Episodic radiations in the fly tree of life

Brian M. Wiegmann1,2, Michelle Trautwein2,3, Isaac S. Winkler2,3, Norman B. Barr4,2, Jungwook Kim2,3, Christine L. Lambkin5,6,7, Matthew A. Bertone2,3, Brian K. Cassel2,3, Keith M. Bayless2,3, Alysha M. Heimberg8, Benjamin M. Wheeler9, Kevin J. Peterson8, Thomas Pape10, Bradley J. Sinclair11, Jeffrey H. Skevington12, Vladimir Blagoderov13, Jason Caravas14, Sujatha Narayanan Kutty15,16, Urs Schmidt‐Ott17, Gail E. Kampmeier18, F. Christian Thompson19, David A. Grimaldi20, Andrew T. Beckenbach21, Gregory W. Courtney22, Markus Friedrich14, Rudolf Meier15,23, David K. Yeates5,6
1Department of Entomology, North Carolina State University, Raleigh, NC 27695, USA
2Departments of aEntomology and
3North Carolina State University ,
4Center for Plant Health Science and Technology, Mission Laboratory, US Department of Agriculture-Animal and Plant Health Inspection Service, Moore Air Base, Edinburg, TX 78541;
5CSIRO,
6Commonwealth Scientific and Industrial Research Organization Entomology, Canberra, ACT 2601, Australia
7Queensland Museum, South Bank, Brisbane, Queensland 4101, Australia;
8Department of Biological Sciences, Dartmouth College, Hanover, NH 03755.
9Computer Science, North Carolina State University, Raleigh, NC 27695;
10Natural History Museum of Denmark, University of Copenhagen, 2100 Copenhagen Ø, Denmark;
11Canadian National Collection of Insects, Ottawa Plant Laboratory-Entomology, Canadian Food Inspection Agency, Ottawa, ON, Canada K1A 0C6;
12Invertebrate Biodiversity, Agriculture and Agri-Food Canada, Ottawa, ON, Canada K1A 0C6;
13Department of Entomology, Natural History Museum, London SW7 5BD, United Kingdom
14Department of Biological Sciences, Wayne State University, Detroit, MI 48202;
15‡Department of Biological Sciences and
16National University of Singapore;
17Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637;
18Illinois Natural History Survey, Institute of Natural Resource Sustainability, University of Illinois, Champaign, IL 61820;
19Department of Entomology, Smithsonian Institution, Washington, DC 20560;
20American Museum of Natural History, New York, NY 10024-5192;
21Department of Biological Sciences, Simon Fraser University, Burnaby, BC, Canada, V5A 1S6
22Department of Entomology, Iowa State University, Ames, IA 50011; and
23University Scholars Programme, National University of Singapore, Singapore 117543, Singapore;

Tóm tắt

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 domesticahouse fly), their role as pests (Anopheles gambiaemalaria 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.

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