Strong reproductive isolation among sympatric lineages of an international mosquito pest

Reproductive isolation describes the degree to which genetic differences among populations reduce the level of neutral gene flow between them. This has been extensively studied across major mosquito genera including Aedes, Anopheles, and Culex, which often exist as complexes of multiple species or ecotypes in which hybridisation and introgression are common. Here we use population genomic approaches coupled with extensive geographical sampling 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). We found a single lineage (VIC1) was the source of all international invasions, and this lineage was also distributed across much of Australia including the Greater Melbourne region where it was sympatric with a second lineage (VIC2). Although VIC1 and VIC2 were frequently sampled co-locally, hybrids were observed less frequently than expected under random mating, and admixture levels were low and suggestive of selection against hybrids. A strong bottleneck observed between VIC1 and its associated northern lineages suggests that VIC1 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 VIC2 that was segregating at intermediate frequencies across the Greater Melbourne region but was fixed in VIC1. Together these results show key genetic differences between cryptic lineages of this international disease vector that point to potential differences in behaviour and vector competence that warrant further investigation.