UCE data reveal multiple origins of rose gallers in North America: Global phylogeny of Diplolepis Geoffroy (Hymenoptera: Cynipidae)

• Published in: Molecular phylogenetics and evolution Vol. 153; p. 106949
• Main Authors: Zhang, Y. Miles, Buffington, Matthew L., Looney, Chris, László, Zoltán, Shorthouse, Joseph D., Ide, Tatsuya, Lucky, Andrea
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.12.2020
• Subjects: Ancestral state reconstruction; Animals; Biogeography; Conserved Sequence - genetics; Diplolepis; Gall wasp; galls; Genes, Mitochondrial - genetics; herbivores; host plants; leaves; mitochondrial genes; monophyly; Nearctic region; North America; Palearctic region; Phylogenomic; Phylogeny; Rosa; Rosa - parasitology; stems; Target capture; topology; Ultraconserved elements; Wasps - classification; Wasps - genetics; North America; Biogeography; Ancestral state reconstruction; Ultraconserved elements; Target capture; Phylogenomic; Gall wasp
• ISSN: 1055-7903; 1095-9513; 1095-9513
• DOI: 10.1016/j.ympev.2020.106949

[Display omitted] •First phylogenomic study of global rose gall wasps (Diplolepis), which employed UCEs.•Two main clades, one with Nearctic stem-galler, and other Holarctic leaf-galler taxa.•Historical biogeographic reconstruction confirms two independent incursions into the Nearctic.•Leaf galling is the ancestral state, and shifts to other host organs are relatively rare. Gall wasps in the genus Diplolepis Geoffroy are specialized herbivores that induce galls exclusively on roses. Despite their wide distribution across the Holarctic, little is known about their evolutionary history. Here we present the first phylogenomic tree of global Diplolepis reconstructed using Ultraconserved Elements (UCEs), resulting in a robust phylogeny based on 757 genes. Results support the existence of two principal clades: a Nearctic stem-galler clade, and a Holarctic leaf-galler clade that further splits into two Palearctic groups and one Nearctic group. This topology is congruent with a previous study based on the mitochondrial gene COI, an unexpected result given the common occurrence of mitonuclear discordance in closely related oak gall wasp lineages. Most Diplolepis species were recovered as reciprocally monophyletic, with some notable exceptions such as the D. polita and the D. ignota complex, for which species boundaries remain unresolved. Historical biogeographic reconstruction was unable to pinpoint the origin of Diplolepis, but confirms two independent incursions into the Nearctic. Ancestral state reconstruction analysis highlights the conservatism of gall location on the host plants, as shifts to different host organs are relatively rare. We suggest that Diplolepis were originally leaf gallers, with a Nearctic stem-galler clade undergoing a major plant organ switch onto rose stems. Host organ switch or reversal is uncommon, which suggests a level of conservatism. Our study showcases the resolving power of UCEs at the species level while also suggesting improvements to advance future Cynipoidea phylogenomics. Our results also highlight the additional sampling needed to clarify taxonomic relationships in the Nearctic and eastern Palearctic regions.