Life-history traits may buffer genetic erosion under isolation in mountain sky-island systems

Abstract

Sky-island systems provide natural case studies for understanding how geography and Quaternary history shape genomes, phenotypes and life-history traits in mountain endemics. We investigated Xatartia scabra (Apiaceae), a monotypic scree specialist plant species restricted to sky-island summits in the eastern Pyrenees, by integrating population genomics with abiotic condition-informed distribution modeling. Using a ddRAD-seq-like protocol (nGBS), we genotyped 125 individuals (21,970 SNPs), and applied species distribution modeling to identify suitable environmental conditions from the Last Glacial Maximum to 2100. Genetic analyses revealed unexpected genetic "resilience", with moderate genome-wide diversity (HE = 0.17, Ho = 0.15) and low inbreeding (FIS = 0.07), despite small census sizes and strong isolation. Significant overall genetic differentiation (FST = 0.16), with pronounced summit-level structure and strong isolation-by-distance, supports deep valleys as barriers to gene flow. Abiotic niche reconstructions recovered extensive Heinrich Stadial 1 connectivity (+ 58,4% relative to present), followed by postglacial loss of suitable habitats at lower elevations and increasing fragmentation; projections under climate change forecast contraction (-61,2%, relative to present) of climatic suitability, expected to intensify drift in small, isolated populations. Demographic inferences align with this narrative, indicating postglacial decline in effective population sizes. Taken together, genetic, climatic, and demographic evidence supports a transition from historically connected lowland corridors to modern sky islands where distance-limited drift dominates. The maintenance of moderate genetic diversity and low inbreeding under strong isolation suggests that X. scabra may have evolved life-history strategies including outcrossing and monocarpy that allow limiting genetic erosion in such extreme and fragmented environments.