Sexual selection, condition dependence and meiotic drive

In many species, females show strong sexual preferences to mate with particular males - those with elaborate and exaggerated sexual ornaments. These traits are thought to be honest signals of male genetic quality. But what is the nature of the "good genes" benefits that females derive from mate preference?

We will address this fundamental question using the stalk-eyed fly, an iconic example of extreme sexually-selected morphological evolution. Male flies have greatly exaggerated eyespan and females prefer to mate with males with the most extreme eyespan. Of great interest, stalk-eyed flies harbour a selfish genetic element on the X chromosome that causes sex-ratio distortion through meiotic drive. In normal male meiosis, the X and Y chromosomes segregate equally into sperm. But the meiotic drive element produces a toxin that attacks the Y chromosome, causing Y-bearing sperm to die. So all sperm contain the drive X chromosome, and only female offspring are produced.

Meiotic drive persists in populations of stalk-eyed flies because of the two-fold advantage the element gains in meiosis (it is passed on to all offspring, whereas other genes are only passed to half the offspring). But its spread is limited because it has overt deleterious effects on the fitness of the organism. Most obviously, it is bad because it kills half of a male's sperm. But it is also bad because the genes causing meiotic drive exist in an "inversion" - a part of the X chromosome that has been flipped around and is orientated in the opposite direction. Inversions cannot undergo normal processes like genetic recombination, and tend to accumulate deleterious mutations.

We hypothesise that females gain benefits from avoiding mating with meiotic drive males, as they have low genetic quality. We will test the prediction that females discriminate against drive males. Preliminary work supports this, as drive males have small eyespan. We will investigate this further by exposing males to a range of environmental stresses that are typical of those experienced in the wild, to test whether the sexual ornament is an "honest" signal of genetic quality, in turn explaining why females use it to select a mate. We will characterise in depth how meiotic drive disrupts fertility (by measuring reproductive organ size, sperm allocation and sperm competition) and survival components of fitness, again under variable environmental stress. An interesting prediction is that the rest of the genome has evolved counter-adaptations to drive that will ameliorate loss of performance. We will investigate evidence for this at both the organismal and genomic levels. Evolutionary responses will be tracked at the sequence level by creating high-quality reference genomes of drive and non-drive chromosomes and investigating genomic signatures of changes that are deleterious or beneficial to fitness. Intensive laboratory experiments will be backed up by extensive field investigations of female mating behaviour and male trait distribution of drive-carrying flies in the wild, and how the frequency of drive varies with environmental stress under field conditions. All these strands contribute to our overarching goal: to show how sexual selection, on males and females, interacts with a chromosomal region with clear deleterious effects on organismal fitness.

Our findings will be of immediate interest to the private sector and policy makers. In recent years there has been considerable interest in commercialising technology via spin-out companies (Oxitec, for example) to control invasive species and disease insect vectors. One method of control is the development of applied gene-drive technologies which exploit CRISPR gene editing and are a synthetic equivalent of naturally occurring meiotic drive systems. Trials using such constructs are already being used for insect vectors of human disease but it remains unclear how they will fare after release into the environment. Valuable insights can be obtained from the evolutionary behaviour of existing natural meiotic drive systems. In addition, there has been considerable interest from policy makers about the release of synthetic constructs into the wild, especially concerning contamination of natural species, and unforeseen deleterious consequences. There is considerable scope for an effective exchange of ideas and insights between researchers in fundamental research and the applied science community. It is important that commercial approaches take account of any evidence that genomes can respond to the presence of drive by evolving counter-adaptations to reduce impaired host performance. Such responses may act as a brake on the efficacy of synthetic gene-drive technology.

We will use a range of dissemination methods: publishing in front-line open-access journals, research conference presentations, and invited talks to other research groups. These provide the bedrock outputs of our research. They will be all open access and hence readily available. We will place our results in a broader perspective and enhance its impact by organising a one-day workshop: "What do natural drive systems tell us about the prospects of synthetic gene-drive technology?" in mid-year 3 of the project. This event will bring leading academic researchers of naturally occurring drive in a range of species together with leaders in the rapidly growing field of synthetic gene-drive technology, to provide a state-of-the-art review and evaluate future research prospects. We will also invite policy makers interested in the ethical issues surrounding synthetic gene-drive technology. In the longer term, there are exciting opportunities for extensive collaborations and knowledge transfer with the private sector and policy makers via secondments and CASE project development. Progress of the project will be regularly publicised via blogs on our websites.

Our findings will also be of broad interest to a wider community of undergraduates, school pupils and the general public. These communities are fascinated by environmental science in general and have a natural curiosity about sexual selection and the interactions between the sexes. Stalk-eyed flies are especially charismatic exemplars of sexual selection. They appear in many textbooks in evolutionary and ecological science, so the research has broad generality. These communities will benefit from seeing how cutting-edge techniques are used to further advance the UK science base. We will offer summer placements (one per year) to engage undergraduate students midway through their studies. We will contribute to both Institutions Researcher Evenings (aimed at adults) and Discovery Evenings (aimed at children), and to education outreach programmes, fostering contact with local schools and provide several places annually for school pupils to have laboratory placements. Our outreach will involve talks at schools and also the provision of a resource pack aimed at 14-18 year olds and their teachers. The pack will explain our project's use of phenotypic and genetic approaches to understand evolution. Our aim is to foster interest among schoolchildren in science careers.