Genetic and phenotypic consequences of local transitions between sexual and parthenogenetic reproduction in the wild

Transitions from sexual to asexual reproduction have occurred in numerous lineages across the tree of life, but many questions remain about how such transitions occur and why asexual populations rarely persist. In facultatively parthenogenetic animals, all-female populations can arise when males are absent or become extinct and, if such populations can persist asexually for many generations, they could ultimately give rise to obligately asexual species. However, the initial stages of this process remain poorly understood. The facultatively parthenogenetic Australian phasmid Megacrania batesii exhibits a spatial mosaic of mixed-sex populations that reproduce predominantly sexually and all-female sites that reproduce exclusively via parthenogenesis. We used this system to compare genetic and phenotypic parameters among multiple natural populations that vary in reproductive mode and geographic location. Analysis of single nucleotide polymorphisms (SNPs) collected from reduced representation whole genome data showed populations grouping by geographic location rather than reproductive mode, with little gene-flow between them. Mixed-sex populations had drastically higher heterozygosities than all-female populations. Phenotypic analysis revealed considerable inter-population variation in rates of deformities in (non-functional) wings, with higher mean frequency and severity of deformities in all-female sites. All-female sites also harbored more parasites, but only in swamp habitats. However, reproductive mode did not explain variation in mean female fecundity, egg hatching success, or missing appendages. These results indicate that local transitions to parthenogenetic reproduction can lead to increased rates of developmental abnormalities and increased vulnerability to disease but can also occur without substantial fitness consequences despite dramatic reductions in genetic diversity and heterozygosity.