Varroa mites escape the evolutionary trap of haplodiploidy

Abstract

AbstractGenetic diversity is essential for populations adapting to environmental changes. Due to genetic bottlenecks invasive species have reduced genetic diversity. However, they must quickly adapt to changes in new environments, potentially including anthropogenic countermeasures. This paradox raises a fundamental question: how do species adapt to changes while having low genetic diversity? The invasion paradox is more pronounced for some species. Parasites go through additional bottlenecks between hosts. Haplodiploid species have a lower effective population size as males can inherit and transmit only half of their mother’s genome. Trying to solve this paradox, we investigated inheritance in the Varroa mite (Varroa destructor), a well-studied invasive parasite of honey bees fitting all of the above criteria. By following the flow of alleles across three-generation pedigrees we found that Varroa, so far believed to be haplodiploid, is actually not. Rather, it has a unique reproductive system in which females clonally produce functionally diploid sons. While males lose somatic DNA during development, they can transmit either copy of the maternal genome to their daughters. This enhances female fitness, particularly under sib-mating typical of Varroa. We suggest this allows a greater effective population size relative to haplodiploidy and, thus, an increased evolutionary potential. This reversion to diploidy is a singular example of escaping the ‘evolutionary trap’ of haplodiploidy, which is believed to be an evolutionary stable end state. Plasticity in reproductive systems could be more common than assumed, and may potentially explain the remarkable resilience and high adaptivity of Varroa and other invasive parasites.SignificanceVarroa mites have driven the collapse of honey bee populations since their worldwide spread in the middle of the 20th century. Despite repeated genetic bottlenecks, Varroa has adapted to diverse environments and has overcome many pesticides. Using pedigree analysis, we found that Varroa re-evolved diplodiploid reproduction from an evolutionary history of haplodiploidy. Diplodiploidy permits a higher effective population size and evolutionary potential, likely facilitating Varroa’s ongoing success. Females produce males clonally, passing on their entire genomes. Varroa is a singular exception to the theoretically and empirically observed rule that, one evolved, haplodiploidy is an evolutionarily stable end state (an ‘evolutionary trap’). Novel mechanistic studies of even well-known organisms can lead to surprising insights into the evolutionary plasticity of reproductive systems.