Pleistocene demographic histories dominate contemporary genomic diversity in a continental radiation of Himalayan-Hengduan songbirds

Abstract

While population genetic theory expects genetic diversity to scale predictably with population size, mounting empirical evidence has challenged this fundamental prediction. This striking inconsistency has prompted a paradigm shift in our understanding of the determinants of genetic diversity, driving increased efforts to disentangle the relative contributions of Pleistocene demography and linked selection. Here, based on systematic sampling and a unified analytical pipeline, we de novo assembled genomes for 120 songbird species breeding in the Himalayas-Hengduan Mountains (HHMs) and conducted population genomic analysis to examine the drivers of their genomic diversity. We observed a 6.5-fold variation in genome-wide heterogeneity and a 16.4-fold variation nucleotide diversity and across species. Notably, these measures of genomic diversity showed no correlation with recent population dynamics, current population size, or other contemporary factors--such as natural selection, elevational distribution, or life-history traits. Instead, historical demography strongly predicted genetic diversity, with ancestral population size during the late Pleistocene emerging as the sole correlate: larger ancestral sizes consistently coincided with higher diversity. These findings underscore the critical influence of historical demography on contemporary genetic diversity in natural populations--an insight essential for designing effective conservation strategies.