Episodic radiations in the fly tree of life

Abstract

Flies are one of four superradiations of insects (along with beetles, wasps, and moths) that account for the majority of animal life on Earth. Diptera includes species known for their ubiquity (Musca domestica house fly), their role as pests (Anopheles gambiae malaria mosquito), and their value as model organisms across the biological sciences (Drosophila melanogaster). A resolved phylogeny for flies provides a framework for genomic, developmental, and evolutionary studies by facilitating comparisons across model organisms, yet recent research has suggested that fly relationships have been obscured by multiple episodes of rapid diversification. We provide a phylogenomic estimate of fly relationships based on molecules and morphology from 149 of 157 families, including 30 kb from 14 nuclear loci and complete mitochondrial genomes combined with 371 morphological characters. Multiple analyses show support for traditional groups (Brachycera, Cyclorrhapha, and Schizophora) and corroborate contentious findings, such as the anomalous Deuterophlebiidae as the sister group to all remaining Diptera. Our findings reveal that the closest relatives of the Drosophilidae are highly modified parasites (including the wingless Braulidae) of bees and other insects. Furthermore, we use micro-RNAs to resolve a node with implications for the evolution of embryonic development in Diptera. We demonstrate that flies experienced three episodes of rapid radiation--lower Diptera (220 Ma), lower Brachycera (180 Ma), and Schizophora (65 Ma)--and a number of life history transitions to hematophagy, phytophagy, and parasitism in the history of fly evolution over 260 million y.

Fig. 1.

Combined molecular phylogenetic tree for Diptera. Partitioned ML analysis of combined taxon sets of tier 1 and tier 2 FLYTREE data samples (−lnL = 344155.6169) calculated in RAxML. Circles indicate bootstrap support >80% (black/bp = 95–100%, gray/bp = 88–94%, white/bp = 80–88%). Nodes with improved bootstrap values resulting from postanalysis pruning of unstable taxa are marked by stars (black/bp = 95–100%, gray/bp = 88–94%, white/bp = 80–88%). Colored squares on terminal branches indicate the presence, in at least one species of a family, of ecological traits as shown to lower left. The number of origins of each trait was estimated with reference to the phylogeny, the distribution of each trait among genera within a family, and the known biology of the organisms.

Fig. 2.

Phylogenetic distribution of known dipteran miRNA families showing synapomorphic accumulation of miRNA through phylogeny (29). The values below each node are the number of unique miRNAs shown to have been acquired in that lineage, and the numbers above each node are miRNA families that have been lost.

Fig. 3.

Chronogram depicting dipteran phylogeny and estimated age of clade divergences. Shaded boxes correspond to areas of rapid radiation and phylogenetic uncertainty. These regions (lower Diptera, lower Brachycera, and Schizophora) are considered major periods of rapid diversification in flies. The vertical height of each triangle represents the approximate number of described species in corresponding clades, with the scale bar indicating 10,000 species.