The genomic basis of adaptation to virulent pathogens in asexual bdelloid rotifers

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Sex is embarrassing for scientists, because it is such an inefficient way to make offspring that simple theory says it should not exist at all. In theory, female animals could pass on their genes twice as effectively by making eggs that hatch into identical clones, rather than letting males contribute 50% of the DNA. An all-female 'asexual' population could grow twice as quickly. With this huge advantage, it is hard to see why nearly all plants and animals keep males around, or spend so much time and energy on sex. This is one of the Big Questions that has puzzled biologists since Darwin. One leading idea is that clonal populations are driven extinct by diseases. If individuals are genetically identical, a pathogen that evolves to infect one can kill them all. Sex continually shuffles DNA and introduces genetic diversity to the immune system. This helps each new generation to resist the ever-changing pathogens. This idea is called the 'Red Queen' hypothesis (RQH), after a character from Alice in Wonderland who had to run all the time to stay in the same place. Animal groups that completely abandon sex almost always vanish soon afterwards, but it is not clear if this is due to diseases or something else. We plan to answer this by investigating a strange group of animals that seem to break all the rules. Bdelloid rotifers are tiny aquatic invertebrates that seemingly abandoned sex over 50 million years ago, but are highly successful all over the world, with more than 500 species. They have been called 'an evolutionary scandal' because sex is supposed to be indispensable. Their success is a problem for the RQH, as they are attacked by nasty fungal pathogens that can exterminate populations in just a few weeks. Why haven't they gone extinct? If the RQH is right, bdelloids must have unusual alternative strategies to cope with diseases. We will investigate two possibilities: (1) Bdelloids might use previously unknown genetic tricks to shuffle their immune defences. Using genome sequencing technology, we will identify the genes and proteins that protect rotifers from fungal attack. We will ask whether variation in these immunity genes is driven by special processes, like odd forms of sex, or a weird mechanism that lets them pick up DNA from other organisms. Evidence for either idea would support the RQH's prediction that even bdelloid rotifers need to 'run' as fast as they can to keep up with pathogens genetically. If we find no such mechanisms, even for immune genes, it would confirm that bdelloids lack genetic shuffling. In either case, we will gain new insights about how animals resist diseases, and perhaps even find antimicrobials that might be useful against fungi. (2) Bdelloids' ecology and lifestyle might let them escape from pathogens. Bdelloids thrive in temporary patches of moss and rainwater, and have the unusual ability to survive complete desiccation. They form dust-like particles that can be carried by wind for miles, but the fungi cannot survive this process. Perhaps the rotifers disperse among moss patches so often that the pathogens cannot physically keep up, so that the bdelloids 'run away' by dispersal instead of genetic shuffling. To test this scenario we will track changes in rotifer genotypes in moss over time, and see whether incoming animals are better at resisting diseases. If bdelloids are playing ecological "hide-and-seek" with pathogens, it would again show that special mechanisms are needed to replace sex. Evidence for one or both possibilities would support the RQH by showing how bdelloids escape disease and extinction. It would solve an 'evolutionary scandal' and help explain why sex is so common. But, if we find that bdelloids are thriving without odd genetic or ecological tricks, it would imply that the threat of disease to long-term clonal lineages has been overstated, which would lead to a substantial rethink about the embarrassing problem of sex.