Regional history outweighs phylogeny in shaping recent demographic trajectories of Indo-West Pacific sea snakes
Aim Understanding how biodiversity is formed and distributed is fundamental to anticipating how populations will respond to ongoing climate change and conserving future diversity. Sea snakes are a recent marine radiation comprising replicate lineages separated by vicariance and long-term isolation among major Indo-Pacific ocean basins. This system provides a powerful opportunity for testing whether demographic trajectories are shaped by regional history, phylogeny, or geographic range size. We therefore compare the demographic and phylogeographic histories of fully marine sea snakes to evaluate the role of Pleistocene climate change in structuring biodiversity across major biogeographic regions, including the global marine hotspot of the Indo-Australian Archipelago. Location Indo-Pacific tropical and sub-tropical marine. Methods We quantified demographic trajectories using whole-genome sequencing and integrated these with a broad-scale phylogeographic analysis of genome-wide single nucleotide polymorphisms (SNP). SNP sequencing used 652 individuals to investigate the phylogeographic structure of 20 species across the Indian Ocean, Southeast Asian and Australian West-Pacific biogeographic regions. Whole genome data from 36 individuals provided coalescent estimates of effective population size (Ne) through time. These Ne trajectories were then analysed using phylogenetic comparative methods to test the effects of regional history, phylogeny, and geographic range size. Results Distinct within-species phylogeographic structure was uncovered between the regions supporting vicariance across biogeographic barriers. Ne trajectories in the last 200 thousand years (kyr) were more strongly influenced by regional history than by phylogeny or contemporary range size. Southeast Asian lineages maintained the largest historical populations and experienced the shallowest population declines compared to lineages in the Indian Ocean and Australian West-Pacific. These results are consistent with the role of the marine biodiversity hotspot centred on the Indo-Australian Archipelago (IAA) as a region of long-term population persistence and stability during Pleistocene climatic fluctuations. Main Conclusions Demographic responses to Pleistocene climate change are strongly region-specific across the Indo-West Pacific, reflecting variation in habitat persistence and connectivity among ocean basins. Over the last 200kyr, regional biogeographic history is a stronger determinant of demographic history than shared ancestry and species range size. Based on these patterns, we recommend a hierarchical conservation framework in which ocean basins represent primary management units, and within-basin genetic structure informs finer-scale spatial planning. Of particular concern are Indian Ocean lineages, which exhibit lower effective population sizes and face intense fishing pressure and habitat loss. In contrast, Australian populations maintain relatively high genetic diversity and may represent an important regional refuge under future change. The demographic stability of Southeast Asian lineages supports the IAA as a long-term centre of population persistence, but this historical resilience offers little protection against current pressures: shallow marine habitats in the region are heavily degraded and sea snakes are directly harvested for trade.