Genomic data reveal historical introgression and genetic erosion across an imperiled radiation of Caribbean Spondylurus skinks

Abstract

Understanding how island biodiversity originates and persists is central to evolutionary biology and conservation. Caribbean islands, shaped by repeated cycles of isolation and connectivity, provide a natural laboratory to evaluate how dispersal, divergence, and introgression interact during diversification. Here we use low-coverage whole-genome data from modern and historical specimens of Caribbean Spondylurus skinks, sampling 14 of 17 described species, to reconstruct the evolutionary history and assess current genetic diversity of this insular radiation. Phylogenomic analyses of mitochondrial and nuclear single nucleotide polymorphisms reveal pervasive discordance among gene trees, extensive introgression, and reject a simple stepping-stone model of diversification across the Caribbean. Instead, Spondylurus diversification reflects repeated long-distance dispersal, gene flow following divergence, and persistence on small islands and cays. Genomic patterns of diversity, runs of homozygosity, effective population sizes, and genetic loads show strong contrasts among species with different recent demographic histories, including severe inbreeding, elevated realized genetic load, and sharp population declines associated with invasive predators. Historical specimens exhibit higher heterozygosity and lower genetic load than contemporary samples, indicating rapid genomic erosion over the last century. Together, our results highlight introgression as a persistent force shaping Caribbean skink evolution and reveal urgent conservation risks driven by recent demographic collapse and loss of genomic resilience.