Geoclimatic oscillations and ancient reciprocal adaptive introgression shape the evolutionary trajectories of threatened Coilia

Abstract Geoclimatic oscillations have repeatedly reshaped biodiversity, yet how ancient lineages persist and diversify through profound environmental upheavals remains a central question in evolutionary genomics. By integrating chromosome-level genome assemblies, population genomics, and transcriptomic data across the Coilia species complex, we reconstruct deep evolutionary histories of Coilia along the dynamic East Asian margins. Our analyses reveal divergences dating to the Miocene, coinciding with major tectonic and climatic transitions, including Tibetan Plateau uplift-linked reorganization of the Yangtze drainage toward the East China Sea, and the Middle Miocene Climatic Optimum. Despite long-term separation, we uncover evidence for ancient, reciprocal introgression among Coilia lineages, with gene flow confined to discrete genomic regions rather than distributed genome-wide. These introgressed regions are enriched for loci associated with immune function, vascular development, and osmoregulatory processes, and exhibit population genetic signatures consistent with positive selection. Temporal modelling indicates that this window of adaptive exchange preceded Pleistocene glacial intensification, after which gene flow became effectively restricted. Together, our results suggest that transiently permeable species boundaries historically acted as reservoirs of adaptive variation, shaping evolutionary trajectories and facilitating niche differentiation under repeated geoclimatic oscillations. This study highlights ancient adaptive introgression as an important evolutionary process contributing to the long-term persistence of threatened coastal fishes. Competing Interest Statement The authors have declared no competing interest. Data availability The raw whole-genome re-sequencing data and transcriptomic expression data generated in this study have been deposited in the CNGB Sequence Archive (CNSA) of China National GeneBank DataBase (CNGBdb) under project accession number CNP0009055. The C. mystus reference genome assembly generated in this study has been deposited at GenBank under accession number GCA_050626335.1. Genome annotations (GFF3), coding sequences (CDS), and protein sequences are available on Figshare at https://doi.org/10.6084/m9.figshare.31342996. The raw sequencing data used for genome assembly (including PacBio HiFi, Hi-C, and RNA-seq reads) are available in the NCBI Sequence Read Archive (SRA) under BioProject accession number PRJNA1161598.