Radiações episódicas na árvore da vida das moscas

Episodic radiations in the fly tree of life

Brian M. Wiegmann a,1, Michelle D. Trautwein a, Isaac S. Winkler a, Norman B. Barr a,b, Jung-Wook Kim a, Christine Lambkin c,d, Matthew A. Bertone a, Brian K. Cassel a, Keith M. Bayless a, Alysha M. Heimberg e, Benjamin M. Wheeler f, Kevin J. Peterson e, Thomas Pape g, Bradley J. Sinclair h, Jeffrey H. Skevington i, Vladimir Blagoderov j, Jason Caravas k, Sujatha Narayanan Kutty l, Urs Schmidt-Ott m, Gail E. Kampmeier n, F. Christian Thompson o, David A. Grimaldi p, Andrew T. Beckenbach q, Gregory W. Courtney r, Markus Friedrich k, Rudolf Meier l,s, and David K. Yeates d

Author Affiliations

Departments of aEntomology and

fComputer Science, North Carolina State University, Raleigh, NC 27695;

bCenter for Plant Health Science and Technology, Mission Laboratory, US Department of Agriculture-Animal and Plant Health Inspection Service, Moore Air Base, Edinburg, TX 78541;

cQueensland Museum, South Bank, Brisbane, Queensland 4101, Australia;

eDepartment of Biological Sciences, Dartmouth College, Hanover, NH 03755;

gNatural History Museum of Denmark, University of Copenhagen, 2100 Copenhagen Ø, Denmark;

hCanadian National Collection of Insects, Ottawa Plant Laboratory-Entomology, Canadian Food Inspection Agency, Ottawa, ON, Canada K1A 0C6;

iInvertebrate Biodiversity, Agriculture and Agri-Food Canada, Ottawa, ON, Canada K1A 0C6;

jDepartment of Entomology, Natural History Museum, London SW7 5BD, United Kingdom;

kDepartment of Biological Sciences, Wayne State University, Detroit, MI 48202;

lDepartment of Biological Sciences and

sUniversity Scholars Programme, National University of Singapore, Singapore 117543, Singapore;

mDepartment of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637;

nIllinois Natural History Survey, Institute of Natural Resource Sustainability, University of Illinois, Champaign, IL 61820;

oDepartment of Entomology, Smithsonian Institution, Washington, DC 20560;

pAmerican Museum of Natural History, New York, NY 10024-5192;

qDepartment of Biological Sciences, Simon Fraser University, Burnaby, BC, Canada V5A 1S6;

rDepartment of Entomology, Iowa State University, Ames, IA 50011; and

dCommonwealth Scientific and Industrial Research Organization Entomology, Canberra, ACT 2601, Australia

Edited by David M. Hillis, University of Texas, Austin, TX, and approved February 10, 2011 (received for review August 26, 2010)

Abstract

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 domestica house fly), their role as pests (Anopheles gambiae malaria 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.

molecular systematics, phylogenetics, Insecta, adaptive radiation

Footnotes

1To whom correspondence should be addressed. 

E-mail:bwiegman@unity.ncsu.edu.

Author contributions: B.M.W., K.J.P., T.P., G.W.C., M.F., R.M., and D.K.Y. designed research; B.M.W., M.D.T., I.S.W., N.B.B., J.-W.K., C.L., M.A.B., B.K.C., K.M.B., A.M.H., B.M.W., T.P., B.J.S., J.H.S., V.B., J.C., S.N.K., U.S.-O., G.E.K., F.C.T., D.A.G., A.T.B., G.W.C., M.F., R.M., and D.K.Y. performed research; B.M.W., M.D.T., I.S.W., and C.L. analyzed data; B.M.W., M.D.T., I.S.W., and D.K.Y. wrote the paper; and G.E.K. and F.C.T. maintained and developed databases and bioinformatics.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

Database deposition: The sequences reported in this paper have been deposited in the GenBank database. For a list of accession numbers, see Table S1.

This article contains supporting information online at

www.pnas.org/lookup/suppl/doi:10.1073/pnas.1012675108/-/DCSupplemental.

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