Temporal genomics unravels demographic and selective invasion dynamics of Drosophila suzukii at a European range edge

Drosophila suzukii is a globally invasive fruit fly that causes significant economic impacts on soft-skinned fruit crops. While its invasion history has been studied on a global scale, regional-scale demographic and selective dynamics remain less understood. Portugal is at the westernmost limit of the European expansion, a key region to investigate genetic diversity and adaptation at the most recently colonized areas. Previous whole-genome sequencing of Portuguese populations suggested a Mediterranean invasion route and identified candidate variants potentially involved in local adaptation. Here, we re-sample the Portuguese populations two to four years later, to examine temporal changes in the invasion dynamics. Our results confirm the Mediterranean invasion route and show that the extremely low genetic diversity in one early-sampled population (PT-VM19) reflects a founder event. We show that this population gained genetic diversity over time, likely through gene flow from neighboring populations. We detect signatures of selection along the genome and find that most overlap with previously reported candidate genes is driven by PT-VM19, suggesting that many earlier signals were false positives associated with its low diversity. Yet, nine genes consistently exhibit signatures of selection across Portuguese populations through time, making them strong candidates for local adaptation. These genes are involved in neural development, embryogenesis, metabolism, and chromatin organization. Based on these, we developed and validated a set of SNP markers for monitoring D. suzukii . Our study underscores how temporal genomic data from recently invaded regions can uncover demographic recovery and ongoing adaptation, and contributes genomic tools for applied population monitoring.