Whole Genome Resequencing Reveals the Evolutionary History and Geographic Isolation of the eastern Asian Hickory (Carya)

Abstract

Abstract Background The biogeographic characteristics of disjunctive distribution play a crucial role in plant geography and understanding mechanisms related to endangerment. Genome sequencing offers an opportunity to explore genetic relationships, population dispersal, and the floristic evolution of disjunctively distributed flora. In this study, we conducted comprehensive whole-genome deep resequencing of EA Carya to elucidate their evolutionary history and the factors contributing to disjunctive distribution. Results After conducting high-depth sequencing of five EA Carya species and filtering the data, we obtained a dataset comprising 3,869,439 high-quality SNPs. The phylogenetic analysis of the entire Carya revealed two monophyletic clades, separating EA Carya from NA Carya. Population genetic analysis indicated that C. kweichowensis, an endangered species, exhibited the lowest nucleotide diversity and the earliest divergence among the studied EA Carya species. Through selection elimination analysis, we identified a set of adaptive genes in C.hunanensis characterized by the highest nucleotide diversity and the widest distribution compared to other EA Caryaspecies. These genes were primarily associated with mitochondrial function and alkaloid biosynthesis. Additionally, species distribution modeling predicted the suitable habitat for the five EA Carya species, revealing the potential distribution of the endangered C. kweichowensis. Importantly, our analysis indicated minimal spatial overlap in distribution regions among EA Carya species during different time periods. Conclusions The results of population historical dynamics combined with climate and geological changes support the hypothesis that EA Carya migrated from NA to Europe during the Paleogene or Eocene and continued their migration to Asia, subsequently moving eastward until reaching EA. The uneven regional distribution of EA Carya is believed to be a consequence of Quaternary climate fluctuations, mountain barriers hindering species dispersal, and the limited cold tolerance of these trees. EA Carya highlight the significant role of climate and geological changes in their regional distribution and migration routes in Asia. Furthermore, the discovery of potential habitats offers a promising avenue for the conservation of C. kweichowensis.