Genomic Signatures of Adaptive Evolution in Taenioides sp. During Northward Invasion

The success and impact of biological invasions depend on adaptations to novel abiotic and biotic selective pressures. However, the genetic mechanisms underlying adaptations in invasive species are inadequately understood. Taenioides sp. is an invasive worm goby, originally endemic to brackish waters in the estuaries of Southeastern China, and now colonizes multiple inland freshwaters of North China within decades as a byproduct of the East Route of South-to-North Water Transfer (ESNT) project. However, the molecular mechanisms underlying their adaptations to the climate of North China, especially the temperature regime, are unknown. Here, we performed genomic resequencing analysis to assess genetic diversity and population genetic structure, and further investigated the genomic signatures of local adaptation in the invasive population of Taenioides sp. during their northward invasion. We revealed that all invasive populations exhibited no genetic differentiation but low gene flow and an obvious signal of population bottleneck. Yangtze River estuary may serve as the source population, while Gaoyou Lake serves as a potential bridgehead of the invasion. Selective sweep analyses revealed 117 genomic regions, containing 673 candidate genes, under positive selection in populations at the invasive front. Redundancy analysis suggested that local temperature variables, particularly the monthly minimum temperature, represent critical evolutionary forces in driving adaptive divergence. Functional enrichment analyses revealed that multiple biological processes, including metabolism and energy production, substance transmembrane transport, and neural development and synaptic transmission, may play important roles in adaptation to regional temperature conditions. Our findings revealed a scenario of adaptive evolution in teleost species that underpins their regional climate adaptation and successful establishment of invasive populations in a human-facilitated invasion context. Proper management strategies should be established to manage Taenioides sp invasion as soon as possible.