Anchored hybrid enrichment challenges the traditional classification of flesh flies (Diptera: Sarcophagidae)

Abstract

Sarcophagidae is one of the most species‐rich families within the superfamily Oestroidea. This diversity is usually represented by three lineages: Miltogramminae, Paramacronychiinae and Sarcophaginae. Historically, the phylogenetic relationships among these lineages have been elusive, due to poorly supported hypotheses or small taxon sets, or both. This study provides a dramatic increase in molecular data, more balanced sampling of all three lineages from all biogeographical regions and a reassessment of morphological characters using scanning electron microscopy in the most comprehensive assessment of subfamily‐level phylogeny in Sarcophagidae to date. This analysis of the largest molecular dataset ever produced for a phylogenetic analysis of a fly lineage, with 950 loci from anchored hybrid enrichment comprising 435 930 bp from 101 species, revealed Paramacronychiinae as sister to Miltogramminae, not to Sarcophaginae, as suggested by adult morphology. Maximum likelihood analysis produced a well‐supported topology, with 91% of the nodes receiving strong bootstrap proportions (> 97%). In contrast to the molecular data, three out of nine morphological characters studied point to a sister‐group relationship of (Sarcophaginae + Paramacronychiinae) and the remaining six characters are either silent on subfamily relationships or in need of further study. Re‐examination of morphological structures provides new insights into the evolution of male genitalic traits within Sarcophagidae and highlights their convergence producing conflicting phylogenetic signal. Our phylogeny reconciles older and widely used systems of classification with tree‐based thinking and sets up a classification of flesh flies that is more aligned with their evolutionary history.

Protein‐encoding ultraconserved elements provide a new phylogenomic perspective of Oestroidea flies (Diptera: Calyptratae)

“…The Calyptratae radiation has been suggested as multiple episodes of rapid diversification in the early Tertiary (Kutty et al ., 2010) possibly associated with the opening of new niches following the Cretaceous‐Palaeogene mass extinction event (Cerretti et al ., 2017). Our results are concordant with studies showing lineages within Sarcophagidae (Piwczyński et al ., 2014; Piwczyński et al ., 2017; Buenaventura & Pape, 2017a; Buenaventura et al ., 2019) and Tachinidae (Cerretti et al ., 2014b; Stireman et al ., 2019) as the dominant fast‐evolving groups of Oestroidea. Furthermore, our results support a super‐radiation within the genus Sarcophaga Meigen (Sarcophagidae), as recent studies suggest (Piwczyński et al ., 2014; Buenaventura et al ., 2017; Buenaventura & Pape, 2017a; Buenaventura et al ., 2019).…”

“…Our results are concordant with studies showing lineages within Sarcophagidae (Piwczyński et al ., 2014; Piwczyński et al ., 2017; Buenaventura & Pape, 2017a; Buenaventura et al ., 2019) and Tachinidae (Cerretti et al ., 2014b; Stireman et al ., 2019) as the dominant fast‐evolving groups of Oestroidea. Furthermore, our results support a super‐radiation within the genus Sarcophaga Meigen (Sarcophagidae), as recent studies suggest (Piwczyński et al ., 2014; Buenaventura et al ., 2017; Buenaventura & Pape, 2017a; Buenaventura et al ., 2019). This super‐radiation can be recognized by the presence of many short branches at the level of the subgeneric diversification, which is accompanied by lower BS and LPP in comparison with the rest of the tree nodes (Figs.…”

“…universal) probes and should aid in locus recovery (Branstetter et al ., 2017; Gustafson et al ., 2019a; Gustafson et al ., 2019b; Kulkarni et al ., 2020). Previous molecular studies on Oestroidea (Kutty et al ., 2010; Buenaventura et al ., 2017; Buenaventura & Pape, 2017a; Buenaventura et al ., 2019) and similar radiations predict that reconstructing a strong phylogeny would require a large increase in molecular data (Dell'Ampio et al ., 2014; Giarla & Esselstyn, 2015) and the combination of information from multiple genome regions to attempt to produce accurate species tree estimates (Degnan & Rosenberg, 2009). A unique tailored UCE probe set for Calyptratae and Oestroidea flies could increase locus recovery, whereas a generalized UCE probe set designed for the entire order like the Diptera‐wide UCE probe set (Faircloth, 2017) would capture a smaller and perhaps an insufficient number of loci to reconstruct this rapid radiation.…”

“…Tachinidae includes mostly parasitoids playing significant roles in regulating their host populations, and hence being relevant for biological control programmes (Stireman et al ., 2006). During the last decade, several studies have explored the phylogenetic relationships of Oestroidea (Marinho et al ., 2012; Singh & Wells, 2013; Zhang et al ., 2016a; Cerretti et al ., 2017; Michelsen & Pape, 2017; Buenaventura et al ., 2019; Cerretti et al ., 2019; Kutty et al ., 2019); however, our knowledge about their evolution and diversity patterns remains limited, especially with regard to Calliphoridae. The most limiting factor has been the identification and screening of orthologous loci across an evolutionarily distant set of taxa, which when compared in phylogenetic analyses, recover poorly supported relationships of the important major lineages.…”

“…DNA aliquots may face the same constraints of using suboptimally preserved samples like museum specimens. To date, only a few studies using anchored hybrid enrichment (AHE) or ultraconserved elements (UCE) have capitalized on museum specimens, but not on legacy DNA aliquots (Faircloth et al ., 2013; McCormack et al ., 2016; Blaimer et al ., 2016b; Baca et al ., 2017; Wood et al ., 2018; Derkarabetian et al ., 2019), although with few exceptions (Buenaventura et al ., 2019).…”