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Open Access Highly Accessed Research article

Toward reconstructing the evolution of advanced moths and butterflies (Lepidoptera: Ditrysia): an initial molecular study

Jerome C Regier1, Andreas Zwick1, Michael P Cummings3, Akito Y Kawahara2, Soowon Cho24, Susan Weller5, Amanda Roe56, Joaquin Baixeras7, John W Brown8, Cynthia Parr9, Donald R Davis10, Marc Epstein11, Winifred Hallwachs12, Axel Hausmann13, Daniel H Janzen12, Ian J Kitching14, M Alma Solis8, Shen-Horn Yen15, Adam L Bazinet3 and Charles Mitter2*

Author Affiliations

1 Center for Biosystems Research, University of Maryland Biotechnology Institute, College Park, Maryland 20742, USA

2 Department of Entomology, University of Maryland, College Park, Maryland 20742, USA

3 Laboratory of Molecular Evolution, Center for Bioinformatics and Computational Biology, University of Maryland, College Park, Maryland 20742, USA

4 Department of Plant Medicine, Chungbuk National University, Cheongju 361-763, Korea

5 Department of Entomology, University of Minnesota, St. Paul, Minnesota 55455, USA

6 Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada

7 Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, Apartat de correus 2085, 46071 Valencia, Spain

8 Systematic Entomology Laboratory, Agricultural Research Service, United States Department of Agriculture, Beltsville, Maryland 20705, USA

9 Encyclopedia of Life, Smithsonian Institution, Washington, D.C. 20013-7012, USA

10 Department of Entomology, Smithsonian Institution, Washington, D.C. 20013-7012, USA

11 Plant Pest Diagnostics Branch, California Department of Food and Agriculture, 3294 Meadowview Road, Sacramento, California 95832-1448, USA

12 Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA

13 Bavarian State Collection of Zoology, Münchhausenstrasse 21, D-81247 München, Germany

14 Department of Entomology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK

15 Department of Biological Sciences, National Sun Yat-Sen University, Kaohsiung 804, Taiwan

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BMC Evolutionary Biology 2009, 9:280  doi:10.1186/1471-2148-9-280

Published: 2 December 2009

Abstract

Background

In the mega-diverse insect order Lepidoptera (butterflies and moths; 165,000 described species), deeper relationships are little understood within the clade Ditrysia, to which 98% of the species belong. To begin addressing this problem, we tested the ability of five protein-coding nuclear genes (6.7 kb total), and character subsets therein, to resolve relationships among 123 species representing 27 (of 33) superfamilies and 55 (of 100) families of Ditrysia under maximum likelihood analysis.

Results

Our trees show broad concordance with previous morphological hypotheses of ditrysian phylogeny, although most relationships among superfamilies are weakly supported. There are also notable surprises, such as a consistently closer relationship of Pyraloidea than of butterflies to most Macrolepidoptera. Monophyly is significantly rejected by one or more character sets for the putative clades Macrolepidoptera as currently defined (P < 0.05) and Macrolepidoptera excluding Noctuoidea and Bombycoidea sensu lato (P ≤ 0.005), and nearly so for the superfamily Drepanoidea as currently defined (P < 0.08). Superfamilies are typically recovered or nearly so, but usually without strong support. Relationships within superfamilies and families, however, are often robustly resolved. We provide some of the first strong molecular evidence on deeper splits within Pyraloidea, Tortricoidea, Geometroidea, Noctuoidea and others.

Separate analyses of mostly synonymous versus non-synonymous character sets revealed notable differences (though not strong conflict), including a marked influence of compositional heterogeneity on apparent signal in the third codon position (nt3). As available model partitioning methods cannot correct for this variation, we assessed overall phylogeny resolution through separate examination of trees from each character set. Exploration of "tree space" with GARLI, using grid computing, showed that hundreds of searches are typically needed to find the best-feasible phylogeny estimate for these data.

Conclusion

Our results (a) corroborate the broad outlines of the current working phylogenetic hypothesis for Ditrysia, (b) demonstrate that some prominent features of that hypothesis, including the position of the butterflies, need revision, and (c) resolve the majority of family and subfamily relationships within superfamilies as thus far sampled. Much further gene and taxon sampling will be needed, however, to strongly resolve individual deeper nodes.