Phylogenomics reveals accelerated late Cretaceous diversification of bee flies (Diptera: Bombyliidae)

Abstract

Bombyliidae is a very species-rich and widespread family of parasitoid flies with more than 250 genera classified into 17 extant subfamilies. However, little is known about their evolutionary history or how their present-day diversity was shaped. Transcriptomes of 15 species and anchored hybrid enrichment (AHE) sequence captures of 86 species, representing 94 bee fly species and 14 subfamilies, were used to reconstruct the phylogeny of Bombyliidae. We integrated data from transcriptomes across each of the main lineages in our AHE tree to build a data set with more genes (550 loci versus 216 loci) and higher support levels. Our overall results show strong congruence with the current classification of the family, with 11 out of 14 included subfamilies recovered as monophyletic. Heterotropinae and Mythicomyiinae are successive sister groups to the remainder of the family. We examined the evolution of key morphological characters through our phylogenetic hypotheses and show that neither the "sand chamber subfamilies" nor the "Tomophthalmae" are monophyletic in our phylogenomic analyses. Based on our results, we reinstate two tribes at the subfamily level (Phthiriinae stat. rev. and Ecliminae stat. rev.) and we include the genus Sericosoma Macquart (previously incertae sedis) in the subfamily Oniromyiinae, bringing the total number of bee fly subfamilies to 19. Our dating analyses indicate a Jurassic origin of the family , with the sand chamber evolving early in bee fly evolution, in the late Jurassic or mid-Cretaceous (100-165 Ma). We hypothesize that the angiosperm radiation and the hothouse climate established during the late Cretaceous accelerated the diversification of bee flies, by providing an expanded range of resources for the parasitoid larvae and nectarivorous adults.

The Angiosperm Terrestrial Revolution and the origins of modern biodiversity

“…This pattern is supported by direct evidence of Cretaceous angiosperm–fly mutualism – remains of angiosperm pollen grains in their guts as well as nectar‐feeding mouthparts, consistent with their modern representatives (Grimaldi & Engel, 2005). Phylogenomic data suggest that Bombyliidae, over 5000 species of bee flies, show accelerated evolution in the Late Cretaceous linked to warmer climates and the diversification of angiosperms, which provided expanded resources for their parasitoid larvae and nectar‐feeding adults (Li et al ., 2021).…”

Phylogenomic Subsampling and the Search for Phylogenetically Reliable Loci

“…Ultimately, levels of both signal and noise are manifestations of underlying differences in rates of evolution. Rate-based subsampling is therefore also common, but there seems to be little consensus on how it should be implemented: studies have variously supported the use of molecular data that evolve at fast, intermediate, or slow rates, as well as the generation of partitions with homogenous rates (e.g., Cummins and McInerney 2011 ; Rota-Stabelli et al 2011 ; Fernández et al 2014 ; Sharma et al 2014 , 2015; Telford et al 2014 ; Streicher et al 2018 ; Rangel and Fournier 2019 ; Evangelista et al 2021 ; Li et al 2021) . These studies have also relied on different types of rate estimates—including tree- and alignment-based metrics of substitution rates, measures of character similarity and compatibility, and proportions of variable/informative sites—as well as different units of measurement (sites or loci).…”

Geographic Mosaics of Fly Pollinators With Divergent Color Preferences Drive Landscape-Scale Structuring of Flower Color in Daisy Communities

“…The genus Dimorphotheca is estimated to have arisen 20.12 (8.94–27.88) mya ( Barreda et al, 2015 ), and thus the sister species pair we studied is undoubtedly much younger, as the only taxonomically useful trait separating them is flower color ( Norlindh, 1943 ). In contrast, the split between Megapalpus (a monospecific genus) and its sister genus, Corsomyza , is substantially older (26 my – de Jager and Ellis, 2017 , 38 my – Li et al, 2020 ). This arguably makes it more likely that flower colors have diverged across a pre-existing geographic mosaic of fly species.…”