Drift and isolation drive genomic erosion and island speciation in a lineage of macaques

Abstract

Allopatric speciation, especially on large islands and archipelagos, is a significant driver of evolutionary diversification, as geographic isolation fosters the independent evolution of populations1,2. In these isolated populations, lineage sorting and genetic drift dominate, accelerating allele fixation and reducing shared genetic variation3,4. Here, we investigated how sea-level transgression during the Early Holocene triggered rapid speciation in large vertebrates by studying macaques isolated on Dangan Island (DGD), located just 30 km from present-day Hong Kong. Whole-genome sequencing revealed that [~]10,000 years of isolation drove the macaques evolution into a distinct species, as indicated by pronounced genomic divergence (mean Fst > = 0.462 vs. mainland), 1.94 million lineage-specific variants, and complete ancestral differentiation with no evidence of post-isolation gene flow. A severe demographic collapse (effective population size, Ne {approx} 40) led to substantial genomic erosion (65.8% loss of genetic diversity). Paradoxically, this also enhanced resilience through drift-mediated genetic triage. Increased homozygosity exposed and purged lethal recessive alleles in lipid metabolism pathways (68% reduction in genetic load), while simultaneously fixing mildly deleterious variants--such as a splice-site mutation in SKAP2--thereby generating a form of genomic "burden" alongside rapid immune adaptation via 251 fixed missense mutations. These findings demonstrate that island isolation can drive vertebrate speciation within a few thousand years, with genetic drift playing a dominant role in shaping genomic architecture. Accordingly, conservation strategies should prioritize monitoring loss-of-function (LoF) variants in essential pathways and prescreening for deleterious allele combinations between donors and recipients prior to implementing genetic rescue in small, drift-sensitive populations.