The Red Queen and the bdelloid rotifers: how to keep up with co-evolving parasites in the long-term absence of sexual reproduction

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Sex is embarrassing for evolutionary biologists, who have struggled for decades to explain why almost all animals and plants engage in such an inefficient activity. In principle, females could transmit their genes with 100% efficiency by producing identical clonal daughters. Sex, by contrast, reduces a female's genetic stake in each offspring to 50%, with the remainder supplied by a male who shares few of the production costs. Given this twofold disadvantage to sexual females, why aren't all organisms asexual?One leading idea is that a lack of genetic variation leaves asexual populations vulnerable to diseases. In this view, colourfully named the 'Red Queen hypothesis', parasites and pathogens are constantly evolving to overcome the immune defenses of their hosts. Sexual hosts can fight back with new combinations of defensive genes each generation, allowing them to keep up with parasites in an endless co-evolutionary race. However, asexual hosts have no way to change their outdated defences, and are doomed to be overtaken and exterminated. Consistent with this view, lineages that completely abandon sex almost inevitably go extinct soon after, and evidence suggests that disease plays a role. However, there is one remarkable and informative exception.Bdelloid rotifers are microscopic freshwater invertebrates that abandoned sex and males more than 30 million years ago, but have persisted and diversified into more than 450 species. Their success has been called 'an evolutionary scandal,' because sex was believed to be indispensable. They appear to refute the Red Queen hypothesis, as they suffer from a range of deadly fungal parasites, but have not been driven extinct as predicted. Should we abandon this otherwise promising hypothesis? What if bdelloid rotifers have found unusual alternative ways of dealing with parasites? If so, their asexuality may actually strengthen, rather than challenge the Red Queen hypothesis.I am investigating whether unique aspects of the bdelloids' lifestyle help them stay ahead of parasites without needing sex. These animals can tolerate complete desiccation, allowing them to thrive in tiny, ephemeral patches of moss and rainwater. When dry, they form miniscule particles that can be transported by wind for hundreds of metres. Crucially, however, their parasitic fungi cannot withstand this process. In principle, therefore, a bdelloid clone could leave its co-adapted parasites behind, and disperse to a new habitat patch where the local parasites are less well-adapted. If these migrations happen often enough, parasites in any patch will be exposed to a constantly changing array of host genotypes, just as if the bdelloids were having sex.I aim to test this intriguing scenario directly. I will use genetic 'barcodes' to identify and track bdelloid clones as they migrate among patches of moss in UK woodland. I will test whether bdelloids from the same area differ in their resistance to fungal parasites, and determine whether the rotifers or their enemies are 'ahead' in the race. I will set up sterile, elevated patches of moss in the field, to see how quickly they are colonised by windblown bdelloid clones. Some of these new patches will be seeded with parasites, to determine whether their presence favours rotifers with specific genetic immunities. Results will be compared with theoretical work that describes the patterns to expect if bdelloids are indeed playing an ecological game of "hide-and-seek" with their parasites.If confirmed, this would be a fascinating and unprecedented solution to a universal problem, throwing new light on the role of dispersal in co-evolutionary dynamics. It would also reconcile the 'scandalous' bdelloid rotifers with the Red Queen hypothesis. Alternatively, if this promising scenario is refuted, the bdelloids' success would become even more mysterious and intriguing, forcing a serious reconsideration of the supposed vulnerability of asexuals to parasitism.