Integrative genomic insights into parallel local adaptation to Danxia and Karst edaphic islands in the endangered tree Firmiana danxiaensis

Abstract

Uncovering the genetic basis of local adaptation is a central goal in evolutionary biology. Edaphic islands, such as Karst (KL) and Danxia (DL) landforms, provide ideal natural laboratories for this endeavor. However, the mechanisms underlying parallel adaptation to contrasting edaphic extremes within a single species remain poorly understood. Firmiana danxiaensis, an endangered tree endemic to both KL and DL in the Nanling Mountains, offers a rare opportunity to address this question. We integrated a chromosome-level genome assembly, population genomic analysis of 225 individuals from 20 populations across its entire range, and genotype-environment association (GEA) with high-resolution soil and climate data. The relatively large genome of F. danxiaensis (1.51 Gb) reveals two ancient whole-genome duplications and a Quaternary burst of LTR retrotransposons, which, together with significant expanded drought-related transcription factor (TF) families, together constitute its genomic basis of adaptation. Population structure resolved four genetic lineages with distinct demography and inbreeding patterns. GEA identified stronger local adaptation in DL than KL, driven mainly by soil factors (e.g., cadmium, zinc), while climate variables (e.g., Bio9, Bio11) predominated in KL. Despite these divergent drivers, drought stress and elevated metal ion acted as major selective pressures in both landforms. Furthermore, six key TFs (e.g., NAC090, bHLH42, MAPKKK20) under both local adaptation and positive selection in DL are involved in drought response and metal ion binding, facilitating survival in stressful habitats. Our findings provide novel insights into parallel local adaptation to contrasting edaphic islands and offer concrete genomic guidance for the conservation of F. danxiaensis. Significance statementThe genetic basis of parallel local adaptation to contrasting environments remains unclear. Using the endangered tree Firmiana danxiaensis, we uncover genomic mechanisms enabling its adaptation to both Karst and Danxia edaphic islands. We demonstrate that adaptation is primarily driven by soil factors in Danxia and climate in Karst, generating divergent genomic signatures yet converge on drought response. These findings establish a framework for understanding parallel local adaptation and offer concrete genomic guidance for conservation.