Reproductive isolation and structural variation among sympatric lineages of an international mosquito pest

Background: Reproductive isolation describes the degree to which genetic differences among populations reduce the level of neutral gene flow between them. Genomic approaches are currently showing great utility for identifying reproductive isolation between sympatric, morphologically indistinct populations, where hybridisation and introgression may yet be common. Here we use population genomic approaches and a chromosome-level reference assembly to uncover three highly differentiated, cryptic lineages of Aedes notoscriptus, an Australian mosquito disease vector that has invaded New Zealand (c. 1920) and California (c. 2014). Results: We identified a single lineage (Noto1) that was the source of the New Zealand and Californian invasions, and this lineage was also distributed across much of Australia including the Greater Melbourne region where it was sympatric with a second lineage (Noto2). Although Victorian Noto1 and Noto2 were frequently sampled co-locally, hybrids were observed less frequently than expected under random mating, and admixture levels were low, suggestive of selection against hybrids. A bottleneck observed in Victorian Noto1 suggests that Noto1 may have recently expanded its range into the Greater Melbourne region. We also identified a massive structural variant (~25 Mbp; ~10% of chromosome size) in Noto2 that was segregating at intermediate frequencies across the Greater Melbourne region but was fixed in Noto1. Conclusion: Together, these results identify key genetic differences between cryptic lineages of this international disease vector that warrant further investigation given potential differences in vector competence.