Characterization of genome-wide phylogenetic conflict uncovers evolutionary modes of carnivorous fungi

Mass extinction has often paved the way for rapid evolutionary radiation, resulting in the emergence of diverse taxa within specific lineages. The emergence and diversification of carnivorous nematode-trapping fungi (NTF) in Ascomycota have been linked to the Permian-Triassic (PT) extinction, but the processes underlying NTF radiation remain unclear. We conducted phylogenomic analyses using 23 genomes that represent three NTF lineages, each employing distinct nematode traps—mechanical traps (Drechslerella spp.), three-dimensional (3D) adhesive traps (Arthrobotrys spp.), and two-dimensional (2D) adhesive traps (Dactylellina spp.), and the genome of one non-NTF species as the outgroup. These analyses revealed multiple mechanisms that likely contributed to the tempo of the NTF evolution and rapid radiation. The species tree of NTFs based on 2,944 single-copy orthologous genes suggested that Drechslerella emerged earlier than Arthrobotrys and Dactylellina. Extensive genome-wide phylogenetic discordance was observed, mainly due to incomplete lineage sorting (ILS) between lineages. Two modes of non-vertical evolution (introgression and horizontal gene transfer) also contributed to phylogenetic discordance. The ILS genes that are associated with hyphal growth and trap morphogenesis (e.g., those associated with the cell membrane system and polarized cell division) exhibited signs of positive selection. IMPORTANCE By conducting a comprehensive phylogenomic analysis of 23 genomes across three NTF lineages, the research reveals how diverse evolutionary mechanisms, including ILS and non-vertical evolution (introgression and horizontal gene transfer), contribute to the swift diversification of NTFs. These findings highlight the complex evolutionary dynamics that drive the rapid radiation of NTFs, providing valuable insights into the processes underlying their diversity and adaptation.