand) and offer a talk (TC) and 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 also aim to develop these materials following 'road testing', for the SET for success exhibition at the Royal Society in the summer of 2013. 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 'the eternal love (or not) triangle' and to utilize the visual impact of the 'glow in the dark' fluorescent sperm.

2. HOW WILL THEY BENEFIT FROM THIS RESEARCH

The beneficiaries named above will benefit through:

(i). Increased economic competitiveness of UK plc through increased visibility of research outputs and increased engagement with the private sector.
(ii). The impacts are likely to be primarily of academic and public interest. Here the beneficiaries will gain through enhanced effectiveness in the transmission of research findings.
(iii). Increased learning and awareness (through school visits) of the opportunities, relevance and range career choices available through academia.
(iv). An increased range of career options (DS) through training in media, communication, business and private sector practices, which could be employed in a range of employment sectors.