Beyond Drosophila: resolving the rapid radiation of schizophoran flies with phylotranscriptomics.

Affiliation

Bayless KM(#)(1)(2)(3), Trautwein MD(#)(4), Meusemann K(5)(6)(7), Shin S(8)(9), Petersen M(10), Donath A(6), Podsiadlowski L(6), Mayer C(6), Niehuis O(7), Peters RS(11), Meier R(12)(13), Kutty SN(12)(14), Liu S(15), Zhou X(15), Misof B(16), Yeates DK(5), Wiegmann BM(8).
Author information:
(1)Australian National Insect Collection, CSIRO National Research Collections Australia
(NRCA), Acton, Canberra, ACT, Australia. [Email]
(2)Department of Entomology, California Academy of Sciences, San Francisco, CA, USA. [Email]
(3)Department of Entomology & Plant Pathology, North Carolina State University, Raleigh, NC, USA. [Email]
(4)Department of Entomology, California Academy of Sciences, San Francisco, CA, USA.
(5)Australian National Insect Collection, CSIRO National Research Collections Australia
(NRCA), Acton, Canberra, ACT, Australia.
(6)Centre for Molecular Biodiversity Research
(ZMB), Zoologisches Forschungsmuseum Alexander Koenig
(ZFMK), Bonn, Germany.
(7)Department of Evolutionary Biology & Ecology, Institute of Biology I, Albert Ludwig University of Freiburg, Hauptstraße 1, Freiburg i. Br., Germany.
(8)Department of Entomology & Plant Pathology, North Carolina State University, Raleigh, NC, USA.
(9)School of Biological Sciences, Seoul National University, Seoul, Republic of Korea.
(10)Max-Planck-Institut of Immunobiology and Epigenetics, Freiburg, Germany.
(11)Centre of Taxonomy and Evolutionary Research, Arthropoda Department, Zoological Research Museum Alexander Koenig, Bonn, Germany.
(12)Department of Biological Sciences, National University of Singapore, Singapore, Singapore.
(13)Lee Kong Chian Natural History Museum, National University of Singapore, Singapore, Singapore.
(14)Tropical Marine Science Institute, National University of Singapore, Singapore, Singapore.
(15)Department of Entomology, China Agricultural University, Beijing, People's Republic of China.
(16)Zoological Research Museum Alexander Koenig
(ZFMK), Bonn, Germany.
(#)Contributed equally

Abstract

BACKGROUND: The most species-rich radiation of animal life in the 66 million years following the Cretaceous extinction event is that of schizophoran flies: a third of fly diversity including Drosophila fruit fly model organisms, house flies, forensic blow flies, agricultural pest flies, and many other well and poorly known true flies. Rapid diversification has hindered previous attempts to elucidate the phylogenetic relationships among major schizophoran clades. A robust phylogenetic hypothesis for the major lineages containing these 55,000 described species would be critical to understand the processes that contributed to the diversity of these flies. We use protein encoding sequence data from transcriptomes, including 3145 genes from 70 species, representing all superfamilies, to improve the resolution of this previously intractable phylogenetic challenge. RESULTS: Our results support a paraphyletic acalyptrate grade including a monophyletic Calyptratae and the monophyly of half of the acalyptrate superfamilies. The primary branching framework of Schizophora is well supported for the first time, revealing the primarily parasitic Pipunculidae and Sciomyzoidea stat. rev. as successive sister groups to the remaining Schizophora. Ephydroidea, Drosophila's superfamily, is the sister group of Calyptratae. Sphaeroceroidea has modest support as the sister to all non-sciomyzoid Schizophora. We define two novel lineages corroborated by morphological traits, the 'Modified Oviscapt Clade' containing Tephritoidea, Nerioidea, and other families, and the 'Cleft Pedicel Clade' containing Calyptratae, Ephydroidea, and other families. Support values remain low among a challenging subset of lineages, including Diopsidae. The placement of these families remained uncertain in both concatenated maximum likelihood and multispecies coalescent approaches. Rogue taxon removal was effective in increasing support values compared with strategies that maximise gene coverage or minimise missing data. CONCLUSIONS: Dividing most acalyptrate fly groups into four major lineages is supported consistently across analyses. Understanding the fundamental branching patterns of schizophoran flies provides a foundation for future comparative research on the genetics, ecology, and biocontrol.