A phylogenomic approach to species delimitation in the mango fruit fly (Bactrocera frauenfeldi) complex: A new synonym of an important pest species with variable morphotypes (Diptera: Tephritidae)

Authors: DOORENWEERD, CAMIEL - University Of Hawaii; SAN JOSE, MICHAEL - University Of Hawaii; Geib, Scott; DUPUIS, JULIAN - University Of Kentucky; LEBLANC, LUC - University Of Idaho; BARR, NORMAN - Animal And Plant Health Inspection Service (APHIS); FIEGALAN, ELAIDA - Central Luzon State University; MORRIS, KIMBERLY - University Of Hawaii; RUBINOFF, DANIEL - University Of Hawaii

Submitted to: Systematic Entomology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/13/2022
Publication Date: 7/20/2022
Citation: Doorenweerd, C., San Jose, M., Geib, S.M., Dupuis, J., Leblanc, L., Barr, N., Fiegalan, E., Morris, K., Rubinoff, D. 2022. A phylogenomic approach to species delimitation in the mango fruit fly (Bactrocera frauenfeldi) complex: A new synonym of an important pest species with variable morphotypes (Diptera: Tephritidae). Systematic Entomology. 48(1):10-22. https://doi.org/10.1111/syen.12559.
DOI: https://doi.org/10.1111/syen.12559

Interpretive Summary: The Mango fruit fly is a pest fruit fly species of important concern throughout SE Asia, Oceana, and subtropical regions of the western hemisphere. It is a member of a species complex including many other species for which morphological separation of the species does not match genetic separation using mitochondrial gene sequencing. This create the problem of not knowing if a collected specimen is of concern and member of a pest group, or not of concern, being a member of a non-pest species closely related to the mango fruit fly. To resolve this, we used genome-wide sequencing of hundreds of nuclear genes to resolve the mango fruit fly species complex. Most importantly, two species, Bactrocera albistrigata and Bactrocera frauenfeldi we chose to synonomize into a single pest species based on best genetic and morphological data demonstrated in this manuscript. This resolves a longstanding issue of discrimination of these species as they should be treated as a single diverse species with variation across its population range from southeast Asia to Oceana.

Technical Abstract: The frequency with which mimicry promotes divergent selection on regional phenotypes remains poorly understood. The mango fruit fly, Bactrocera frauenfeldi, is one of seven members of a monophyletic species complex distributed across Southeast Asia, Australasia, and Oceania. We used a phylogenomic approach with highly multiplexed amplicon sequencing to test species limits and evaluate the relationships among different morphological forms in the B. frauenfeldi species complex. We obtained sequence data from 196 specimens for 395 nuclear DNA loci, totaling 102 kb, of which only 2.2 kb are parsimony informative sites. Phylogenetic analyses suggest a surprising and counter-intuitive stepwise speciation pattern westward across southern Polynesia, Melanesia, and southern Micronesia, eventually reaching peninsular Southeast Asia. Within the widespread B. frauenfeldi, we find different island forms that were traditionally recognized as two different species. Species delineation analyses over-split the island populations in the complex, likely due to a combination of insufficient data and weaknesses of the models. Based on morphology, biogeography, and phylogenetic analyses, we conclude that the two phenotypes of B. frauenfeldi represent discordant populations and regional forms of a single species, therefore we synonymize the names of two major pests: B. albistrigata (de Meijere, 1911) syn. rev. with B. frauenfeldi (Schiner, 1868). The different intraspecific phenotypes likely represent local adaptation, which is also seen in other Dacini species, suggesting that mimicry is possibly a widespread driver of evolution for this group containing hundreds of species.