Phylogenomic conflict in Lycium (Solanaceae): Revealing the roles of hybridization, incomplete lineage sorting, and biogeographic history using nuclear and mitochondrial genomes.

Abstract

The genus Lycium is of considerable medicinal and economic importance and has a discontinuous intercontinental distribution. However, its evolutionary history remains obscured by morphological convergence, hybridization, and incomplete lineage sorting (ILS). Here, we conducted the first phylogenomic study of Lycium, integrating three independent genomic compartments, single-copy nuclear genes, mitochondrial genomes, and published plastid data to reconstruct its history and dissect the roles of incomplete lineage sorting, hybridization, and long-distance dispersal in its evolution. Both concatenation and coalescence methods based on nuclear genes yielded a congruent, well-resolved phylogeny, strongly supporting the monophyly of Lycium and recovering five major clades with a North American lineage as sisters to all the others. This phylogeny reveals significant conflicts with the traditional morphology. Our analyses clarify the primary cause of two distinct types of conflict. First, the pervasive tripartite (nuclear-plastid-mitochondrial) topological discordance is primarily linked to historical hybridization and introgression events, as demonstrated by strong gene-flow signals and detailed network models. In contrast, the discordance observed among gene trees appears to be predominantly influenced by incomplete lineage sorting, with some nodes exhibiting peaks exceeding 60%, indicative of rapid radiation during the Miocene epoch. Divergence dating and ancestral area reconstruction support a North American origin in the early Miocene (∼21.84 Ma), followed by sequential long-distance dispersal to South America across the Pacific, Africa, and Eurasia. Collectively, our results establish a process-based framework for Lycium's complex evolutionary history, highlighting the interplay of rapid radiation, quantified ILS, modeled hybridization, and bird-mediated dispersal in shaping its intercontinental distribution.