Monophyletic blowflies revealed by phylogenomics

Abstract

Background Blowflies are ubiquitous insects, often shiny and metallic, and the larvae of many species provide important ecosystem services (e.g., recycling carrion) and are used in forensics and debridement therapy. Yet, the taxon has repeatedly been recovered to be para- or polyphyletic, and the lack of a well-corroborated phylogeny has prevented a robust classification. Results We here resolve the relationships between the different blowfly subclades by including all recognized subfamilies in a phylogenomic analysis using 2221 single-copy nuclear protein-coding genes of Diptera. Maximum likelihood (ML), maximum parsimony (MP), and coalescent-based phylogeny reconstructions all support the same relationships for the full data set. Based on this backbone phylogeny, blowflies are redefined as the most inclusive monophylum within the superfamily Oestroidea not containing Mesembrinellidae, Mystacinobiidae, Oestridae, Polleniidae, Sarcophagidae, Tachinidae, and Ulurumyiidae. The constituent subfamilies are re-classified as Ameniinae (including the Helicoboscinae, syn. nov.), Bengaliinae, Calliphorinae (including Aphyssurinae, syn. nov., Melanomyinae, syn. nov., and Toxotarsinae, syn. nov.), Chrysomyinae, Luciliinae, Phumosiinae, Rhiniinae stat. rev., and Rhinophorinae stat. rev. Metallic coloration in the adult is shown to be widespread but does not emerge as the most likely ground plan feature. Conclusions Our study provides the first phylogeny of oestroid calyptrates including all blowfly subfamilies. This allows settling a long-lasting controversy in Diptera by redefining blowflies as a well-supported monophylum, and blowfly classification is adjusted accordingly. The archetypical blowfly trait of carrion-feeding maggots most likely evolved twice, and the metallic color may not belong to the blowfly ground plan.

Characterization and Comparative Analysis of Mitochondrial Genomes Among the Calliphoridae (Insecta: Diptera: Oestroidea) and Phylogenetic Implications

“…Our study supports Calliphoridae as a sister to (Polleniidae (Mesembrinellidae, Tachinidae)) (PP = 0.99; BP = 100) based on the mitogenomic datasets. In addition, in our study, the Calliphoridae, being monophyletic, was supported based on PCG123 and PCG123rRNA (PP = 0.99; BP = 100) (Figure 5, Supplementary Figures S4,6,7), which is consistent with previous studies based on putative synapomorphies (McAlpine, 1989a), Pape, 1992), and single-copy nuclear protein-coding genes (Yan et al, 2021). The non-monophyly status of Calliphoridae is supported here based on PCG12 using BI and ML analyses (Supplementary Figures S3,S5).…”

“…Historically, these groups have been treated as a subfamily of Calliphoridae (Pape, 1992;Rognes, 1997), but some authors have proposed that the Polleniidae and Mesembrinellidae groups have a monophyletic lineage separated from the Calliphoridae, giving family status to the group (Guimarães, 1977;Cerretti et al, 2019). This proposition was supported more recently by phylogenetic analyses based on molecular data (Kutty et al, 2010;Marinho et al, 2012;Singh and Wells, 2013;Yan et al, 2021). Our molecular phylogenetic relationship research based on mitogenomes also supports the family status of Mesembrinellidae and Polleniidae.…”

“…In our study, the sister relationships of Polleniidae and (Mesembrinellidae + Tachinidae) were supported (PP = 0.99; BP = 100) based on the most mitogenomic datasets, except for (Mesembrinellidae (Polleniidae, Tachinidae)) based on PCG12 using ML analyses ( Supplementary Figure S5 ). Polleniidae is supported as the sister group to the family Tachinidae in most molecular-based phylogenetic analyses, based on COI, CAD, EF1 α , 28 S rRNA ( Singh & Wells 2013 ), UCEs ( Buenaventura et al, 2021 ), nucleotide, and amino acid data for 1,456 single-copy protein-coding genes ( Kutty et al, 2010 ), four nuclear loci (7,800 bp) ( Stireman et al, 2019 ), and transcriptome and genomic data ( Yan et al, 2021 ). In addition, the close relationship between Tachinidae and Mesembrinellidae has been supported using molecular analyses ( Kutty et al, 2010 ).…”

“…The classification and composition of Calliphoridae subfamilies have gone through many variations (Kurahashi, 1989), ranging from five subfamilies (Calliphorinae, Chrysomyinae, Mesembrinellinae, Ameniinae, and Rhiniinae) (Hennig, 1973) to 13 subfamilies (Chrysomyinae, Calliphorinae, Luciliinae, Toxotarsinae, Melanomyinae, Auchmeromyinae, Bengaliinae, Polleniinae, Mesembrinellinae, Phumosiinae, Rhiniinae, Helicoboscinae, and Ameniinae) (Rognes, 1986;Rognes, 1991;Rognes, 1997). Yan et al (2021) redefined the blowflies as the most inclusive monophylum within the superfamily Oestroidea not containing Mystacinobiidae, Mesembrinellidae, Polleniidae, Oestridae, Tachinidae, Sarcophagidae, and Ulurumyiidae, based on 2,221 single-copy nuclear protein-coding genes. The constituent subfamilies were reclassified as Bengaliinae, Ameniinae, Chrysomyinae, Calliphorinae, Phumosiinae, Luciliinae, Rhinophorinae stat.…”

“…In addition, the monophyly and non-monophyly status of the Calliphoridae has also long been controversial. Some studies support the monophyletic status of the Calliphoridae ( Yan et al, 2021 ), while others consider them non-monophyletic or paraphyletic ( Marinho et al, 2012 ).…”