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ISSN 0044-5088 Zoologica Original Contributions to Zoology, founded in 1888 Ed. H.F. Paulus, Vienna Volume 161 John D. Plant & Hannes F. Paulus Evolution and Phylogeny of Bees Review and Cladistic Analysis in Light of Morphological Evidence (Hymenoptera, Apoidea) E Schweizerbart Science Publishers Zoologica Original Contributions to Zoology Founded 1888 by R. Leuckart, C. Chun, continued by W. Kükenthal, R. Hesse, W.E. Ankel Edited by Hannes F. Paulus Volume 161 John D. Plant and Hannes F. Paulus Evolution and Phylogeny of Bees: Review and Cladistic Analysis in Light of Morphological Evidence (Hymenoptera, Apoidea) with 232 figures and 49 tables sample pages Schweizerbart Science Publishers Stuttgart • 2016 John D. Plant and Hannes F. Paulus: Evolution and Phylogeny of Bees: Review and Cladistic Analysis in Light of Morphological Evidence (Hymenoptera, Apoidea) Authors’ addresses: Dr. John D. Plant (corresponding author), Department of Evolutionary Biology, University of Vienna, Althanstraße 14, A-1090 Vienna, Austria; [email protected] Hannes F. Paulus, Department of Integrative Zoology, University of Vienna, Austria; present address: Department of Integrative Zoology, Althanstr. 14, A-1090 Wien; [email protected] We would be pleased to receive your comments on the content of this book: [email protected] Front cover: Stenotritus greavesi (Stenotritidae) female, Western Australia (photo: J. Plant) Phylogenetic tree of bees, modified after WARNCKE (1977a) Cretotrigona prisca, a fossil Apidae found in New Jersey amber (GRIMALDI 1999) honeycomb structure: © cepolina.com This publication has been made possible with the generous support of the ROFA Company, Kritzendorf/Vienna, Austria. ISBN 978-3-510-55048-7 ISSN 0044-5088 Information on this title: www.schweizerbart.com/9783510550487 © 2016 E. Schweizerbart’sche Verlagsbuchhandlung (Nägele u. Obermiller), Stuttgart, Germany All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical photocopying, recording, or otherwise, without the prior written permission of E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart Publisher: E. Schweizerbart’sche Verlagsbuchhandlung (Nägele u. Obermiller) Johannesstraße 3A, 70176 Stuttgart, Germany [email protected] www.schweizerbart.dsamplee pages ∞ Printed on permanent paper conforming to ISO 9706-1994 Typesetting: Satzpunkt Ursula Ewert GmbH, Bayreuth Printed in Germany by DDD Digitaldruck Deutschland, Aalen Contents Evolution and Phylogeny of Bees: A Review and a Cladistic Analysis in Light of Morphological Evidence (Hymenoptera, Apoidea) Abstract . 1 Zusammenfassung . 2 Results and Discussion . 143 Statistical Results and Cladograms . 143 Part I: A Preamble to the Evolution and Phylogeny Major Divisions of Bees . 174 of Bees . 4 Short-Tongued Bees . 175 Introduction . 4 Family Halictidae . 177 Trends in Bee Classififi cation . 7 Family Andrenidae . 187 Th eories on the Evolution of Bees . 16 Family Stenotritidae . 201 Wasp Ancestry and Bee Classifification . 35 Family Colletidae . 202 Morphological Phylogeny of Bees . 50 Family Melittidae . 218 Molecular Phylogeny of Bees . 66 Long-Tongued Bees . 229 Parasitic Bees . 78 Family Megachilidae . 231 Antiquity of Bees . 78 Family Apidae . 244 Part II: A Phylogenetic Study of Bees in Light of Summary . 317 Morphological Evidence . 99 Acknowledgements . 327 Introduction . 99 References . 327 Methods . 99 Appendix A: Species Investigated . 108 Family-Group Names of Bees . 359 List of Characters . 108 Appendix B: Data Matrix . 143 Description of New Family-Group Names . 362 sample pages Zoologica Vol. 161, 1–368 Stuttgart, January 2016 Evolution and Phylogeny of Bees: A Review and a Cladistic Analysis in Light of Morphological Evidence (Hymenoptera, Apoidea) by John D. Plant and Hannes F. Paulus With 232 figures and 52 tables Abstract The higher phylogeny of bees (=Apiformes, Anthophila) has yet to be satisfactorily resolved despite several broad-based stud- ies utilizing morphological or molecular data. One the two previous comprehensive studies using morphological data centered on the long-tongued bees (Roig-Alsina & Michener 1993) and the other on the short-tongued bees (Alexander & Michener 1995). The present study thus represents the first extensive cladistic analysis utilizing morphological characters that considers bees as a whole. Molecular studies have pro- duced results that are in many aspects incongruent with morphological based phylogenies. Several vexing aspects of bee phylogeny are addressed in this study; for example, the relationships of the basal groups to each other, the position of the Stenotritidae and Oxaeidae, the relationships within the Colletidae and Apidae, the monophyletic status of the Melittidae, the relationships of several problematic and phylogenetically isolated taxa, i.e. Ancyla, Ctenoplectra, Tarsalia, and Pararhophites, as well as the placement of the many parasitic bees. In Part I, the history of classification, higher taxonomy and evolution of bees is recapitulated in a largely chronological man- ner. The overview cites relevant English and German language publications, as well as that of other languages beginning with Aristotle, Aldrovandi, the pre-Linnaeans and including the numerous and most recent molecular genetic analyses. Evolutionary hypotheses on the origin of bees and their key morphological and behavioral features are discussed in a historical context. The aim of Part II of the study is to examine the higher phylogeny of b ees using a fresh set of morphological characters in computer-assisted phylogenetic analyses. Specimens were selected from all families, subfamilies and most tribes of bees. Repre- sentatives from 55 genera of short-tongued bees were coded: Colletidae (12 genera), Stenotritidae (2), Halictidae (13), Oxaeidae (2), Andrenidae (12), and Melittidae (7); as well as representatives from 90 genera of long-tongued bees: Megachilidae (18) and Apidae (72). Of the investigated long-tongued bee genera, 26 are nest parasites on other bees. The majority of coded characters were morphological (212), and five were related to behavior or biology. Phylogenetic analyses were carried out using a variety of methods: parsimony, successive reweight, implied weight, Bayesian and neighbor-joining. The data sets were constructed of: (i) non-parasitic bees only, (ii) full data set and (iii) combinations of parasitic and non-parasitic taxa. Character support for sub-ter- minal nodes is discussed. The sister group to bees belongs within the spheciform Apoidea (= Sphec iformes, apoid wasps), in particular, the Crabronidae or a part of them. Bees and spheciform wasps together make up the Apoidea. Two groups of spheciform wasps were chosen as outgroups for the cladistic analyses: the Pemphredoninae and Philanthinae. Both subfamilies were formerly placed in the Spheci- dae (e.g. Menke 1997), but according to more recent classification, they are members of Crabronidae (e.g. Melo 1999). The main findings and conclusions of this study are as follows: The monophyly of bees as a whole was supported. Two major clades arose: (i) the basic families of short-tongued bees (sensu Alexander & Michener 1995) (Oxaeidae + (Halictidae + (Andrenidae + (Stenotritidae + Colletidae)))) and (ii) the clade (Melittidae + (Megachilidae + Apidae)). Based on the results of all analyses, except some neighbor-joining, the Stenotritidae consistently occurred at the base of the Colletidae. The stenotritidssample are retained as a family. The Colletidae encompasses pages the two subfamilies: Colletinae and Diphaglossi- nae. The Colletinae is split into several tribes: Hylaeini, Euryglossini, Xeromelissini, Paracolletini, Scraptrini, Lonchopriini, as well as the following new tribes: Trichocolletini, Leioproctini and Callomelittini. The Colletidae is no longer regarded as the most ancestral family of present-day bees. The bilobed nature of the colletid glossa is re-interpreted as an apomorphic feature; it differs from the hooded glossa of the outgroup Pemphredoninae and the bilobed glossa of outgroup Philanthinae (both Crabronidae). © 2016 E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart, Germany www.schweizerbart.de 0044-5088/16-0161 $ 165.60 2 John D. Plant and Hannes F. Paulus The Oxaeidae was recovered as a family at the base of the core short-tongued bees in the parsimony and successive weight analyses. However, the hypothesis that the oxaeids are a subfamily of the Andrenidae was supported in the implied weight and Bayesian analyses, as well as in a separate analysis designed to explore the relationships of the Andrenidae; this is the preferred phylogeny. The monophyly of the Melittidae was supported by several characters; it is not necessary to split the melittids into three families, as carried out by some morphological and molecular studies (Roig-Alsina & Michener 1993, Danforth, Fang & Sipes 2006, Danforth et al. 2006, Michez, Patiny & Danforth 2009). The Apidae was separated into the three conventional subfamilies: Xylocopinae, Nomadinae and Apinae. The latter was segregated into three major lineages, the Eucerine-line, Anthophorine-line and Apine-line. The tribes of the Eucerine-line include Exomalopsini, Ancylini, Emphorini, Tapinotaspidini, Tarsaliini (new tribe) and Eucerini. The Anthophorine-line consists of An- thophorini, Melectini and possibly Ctenoplectrini. The Apine-line contains several non-corbiculate tribes: Tetrapediini, Centri- dini, Rhathymini
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