Revisiting the History and Biogeography of Bactrocera oleae and Other Olive-Feeding Fruit Flies in Africa and Asia

Abstract

Bactrocera oleae Rossi causes important agricultural losses in olive growing regions. Despite its economic relevance, the expansion history and biogeography of B. oleae and other olive-feeding fruit flies remain unclear. We used mitogenomic data of Bactrocera species from a broad geographic range to explore possible historical biogeographic patterns in B. oleae and other olive-feeding fruit flies. Our data suggest that (1) the transition from stenophagy on Oleaceae to oligophagy on Olea most likely occurred in Africa more than 6 million years ago (MYA), and (2) the subsequent transition to monophagy on Olea europaea took place in Asia or in Africa in the Early Pleistocene. Our results support equally the hypotheses that the ancestors of modern B. oleae underwent two waves of migration from Asia to Africa or that they zigzagged between Asia and Africa.

Keywords: Olea europaea; Oleaceae; mitochondrial; olive fruit fly; phylogeography.

Figure 1

(a) Geographic distribution of Bactrocera oleae, Bactrocera biguttula, and Bactrocera munroi. The points were drawn based on data from the EPPO Global Database (accessed on 1 December 2024), the True Fruit Flies of the Afrotropical Region database of the Royal Museum for Central Africa, and the authors’ observations. (b) Time-calibrated phylogenetic tree of the genus Bactrocera based on new and publicly available mitogenome sequences (n = 36) with representatives of other Tephritidae species in the genera Dacus, Zeugodacus, Neoceratitis, Ceratitis, and Procecidochares as outgroup. The olive-feeding fruit fly clade, for which the present-day distribution is represented in (a), is highlighted in green, and all other species have their native range in the Asia-Pacific region. The scale bar represents time in millions of years ago, and the blue bars across nodes represent the 95% confidence intervals around the mean of the estimated split dates. Nodal support is shown as posterior probability and bootstrap on the nodes relevant for the phylogenetic relationships among olive-feeding fruit flies.

Figure 2

Time-calibrated phylogenetic tree of olive-feeding fruit flies displaying the divergence between Bactrocera biguttula and Bactrocera munroi (both native to Africa, shown at the bottom of the tree), and the Bactrocera oleae branch (presently widespread) based on new and publicly available mitogenome sequences (n = 36). The scale bar represents time in million years. Asterisks represent nodes with full support (posterior probability = 1; bootstrap = 100). Red branches—Asian lineages (Pakistan); green branches—African lineages (B. munroi and B. biguttula, and B. oleae from Kenya, South Africa and Namibia); blue branches—Mediterranean lineages Turkey, Israel, USA, Iran, Italy, Algeria, Portugal, Morocco); grey branch—lineages of undetermined origin (Reunion).

Figure 3

Hypotheses for the phylogenetic history of olive-feeding fruit flies: (1) Initial origin and dispersion of fruit flies stenophagous on Oleaceae. Dispersion of stenophagous fruit flies may have reached Africa, as indicated by the question mark. (2) Subsequent transition to oligophagy on Olea may have occurred in Asia (short yellow arrow) or in Africa (short turquoise arrow) in the Late Miocene (>6 MYA). In either case, these oligophagous olive fruit flies reached both continents (long arrows). The extant geographic range is depicted (purple). (3) Later, the transition to monophagy in Olea europaea occurred in Asia in the Early Pliocene (~4 MYA), with subsequent dispersion throughout the historic geographic range of the host. Arrows indicate the direction of dispersals, and shaded areas indicate approximate geographic ranges.

Figure 3

Hypotheses for the phylogenetic history of olive-feeding fruit flies: (1) Initial origin and dispersion of fruit flies stenophagous on Oleaceae. Dispersion of stenophagous fruit flies may have reached Africa, as indicated by the question mark. (2) Subsequent transition to oligophagy on Olea may have occurred in Asia (short yellow arrow) or in Africa (short turquoise arrow) in the Late Miocene (>6 MYA). In either case, these oligophagous olive fruit flies reached both continents (long arrows). The extant geographic range is depicted (purple). (3) Later, the transition to monophagy in Olea europaea occurred in Asia in the Early Pliocene (~4 MYA), with subsequent dispersion throughout the historic geographic range of the host. Arrows indicate the direction of dispersals, and shaded areas indicate approximate geographic ranges.