The phylogeny and divergence times of leaf-mining flies (Diptera: Agromyzidae) from anchored phylogenomics

Authors: XUAN, JING-LI - North Carolina State University; Scheffer, Sonja; Lewis, Matthew; CASSEL, B - North Carolina State University; LIU, WAN-XUE - North Carolina State University; WIEGMANN, BRIAN - North Carolina State University

Submitted to: Molecular Biology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/31/2023
Publication Date: 4/17/2023
Citation: Xuan, J., Scheffer, S.J., Lewis, M.L., Cassel, B.K., Liu, W., Wiegmann, B. 2023. The phylogeny and divergence times of leaf-mining flies (Diptera: Agromyzidae) from anchored phylogenomics. Molecular Biology and Evolution. 184:Article e107778. https://doi.org/10.1016/j.ympev.2023.107778.
DOI: https://doi.org/10.1016/j.ympev.2023.107778

Interpretive Summary: Leafmining flies are important pests of hundreds of agricultural crops, causing millions of dollars in losses each year to US and global food production. Due to their small size, the identification and taxonomy of these flies has been problematic. This research uses hundreds of gene sequences to infer evolutionary relationships within leafmining flies. Recent nomenclatural changes were confirmed and a new subfamily proposed. The phylogeny was used to investigate the evolution of host-use as well as the timing of diversification. This work will be of interest to scientists in multiple disciplines (e.g., taxonomists, evolutionary biologists, ecologists).

Technical Abstract: Leaf-mining flies (Diptera: Agromyzidae) are a diverse clade of phytophagous Diptera known largely for their economic impact as leaf- or stem-miners on vegetable and ornamental plants Higher-level phylogenetic relationships of Agromyzidae have remained uncertain because of challenges in sampling of both taxa and characters for morphology and PCR-based Sanger-era molecular systematics. Here, we used hundreds of orthologous single-copy nuclear loci obtained from anchored hybrid enrichment (AHE) to reconstruct phylogenetic relationships among the major lineages of leaf-mining flies. Resulting phylogenetic trees are highly congruent and well-supported, except for a few deep nodes, when using different molecular data types and phylogenetic methods. Based on divergence time dating using a relaxed clock and model-based historical biogeography analysis, leaf-mining flies are shown to have originated in the Nearctic Region at approximately 64.47 million years ago. Diversification and speciation rates in Agromyzidae increased rapidly during the Miocene, a pattern which may be attributable to vicariance events associated with the disjunction of North American and Eurasian plates, and with numerous host plant shifts in multiple agromyzid lineages. Our study not only reveals a revised classification system of leaf-mining flies, but also provides a new phylogenetic framework to understand their macroevolution.