The genetic basis of reproductive isolation through intragenomic conflict

Species are perhaps the most vital biological unit, with members of the same species sharing gene flow and common traits. Understanding how species are formed is critical for a broad understanding of biology, particularly of how biodiversity is created. The textbook explanation for how one species splits into two is "ecological speciation": populations diverge because of differences in local ecology. The classic example is Darwin's finches, where on one island birds mostly eat small seeds, and evolve delicate bills to easily gather them, while on another island large nuts are available, and the population evolves large beaks to crack them open. Eventually the differences between the populations are so great that they cannot interbreed. There are many good examples of this kind of ecological speciation, such as stickleback fish and Darwin's finches.

However, there is a major alternative theory about how speciation might occur. This theory is called conflictual speciation, and holds that populations that are isolated will diverge in their selfish genetic elements. While most genes typically cooperate within an individual to increase the number of offspring produced, selfish elements instead manipulate reproduction to increase their own success, cheating the other genes in their genome. The conflict these genes cause is thought to rapidly create differences between populations in key reproductive genes. This makes hybrids between populations less able to survive and breed -and is particularly damaging to sperm production in males. Conflictual speciation theory suggests that new species form due to these internal conflicts within the genome, rather than external ecological factors. If strong evidence is found to support conflictual speciation, we will have to fundamentally rethink many of our ideas about how and why speciation occurs.

Conflictual speciation has been supported by a wealth of circumstantial evidence, but crucial evidence of the process in action between closely related populations is lacking. In this project, we will study a pair of populations where this process is thought to be ongoing. We have found that North African Drosophila subobscura flies can interbreed happily with European populations. However, some D. subobscura in North Africa carry a selfish X chromosome called "SRs", which in males kills all his Y-chromosome sperm, so all his offspring inherit the SRs chromosome and are daughters. As this selfish X is passed on to almost all offspring, while normal X chromosomes are only passed to half a male's offspring, the selfish X should spread rapidly through populations. However, the SRs X cannot spread into Europe because hybrid males that carry SRs are sterile, probably because their sperm killing mechanism malfunctions and kills all their sperm. This unique example of a selfish chromosome creating incompatibilities between populations that are otherwise completely compatible, provides us with an opportunity to study the early stages of conflictual speciation.

In North Africa, some males that carry SRs do produce some sons. We think this is because the rest of the genome has evolved to suppress the killing of Y sperm by SRs, allowing some sons to be produced. We will test the theory of conflictual speciation by first determining the genes that cause the infertility in the SRs hybrids by sequencing hybrids with high and low fertility. We will then test the theory of conflictual speciation by determining whether these genes are the same ones that provide resistance to drive. We will also examine whether these genes have been evolving more rapidly in North Africa than Spain, which would suggest that the difference is caused by SRs being present in Africa, rather than both populations simply diverging genetically over time.

Our Impact Plan has two main strands:

1) Making progress on the potential use of selfish genetic elements for pest control

Our main impact focus will be on organising a stakeholder meeting for people involved in the potential use of selfish genetic elements to target pest species. This is very timely. There are many teams of researchers, some based in the UK, currently developing techniques to modify or exterminate key pest species, using self-replicating selfish genomic agents. The UK is in an excellent position to lead the world in constructing these agents. Perhaps more importantly, the UK is arguably in an even stronger position to lead in developing a regulatory framework for their development and deployment.

We will contribute to this by organising a one-day meeting between academics, business, and government, with the aim of producing a roadmap for progress.


2) Public understanding of science

Beyond this primary impact, we will use this project as an opportunity to educate and inform the public. We will use podcasts, our regular talks at Café Scientific, schools and colleges around the UK, and press releases. We will also engage with social media, including running a Reddit "Ask Me Anything". At a local level, we will produce an exhibit focused on the processes of speciation that will be displayed at the World Museum at Liverpool, and at the Royal Entomology Society's National Insect Week at Ness Garden on the Wirral.