Twin introductions by independent invader mussel lineages are both associated with recent admixture with a native congener in Australia.

Introduced species can impose profound impacts on the evolution of receiving communities with which they interact. If native and introduced taxa remain reproductively semi-isolated, human-mediated secondary contact may promote genetic exchange across newly created hybrid zones, potentially impacting native genetic diversity and invasive species spread. Here, we investigate the contributions of recent divergence histories and ongoing (post-introduction) gene flow between the invasive marine mussel, and a morphologically indistinguishable and taxonomically contentious native Australian taxon, . Using transcriptome-wide markers, we demonstrate that two contemporary introductions into south-eastern Australia originate from genetically divergent lineages from its native range in the Mediterranean Sea and Atlantic Europe, where both introductions have led to repeated instances of admixture between introduced and endemic populations. Through increased genome-wide resolution of species relationships, combined with demographic modelling, we validate that mussels sampled in Tasmania are representative of the endemic Australian taxon ( ), but share strong genetic affinities to . Demographic inferences indicate late-Pleistocene divergence times and historical gene flow between the Tasmanian endemic lineage and northern , suggesting that native and introduced taxa have experienced a period of historical isolation of at least 100,000 years. Our results demonstrate that many genomic loci and sufficient sampling of closely related lineages in both sympatric (e.g. Australian populations) and allopatric (e.g. northern hemisphere  taxa) ranges are necessary to accurately (a) interpret patterns of intraspecific differentiation and to (b) distinguish contemporary invasive introgression from signatures left by recent divergence histories in high dispersal marine species. More broadly, our study fills a significant gap in systematic knowledge of native Australian biodiversity and sheds light on the intrinsic challenges for invasive species research when native and introduced species boundaries are not well defined.