Peruvian origin of early global invasions of five continents by the highly damaging agricultural pest Liriomyza huidobrensis (Diptera; Agromyzidae)

Authors: Scheffer, Sonja; Lewis, Matthew; WEINTRAB, PHYLLIS - Gilat Research Center; MUJICD, NORMA - International Potato Center; MACVEAN, CHARLES - St Francis University; BLANCO-METZLER, HELGA - Universidad De Costa Rica; JOSHI, RAVINDRA - University Of The Philippines; JACOBSEN, FRODE - Cornell College - Iowa; ADJAKWAH, ERIC - State Of Maryland

Submitted to: Evolutionary Applications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/20/2024
Publication Date: 10/21/2024
Citation: Scheffer, S.J., Lewis, M.L., Weintrab, P., Mujicd, N., Macvean, C., Blanco-Metzler, H., Joshi, R., Jacobsen, F., Adjakwah, E. 2024. Peruvian origin of early global invasions of five continents by the highly damaging agricultural pest Liriomyza huidobrensis (Diptera; Agromyzidae). Evolutionary Applications. 17(10). e13702. https://doi.org/10.1111/eva.13702.
DOI: https://doi.org/10.1111/eva.13702

Interpretive Summary: The pea leafminer is an invasive insect pest that attacks a wide range of vegetable and flower crops worldwide, with global economic losses of millions of dollars annually. This leafminer began to spread from its native range of South America in the 1980s. This research used DNA sequence data to explore genetic variation in the native and introduced populations worldwide. Introduced populations possess only a fraction of the genetic variation present in the native range, and Peru was identified as the ultimate source of all invasive populations. Large population sizes in Peru in combination with the evolution of insecticide resistance in the 1980s may have precipitated the spread of this species. This research will be used by entomologists, evolutionary biologists, and quarantine officials.

Technical Abstract: Identification of the geographic origin(s) of an invasive species can be critical to effective management and amelioration of negative impacts in the introduced range. Liriomyza huidobrensis Blanchard is a polyphagous leafmining fly that is a devastating pest of many vegetable and floriculture crops around the world. Native to South America, L. huidobrensis became invasive in the 1980s and has spread to at least 30 countries on five continents. We used phylogeographic analysis of over 2kb of mitochondrial cytochrome oxidase I and II sequence data from 403 field collected specimens from both native and introduced populations to investigate the geographic origins of invasive L. huidobrensis worldwide. Within South America there was substantial genetic variation, as well as the strong phylogeographic structure typical of a native range. In contrast, leafminers from the introduced range and Central America all shared a subset of the same small set of haplotypes, consistent with a history of bottlenecks during introductions. The ultimate origin of globally invasive populations was Peru as essentially all haplotypes from introduced populations were located in Peru and clustered with Peruvian samples in a Neighbor-Joining analysis. Within Peru, the primary port of export is Lima, and samples from this region shared an extremely similar pattern of reduced haplotype variation and composition to the invasive populations. This indicates a pre-invasive reduction in genetic variation within Peru, prior to the export of infested produce. Rather than what first appears to be a pattern of mitochondrial bottlenecks due to founding events during invasions by L. huidobrensis, is seems that evolutionary or other events occurred prior to the global spread of this damaging pest. This is consistent with what is known about the evolution of insecticide resistance and the development of outbreak populations in Peruvian populations prior to the global expansion of this pest.