Sexual versus Asexual Reproduction: Distinct Outcomes in Relative Abundance of Parthenogenetic Mealybugs following Recent Colonization

Asexual reproduction, including parthenogenesis in which embryos develop within a female without fertilization, is assumed to confer advantages over sexual reproduction, which includes a “cost of males.” Sexual reproduction largely predominates in animals, however, indicating that this cost is outweighed by the genetic and/or ecological benefits of sexuality, including the acquisition of advantageous mutations occurring in different individuals and the elimination of deleterious mutations. But the evolution of sexual reproduction remains unclear, because we have limited examples that demonstrate the relative success of sexual lineages in the face of competition from asexual lineages in the same environment. Here we investigated a sympatric occurrence of sexual and asexual reproduction in the pineapple mealybug, Dysmicoccus brevipes. This pest invaded southwestern Japan, including Okinawa and Ishigaki Islands, in the 1930s in association with imported pineapple plants. Our recent censuses demonstrated that on Okinawa sexually reproducing individuals can coexist with and even dominate asexual individuals in the presence of habitat and resource competition, which is considered to be severe for this nearly immobile insect. Molecular phylogeny based on partial DNA sequences in the mitochondrial and nuclear genomes, as well as the endosymbiotic bacterial genome, revealed that the asexual lineage diverged from a common sexual ancestor in the relatively recent past. In contrast, only the asexual lineage exhibiting obligate apomictic thelytoky was discovered on Ishigaki. Co-existence of the two lineages cannot be explained by the results of laboratory experiments, which showed that the intrinsic rate of increase in the sexual lineage was not obviously superior to that of the asexual lineage. Differences in biotic and/or abiotic selective forces operating on the two islands might be the cause of this discrepancy. This biological system offers a unique opportunity to assess the relative success of sexual versus asexual lineages with an unusual morphology and life cycle.