Range-wide population genomics of common seadragons shows secondary contact over a former barrier and insights on illegal capture

BACKGROUND: Common seadragons (Phyllopteryx taeniolatus, Syngnathidae) are an emblem of the diverse endemic fauna of Australia’s southern rocky reefs, the newly recognized “Great Southern Reef.” A lack of assessments spanning this global biodiversity hotspot in its entirety is currently hampering an understanding of the factors that have contributed to its diversity. The common seadragon has a wide range across Australia's entire temperate south and includes a geogenetic break over a former land bridge, which has called its status as a single species into question. As a popular aquarium display that sells for high prices, common seadragons are also vulnerable to illegal capture. RESULTS: Here, we provide range-wide nuclear sequences (986 variable Ultraconserved Elements) for 198 individuals and mitochondrial genomes for 140 individuals to assess species status, identify genetic units and their diversity, and trace the source of two poached individuals. Using published data of the other two seadragon species, we found that lineages of common seadragons have diverged relatively recently (< 0.63 Ma). Within common seadragons, we found pronounced genetic structure, falling into three major groups in the western, central, and eastern parts of the range. While populations across the Bassian Isthmus were divergent, there is also evidence for secondary contact since the passage opened. We found a strong cline of genetic diversity from the range center tapering symmetrically towards the range peripheries. Based on their genetic similarities, the poached individuals were inferred to have originated from around Albany in southwestern Australia. CONCLUSIONS: We conclude that common seadragons constitute a single species with strong geographic structure but coherence through gene flow. The low genetic diversity on the east and west coasts is concerning given that these areas are projected to face fast climate change. Our results suggest that in addition to their life history, geological events and demographic expansions have all played a role in shaping populations in the temperate south. These insights are an important step towards understanding the historical determinants of the diversity of species endemic to the Great Southern Reef. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01628-9.