The Impact of Fast Radiation on the Phylogeny of Bactrocera Fruit Flies as Revealed by Multiple Evolutionary Models and Mutation Rate-Calibrated Clock

SIMPLE SUMMARY: Comparative approaches are widely used to investigate the traits that underlie particular biological and ecological traits. They are effective, however, only if we know the correct relationships among the species under consideration. Here, we aimed at reconstructing a robust phylogeny for selected true fruit flies of the genus Bactrocera, which are well known as important agricultural pests worldwide. Existing phylogenetic inferences are still ambiguous, especially concerning the relationship between the two major pests B. dorsalis and B. tryoni. In this study, we employed a genome-scaled dataset and different models of molecular evolution to reconstruct the phylogenetic relationships of ten Bactrocera species and two outgroups and further date their divergence times. The resulting phylogeny fully supports B. dorsalis as more closely related to B. latifrons than to B. tryoni, opposite to what was supported by previous works. This incongruence likely derives from a fast divergence of these lineages, as revealed by our clock analysis, which can lead to conflicting results when using few genetic markers. Our results thus highlight the utility of using large datasets and of exploring different evolutionary models to study the evolutionary history of species of economic importance. ABSTRACT: Several true fruit flies (Tephritidae) cause major damage to agriculture worldwide. Among them, species of the genus Bactrocera are extensively studied to understand the traits associated with their invasiveness and ecology. Comparative approaches based on a reliable phylogenetic framework are particularly effective, but several nodes of the Bactrocera phylogeny are still controversial, especially concerning the reciprocal affinities of the two major pests B. dorsalis and B. tryoni. Here, we analyzed a newly assembled genomic-scaled dataset using different models of evolution to infer a phylogenomic backbone of ten representative Bactrocera species and two outgroups. We further provide the first genome-scaled inference of their divergence by calibrating the clock using fossil records and the spontaneous mutation rate. The results reveal a closer relationship of B. dorsalis with B. latifrons than to B. tryoni, contrary to what was previously supported by mitochondrial-based phylogenies. By employing coalescent-aware and heterogeneous evolutionary models, we show that this incongruence likely derives from a hitherto undetected systematic error, exacerbated by incomplete lineage sorting and possibly hybridization. This agrees with our clock analysis, which supports a rapid and recent radiation of the clade to which B. dorsalis, B. latifrons and B. tryoni belong. These results provide a new picture of Bactrocera phylogeny that can serve as the basis for future comparative analyses.