Ferns, defined by large genomes, high chromosome counts, and pervasive aneuploidy as well as intraspecific polyploid complexity, diverge significantly from the classical genetic theories and analytical frameworks largely developed based on diploid models.

Studies leveraging second-generation sequencing technologies have long centered on neutral variation in noncoding genomic regions. In the absence of high-quality reference genomes, distinguishing functional coding variation from neutral genetic markers remains a major challenge, which in turn restricts systematic evaluations of natural selection, genetic load, and adaptive evolution in ferns. Against the backdrop of conservation genomics, genome-scale investigations that integrate genetic drift, inbreeding and natural selection are thus urgently required for this plant group.

To fill this knowledge gap, research teams led by Profs. CHEN Hongfeng and KANG Ming at the South China Botanical Garden of the Chinese Academy of Sciences, in collaboration with the Shanghai Chenshan Botanical Garden, Shenzhen Fairy Lake Botanical Garden, Nanning Normal University and Ghent University in Belgium, have systematically clarified the evolutionary history and genomic basis of endangerment in the rare fern Brainea insignis.

The study presents the first chromosome-level genome assembly of B. insignis, with a total assembled size of 8.62 gigabases, and carries out comprehensive comparative and population genomic analyses. The findings reveal that B. insignis underwent an ancient whole-genome duplication event shared with core leptosporangiate ferns, and its large genome size is mainly driven by the long-term accumulation of long terminal repeat retrotransposons (LTR-RTs), coupled with an overall slow rate of molecular evolution. Furthermore, the adaptive evolution of its unique arborescent stem structure is closely linked to the expansion and strong functional conservation of gene families involved in lignin biosynthesis—an explanation for the re-emergence of tree-like growth forms in this evolutionarily distant lineage.

Population genomic analyses identified three genetically distinct lineages of B. insignis distributed in Yunnan, Vietnam and South China. The species' current population structure has been shaped by multiple historical processes, including Quaternary glaciations, postglacial range expansions and regional gene flow. Unlike many endangered species that have persisted with extremely small effective population sizes for long periods, B. insignis has experienced a relatively recent demographic collapse. This event has led to a sharp decline in effective population size, elevated inbreeding levels and substantial accumulation of deleterious mutations, resulting in a marked increase in genetic load. These patterns indicate that purifying selection has not yet become the dominant evolutionary force, and the species' extant populations are on a trajectory of continued decline.

Subsequent environmental association analyses detected signals of local adaptation correlated with climatic variables across the three lineages. Genetic offset simulations predict that under future climate change scenarios, the distribution of B. insignis populations will become increasingly fragmented, with those in the southwestern Indochina Peninsula facing the highest extinction risk.

This research not only advances the field of fern genomics and elucidates the pivotal role of demographic history in shaping the genetic architecture of endangered species, but also provides theoretical foundations and scientific evidence for spatially explicit conservation strategies designed to maintain habitat connectivity and facilitate adaptive gene flow in B. insignis.

The study was recently published in Nature Communications. This work was supported by the National Key Research and Development Program of China, the Guangdong Provincial Basic and Applied Basic Research Flagship Program, and other funding sources.