Genomic evidence for polyphyletic origins and interlineage gene flow within complex taxa: a case study of Picea brachytyla in the Qinghai-Tibet Plateau

Hybridization and introgression are believed to play important roles in plant evolution. However, few empirical studies have been designed to clarify the ways in which these processes complicate taxonomic delimitation. Recent phylogenetic studies based on a number of different DNA fragments have indicated that Picea brachytyla in the eastern Qinghai-Tibet Plateau is polyphyletic, a finding that contrasts with traditional taxonomy based on morphological traits. We aimed to test this conflict using transcriptomic data from 26 trees collected from multiple localities for this and related species. Our phylogenomic analyses suggest that the sampled trees of P. brachytyla cluster into two distinct lineages corresponding to the two taxonomically recognized intraspecific varieties: var. brachytyla and var. complanata. However, var. complanata nested within Picea likiangensis and was sister to one of its three varieties, while var. brachytyla comprised an isolated lineage. The polyphyletic origin hypothesis was further supported by likelihood tree comparisons using Akaike's information criterion (AIC) and by coalescent analyses under the SNAPP model. However, our ABBA-BABA and partial derivative A partial derivative I analyses suggest that gene flow between these two independently evolved lineages has been extensive and bidirectional. Introgression, as well as parallel evolution in the arid habitats common to both lineages, may have given rise to their morphological similarity. Our study highlights the importance of genomic evidence and the use of newly developed coalescent analysis methods for clarifying the evolutionary complexity of certain plant taxa.