Genome-wide SNP data reveal hidden hierarchical population structure and demographic history of endangered...

The endangered black-and-white snub-nosed monkey (Rhinopithecus bieti), endemic to high-altitude forests in southwest China, has increased from fewer than 1,500 individuals pre-1990 to over 3,500 post-2010. However, it faces severe habitat fragmentation, with at least 20 isolated groups. A comprehensive investigation of large-scale population genomic analysis is lacking. We present the first comprehensive genomic reassessment of this species using fecal-DNA and targeted capture sequencing to generate genome-wide single-nucleotide polymorphism data for 309 individuals. We identified five distinct genetic populations (Southwest, Southeast, Central, North-Central, and North) with strong geographic associations. Furthermore, we found previously unrecognized subpopulations, primarily associated with isolation within human-altered landscapes. Roads and human settlements were the primary barriers to contemporary genetic connectivity. Genetic diversity is highest centrally and declines peripherally, reflecting historical/recent barriers. Demographic inference suggests: (i) a possible southwestern origin and northward dispersal at ∼128.5 to 8.2 ka, probably driven by late Pleistocene climatic oscillations and local refugia; (ii) major subpopulation divergences within the last ∼610 to 120 years ago, likely due to human exploitation; and (iii) a sharp decline ∼300 years ago, leaving extremely low effective population size (40 to 314). Admixture origins of both Southeast and North-Central populations highlight their role in facilitating gene flow. Historically, habitats with high connectivity contrast with current severe fragmentation, particularly in the southern regions; this persistent suitability disparity suggests limited historical connectivity promoting genetic divergence between southern and central/northern populations. Our results provide critical insights into the population structure and evolutionary history of R. bieti, offering critical insights for conservation and demonstrating the power of fecal genomics in endangered species.