Uncovering ghost introgression through genomic analysis of a distinct eastern Asian hickory species

• Published in: The Plant journal : for cell and molecular biology 2024-08, Vol.119 (3), p.1386-1399
• Main Authors: Zhang, Wei‐Ping, Ding, Ya‐Mei, Cao, Yu, Li, Pan, Yang, Yang, Pang, Xiao‐Xu, Bai, Wei‐Ning, Zhang, Da‐Yong
• Format: Article
• Language: English
• Subjects: Asia, Eastern; Bifurcations; Biogeography; BPP; Carya; Carya cathayensis; Carya sinensis; Diploids; D‐statistic; East Asian People; Endangered & extinct species; gene flow; Genetic analysis; Genetic Introgression; Genome, Plant - genetics; Genomes; Genomic analysis; Genomics; ghost introgression; Interspecific hybridization; Network analysis; Phylogenetics; phylogenomics; Phylogeny; Plant species; Statistical methods
• ISSN: 0960-7412; 1365-313X; 1365-313X
• DOI: 10.1111/tpj.16859

SUMMARY Ghost introgression, or the transfer of genetic material from extinct or unsampled lineages to sampled species, has attracted much attention. However, conclusive evidence for ghost introgression, especially in plant species, remains scarce. Here, we newly assembled chromosome‐level genomes for both Carya sinensis and Carya cathayensis, and additionally re‐sequenced the whole genomes of 43 C. sinensis individuals as well as 11 individuals representing 11 diploid hickory species. These genomic datasets were used to investigate the reticulation and bifurcation patterns within the genus Carya (Juglandaceae), with a particular focus on the beaked hickory C. sinensis. By combining the D‐statistic and BPP methods, we obtained compelling evidence that supports the occurrence of ghost introgression in C. sinensis from an extinct ancestral hickory lineage. This conclusion was reinforced through the phylogenetic network analysis and a genome scan method VolcanoFinder, the latter of which can detect signatures of adaptive introgression from unknown donors. Our results not only dispel certain misconceptions about the phylogenetic history of C. sinensis but also further refine our understanding of Carya's biogeography via divergence estimates. Moreover, the successful integration of the D‐statistic and BPP methods demonstrates their efficacy in facilitating a more precise identification of introgression types. Significance Statement Hybridization and introgression are widely recognized as significant factors in plant evolution, but the possibility of carrying ancient traits from ancestors that are now extinct (i.e., ghost introgression) has been mostly overlooked in plants. In this study, we employed whole‐genome sequencing datasets using a new combined method to spot this for the first time in hickory trees and anticipate more ghost introgression events to be discovered following this methodology.