Begomovirus species demarcation based on genome-sequence identity yields non-monophyletic species: a case study of sweet potato-infecting begomoviruses

Abstract Sweepoviruses are single stranded DNA viruses in the genus Begomovirus which infect sweet potato (Ipomoea batatas). The Geminiviridae and Tolecusatellitidae study group of the International Committee for the Taxonomy of Viruses (ICTV) specifies a percent nucleotide identity threshold for species demarcation, but these criteria have not been systematically applied across sweepoviruses. Simultaneously, ICTV aims for species to be monophyletic. A maximum likelihood phylogeny of 398 full genome sequences of sweepoviruses only supported the monophyly of four of 14 ICTV-recognized species. Another species has a well-supported paraphyly, which is a legitimate biological possibility for these viruses. These analyses revealed a distinct difference in isolates of the sweet potato leaf curl Hubei virus (Begomovirus ipomoeahubeiense) versus isolates of all other species, a result substantiated by previous findings that this species is the product of recombination with a non-sweepovirus begomovirus. We found extensive recombination amongst the sweepoviruses, including across species boundaries, which is at odds with the goal of monophyletic species. Reclassifying the current sequences of sweepoviruses under the ICTV-specified species delineation would cut the number of sweepovirus species in half, and only five of these seven species could be considered monophyletic. Our analyses highlight the failure of a percent nucleotide identity threshold to create monophyletic species. The particularly low threshold for novel species in Begomovirus also conflates lineages that are mostly separately evolving into a single species, leading to average percent nucleotide identities within species that are less than the threshold for being members of the same species (