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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

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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]

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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

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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 studies 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 produced 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 manner. 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-terminal nodes is discussed. The sister group to bees belongs within the spheciform Apoidea (= Spheciformes, 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).

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 and Ericrocidini, in addition to the corbiculate tribes: Euglossini, Bombini, Apini and Meliponini. The genera Ancylaa and Ctenoplectraa were found to be nested within the long-tongued bees. Their short proboscides are argued to be adaptations acquired in connection with visitation to flowers in which a relatively short and flexible glossa is required. Their mouthparts thus only secondarily resemble plesiomorphic conditions. Nomadinae was the sister-group to Apinae. The investigated parasitic tribes of Apinae (Melectini, Ericrocidini, Isepeolini, Osirini, Rhathymini) grouped together in the parsimony analysis forming a large clade of parasitic tribes (i.e. Melectine-line), as in many molecular analyses. To test the behavior of the data set, each parasitic tribe was subjected to an individual analysis exclud- ing other parasitic groups. The results of the separate analyses were combined into a composite cladogram, which showed that the tribes were largely segregated: Isepeolini and Osirini formed a polytomy at the base of the Apinae; Melectini was retrieved adjacent its host taxa (Anthophorini), likewise Rhathymini and Ericrocidini were aligned with their host taxa (Centridini). The relationships among the corbiculate Apinae (Euglossini + (Bombini + (Apini + Meliponini))) uphold recent results from other studies based on morphological data; however, not those based on molecular data. Due the division of bees into two major clades, (i) the basic families of short-tongued bees (Halictidae, Colletidae and An- drenidae including Oxaeinae) and (ii) the Melittidae plus the long-tongued bees (Megachilidae and Apidae), no single family can be designated as the most ancestral.

Key words: phylogeny of Apoidea, molecular versus morphological trees, theories of bee evolution, cladistics

Zusammenfassung Evolution und Phylogenie der Bienen: Ein Review und eine kladistische An alyse in Hinblick morphologischer Evidenz. Die höhere Phylogenie der Bienen (= Apiformes, Anthophila) ist bislang noch nicht zufriedenstellend gelöst worden, trotz mehrerer breit angelegter Studien, in denen morphologische und molekulare Daten verendet wurden. Von den zwei umfassendsten Studien über die Bienen-Phylogenie auf der Grundlage morphologischer Daten war eine auf die langrüsseligen Bienen (Roig-Alsina & Michener 1993) und die andere auf die kurzrüsseligen Bienen (Alexander & Miche- ner 1995) fokussiert. Die vorliegende Studie stellt somit die erste umfangreiche kladistische Analyse der Bienen als Ganzes anhand morphologischer Merkmale dar. Molekulare Untersuchungen haben Ergebnisse geliefert, die in vielen Aspekten jedoch mit den morphologisch-basierten Phylogenien nicht immer übereinstimmen. Mehrere problematische Aspekte der Bienen-Phylogenie werden in dieser Studie berücksichtigt; zum Beispiel, die Beziehun- gen der basalen Gruppen zueinander, die Stellung der Stenotritidae und Oxaeidae im Stammbaum, die Verwandschaftsbeziehun- gen innerhalb der Colletidae und Apidae, der monophyletische Status der Melittidae, die Verhältnisse von problematischen und phylogenetisch isolierten Taxa (Ancyla, Ctenoplectra, Tarsaliaa und Pararhophitess), sowie die Stellung vieler parasitären Bienen. In Teil I wird die Geschichte der Klassifikation, der höheren Taxonomie und der Evolution der Bienen wird in einer weitge- hend chronologischen Weise rekapituliert. Der Überblick umfasst relevante englische und deutsche Veröffentlichungen, sowie jene anderer Sprachen, beginnend mit Aristoteles, über Aldrovandi und die Prä-Linnaener bis hin zu den zahlreichen neuesten molekularen genetischen Analysen. Evolutionshypothesen über den Ursprung der Bienen und deren Schlüsseleigenschaften in Mor- phologie und Verhaltensample werden in einem historischen Zusammenhang besprochenpages. Das Ziel von Teil II der Studie ist, die höhere Phylogenie der Bienen mit einem frischen Satz morphologischer Merkmale in Computer-unterstützten Analysen neu zu bearbeiten. Bienenarten aller Familien, Unterfamilien und fast aller Tribes wurden für die Untersuchungen ausgewählt. Vertreter aus 55 Gattungen kurzrüsseliger Bienen wurden kodiert: Colletidae (12 Gattungen), Stenotritidae (2), Halictidae (13), Oxaeidae (2), Andrenidae (12) und Melittidae (7); sowie Vertreter aus 90 Gattungen langrüsse- liger Bienen: Megachilidae (18) und Apidae (72). Von den kodierten langrüsseligen Bienen sind 26 Gattungen Nestparasiten anderer Bienen. Neben den 212 morphologischen Merkmalen wurden auch fünf biologische bzw. ethologische Merkmale für die Analyse kodiert. Kladistische Analysen wurden unter Verwendung einer Vielzahl von Methoden durchgeführt: „parsimony“, „successive reweight“, „implied reweight“, „Bayesian“ und „neighbor-joining“. Folgende Datensätze wurden analysiert: (i) der Evolution and Phylogeny of Bees 3

vollständige Datensatz, (ii) ein Subset mit allen nicht-parasitären Bienen, und (iii) Kombinationen von parasitären und nicht- parasitären Taxa. Die Merkmalunterstützung für die jeweils entstandenen Klade wird diskutiert. Die Schwestergruppe der Bienen liegt innerhalb der Gruppe der Grabwespen (= Spheciformes, apoid Wespen) insbesondere gilt die Familie der Crabronidae oder ein Teil von ihnen als mögliche Schwestergruppe. Bienen und Grabwespen zusammen bilden die Überfamilie der Apoidea. Zwei Gruppen der Grabwespen wurden für die kladistischen Analysen als Außengruppen gewählt: die Pemphredoninae und die Philanthinae. Beide Unterfamilien wurden früher zur Familie Sphecidae (z. B. Menke 1997) gestellt, aber entsprechend neuerer Klassifikationen gehören sie jetzt zur Familie Crabronidae (z. B. Melo 1999). Die wichtigsten Ergebnisse und Schlussfolgerungen in dieser Studien sind wie folgt: Die Monophylie der Bienen als eine einheitliche phylogenetische Gruppe wurde bestätigt. Man kann zwei große Klades gut unterscheiden, (i) die Kern-kurzrüsseligen Bienen (Oxaeidae + (Halictidae + (Andrenidae + (Stenotritidae + Colletidae)))) und (ii) die Klade Melittidae plus alle langrüsseligen Bienen (Megachilidae + Apidae). In allen Analysen (mit Ausnahme einiger „neighbor-joining“ Tests) wurde die Familie Stenotritidae als Schwestergruppe der Colletidae positioniert, und wird in dieser Studie als eine eigene Familie betrachtet. Die Colletidae umfassen zwei Unterfamilien: Colletinae und Diphaglossinae; während die Colletinae beinhaltet die Hylaeini, Euryglossini, Xeromelissini, Paracolletini, Scrap- trini, Lonchopriini, sowie die folgenden neuen Tribes: Trichocolletini, Leioproctini und Callomelittini. Die Colletidae werden nicht mehr als die basalste Gruppe der heutigen Bienen betrachtet. Die zweilappige Glossa der Colletidae wird als ein apomorphes Merkmal neu interpretiert; sie unterscheidet sich deutlich von der Hauben-Glossa der Pemphredoninae und der zweilappigen Glossa der Philanthinae, beides Unterfamilien der Crabronidae. Aufgrund der „parsimony“ und „successive reweight“ Analysen können die Oxaeidae als Schwestergruppe der „basic“-kurz- rüsseligen Bienen betrachtet werden. Jedoch deuten die „implied reweight“ und „Bayesian“ Analysen darauf hin, dass die Oxaei- dae auch als eine Unterfamilie der Andrenidae aufgefasst werden könnten. Letztere Hypothese wird in der vorliegenden Studie als die plausiblere Phylogenie bewertet. Die Monophylie der Melittidae wird durch mehrere Merkmale unterstützt. Folglich es ist nicht nötig, die Melittidae in drei Familien zu spalten, wie dies in einigen morphologischen und molekularen Studien bislang geschehen ist (Roig-Alsina & Michener 1993, Danforth, Fang & Sipes 2006, Danforth et al. 2006, Michez, Patiny & Danforth (2009). Die Apidae werden in die drei traditionellen Unterfamilien untergeteilt: Xylocopinae, Nomadinae und Apinae. Die Unterfa- milie Apinae wurde in drei große Linien, die Eucerine-Linie, Anthophorine-Linie und Apine-Linie getrennt. Zu der Tribes des Eucerine-Linie gehören Exomalopsini, Ancylini, Emphorini, Tapinotaspidini, Tarsaliini (neuer Tribus) und Eucerini. Die Antho- phorine-Linie besteht aus Anthophorini, Melectini und möglicherweise auch Ctenoplectrini. Die Apine-Linie enthält die nicht- corbiculaten Tribes: Tetrapediini, Centridini, Rhathymini und Ericrocidini, zusätzlich zu den corbiculaten Tribes: Euglossini, Bombini, Apini und Meliponini. Die Gattungen Ancylaa und Ctenoplectraa gehören zu den langrüsseligen Bienen. Ihre kurzen Mundwerkzeuge sind wahrschein- lich Anpassungen an Blüten, wobei eine flexible Zunge von Vorteil ist, und diese daher nur plesiomorphischen Zuständen ähnelt. Die Nomadinae bilden die Schwestergruppe der Apinae. Die untersuchten parasitischen Tribes der Apinae (Melectini, Ericro- cidini, Isepeolini, Osirini, Rhathymini) wurden in der Parsimonieanalyse zusammen gruppiert und bildeten – wie in vielen molekularen Analysen – ein großes Klade (die Melectine-Line). Um das Verhalten der Datei zu prüfen, wurde jeder parasitischen Tribus einzeln unter Ausschluss aller übrigen parasitischen Gruppen analysiert. Die Ergebnisse der einzelnen Analysen wur den schließlich in einem zusammengesetzten Cladogram kombiniert, welches zeigte, dass die parasitischen Tribes mehrheitlich voneinander getrennt sind. Die Beziehungen zwischen den corbiculaten Apinae (Euglossini + (Bombini + (Apini + Meliponini))) bestätigen die Ergeb- nisse aus Studien, die auf morphologischen Daten, aber nicht aus Studien, die auf molekularen Daten beruhen. Durch die Aufteilung der Bienen in zwei große Klades: (i) die „basic“-kurzrüsseligen Bienen (Halictidae, Colletidae und Andrenidae einschließlich Oxaeinae) und (ii) die Melittidae plus alle langrüsseligen Bienen (Megachilidae und Apidae), kann keine der rezenten sampleFamilien als basalste innerhalb der Bienen bezeichnet wer den.pages Evolution and Phylogeny of Bees 9

Fig. 2: A. The first published drawing of an insect completed with the aid of the microscope was the Italian honeybee (Stel- luti 1625). B. The second published drawing of a bee completed with the aid of a microscope (Stelluti 1630).

like a lion’s mane, that the eyes are hairy…” The five The works of Cesi and Stelluti fell quickly into “tongues” refer to the outstretched mouthparts com- obscurity and were unknown or seldom accessible to posed of the glossa, the paired galeae and labial palpi. subsequent bee researchers due to the rarity and lim- Five years later, Stelluti (1630) produced an- ited number of copies. Today, only three copies exist other similar plate illustrating the honeybee based of the Apiarium and two of the Melissographiaa (Kid- again on his observations with an early microscope well 1970). Furthermore, the scientific value of the (Fig. 2 B). Both works admirably portray a trigon of Apiarium and Melissographiaa was brushed aside with honeybees and minute details of its external anato- the assertion that the works were simply an attempt my, the head and proboscis, antenna, hindlegs, the to exercise political influence on Pope Urban VIII sting, an eye and hairs. (Bignami 2000, Freedberg 2002). A keen observer might notice, however, that the Cesi sought to classify bees in consideration of mandibles cannotsample anatomically close like thongs as various descriptionspages found in the works of Aristotle, shown in the 1630 plate and that the basitarsus of Pliny, Albertus Magnus, Ulisse Aldrovandi and oth- the hind leg is disproportionally larger than the tibia. ers. The wasps were removed entirely, since they pro- Especially in the lateral view of honeybee in the 1630 duce no honey, but the tradition of distinguishing edition, there are almost no differences between the between the social (=civil) and solitary was retained three pairs of legs, as if the fore and middle legs were in his classification (Fig. 3). The sylvestress included merely copies of the hindleg. The 1625 edition is the bumblebees, as well as the newly discovered thus superior to the later version in several respects. stingless bees from Mexico. The solitary bees men- 10 John D. Plant and Hannes F. Paulus

Fig. 3: Classification of bees, after Cesi (1625). Translation based on that of Kidwell (1970).

tioned under uruncui included some that bore into separated into the Bipenniaa (Diptera) and Quadri- hard wood to make their nests (perhaps species of penniaa (largely Hymenoptera). Further, the Quad- Hoplitiss or Xylocopa). ripennia was split into two groups: the social honey- John Ray. The classification of insects was sig- making species and the solitary species. The term nificantly advanced by Ray (1710). In his table of favificaa is interpreted to mean “comb-making” rather classification, insects with membranous wings were than “honey-making”, since it accounted also for the

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Fig. 4: C lassification of Hymenoptera, after Ray (1710). Evolution and Phylogeny of Bees 11

hornets and social wasps. The solitary species were Table 3: Classification of bees, after Réaumur (1740, 1742) divided into the bee-like, wasp-like, butterfly-like 1. Ordinary bees (Apiss) and those possessing an exposed ovipositor (Fig. 4). 2. Bumblebees (Bombuss) Ray apparently abandoned this artificial system 3. Wood nesters (carpenter bees, Xylocopa) when describing individual species in the text, since 4. Mason bees (megachilids) after mentioning the common honeybee, he listed 5. Leaf-cutters (megachilids) nearly twenty species of solitary bees under the name 6. Ground burrowers (various taxa) “Apes sylvestres””, which were followed by various spe- 7. Silk bees (Colletess) cies of Bombylius (= bumblebees) before turning to 8. Tapestry bees (Osmia papaveriss) the hornets (crabroness). René-Antoine Ferchault de Réaumur. The life of the honeybee has attracted the curiosity of natu- (other megachilids) and a tapestryy bee that uses pop- ralists since the birth of occidental science in Ancient py petals to line its brood cells. Réaumur’s classifica- Greek. Yet, our knowledge of the life habits of soli- tion of bees into eight groups was based on nest bio- tary bees remained poor and sporadic up to the mid- logy and corresponded to the chapter headings of his eighteenth century. Then came Réaumur carrying Memoirs, volumes 5 and 6 (Table 3). out his curious observations on bees in the garden of Carl von Linné. Linné also known as Caro- Charenton (to paraphrase Maeterlinck 1914). lus Linnaeus – according to the Latinization of his Réaumur devoted over 150 pages to the Burbons name – is famous for being the founder of the bino- and Abeilles solitaries (Fig. 5). He dared to get his mial system of assigning names to plants and ani- hands and knees dirty digging out the secrets to the mals, in which all specimens are identified by a ge- life history of bumblebees and a species of Colletes, nus and a species name. whose nests, he found were “made of silken mem- From the first to fifth edition off Systema Naturae brane” (Réaumur 1742). He closely observed the (1735, 1747), Linnaeus lumped all aculeate Hyme- workings of the carpenter bee (Xylocopa violacea), the noptera (except the ants) into the genus Apis. The mason bee (Megachile parietina), leaf-cutting bees genus was defined as having a simple caudal stinger and four wings (Cauda aculeo simplici, alaa 4). Ini- tially, Linnaeus subdivided Apis into four groups: Crabro (hornets), Vespa, Bombyliuss (bumblebees) and Apis (s. str.) (Fig. 6). He used this system of classification from the first to ninth edition off Systema Naturae (1735, 1756). In the first edition of the Fauna Svecica (1746), Apis was reduced to three subgroups: Vespaee (now in- corporating Crabro), Apes propriè dictaee and Bombyli hirsuti. Furthermore, species were described for the first time. However, binomial species names were not listed until the sixth edition off Systema Naturae (1748). In the sixth to the ninth edition, 11 binomial species of Apis were given, six of which were true bees. Subsequent editions of the System Naturae increasingly established more genera of aculeate Hy- samplemenoptera pages and species of Apis. The tenth edition of the System Naturae (1758) is celebrated since it was chosen (almost 140 years later) by the “International Rules on Zoological No- menclature” as the starting point for modern con- Fig. 5: Examples of Abeilles solitaries, after Réaumur (1742). ventional nomenclature. In this edition, Linnaeus A. Head and extended proboscis of Xylocopa, B. Colletess sp. continued to narrow the genus Apis by splitting off and C. a halictid. Vespa, Crabro, Sphexx and Chrysis, leaving mostly only 12 John D. Plant and Hannes F. Paulus

Fig. 6: Classification of Angiopteraa insects in the first edition of Systema Naturaee of Linnaeus (1735), wherein Apiss is one of nine genera (second column from left) and is divided into four subgroups (right column).

true bees in Apis. He recognized eight genera of Hy- 1758) and Sphecodes ephippiuss (Linnaeus 1767), menoptera: Cynips, Tenthredo, Ichneumon, Sphex, were allocated to the wasp genus Sphex, possibly be- Vespa, Apis, Formica and Mutilla. cause of their red color and lack of body pubescence, Of these genera, only Apiss possessed a pro- since their proboscides differ little from that of Hal- nounced proboscis. The defining character of the ictus or Lasioglossum. Much of this was rectified by genus was “Os maxillis atque proboscide inflexa vagi- the thirteenth edition of Systema Naturaee (Linnaeus nis duabus bivalvibus”, which is freely translated as: 1790) with the help of Scopoli (1770) and Fab- “Mouthparts consist of mandibles and an inflected pro- ricius (1775). boscis with two double-folding sheaths”.2 In other In naming, at least, 68 species of bees, Linnaeus words, the elongate proboscis is formed in part by was, to a large extend, indebted to the descriptions two pairs of flattened sheath-like structures which previously given by his illustrious predecessors, fold back on themselves at rest, unlike the proboscis which he himself acknowledged, such as Johan of a butterfly which is coiled at rest or that of certain Frisch, R. A. Réaumur, Carl de Geer, Ulisse Aldro- hoverflies which is permanently outstretched. The vandi, Thomas Mouffet, Johannes Swammerdam two sheath-like structures evidently refer to the ga- and John Ray. His simplification of the higher clas- leae and labial palpi. Thus his definition, as inter- sification of bees, by placing all species into a single preted here, applies only to bees (or other aculeate genus, was, on the one hand, a heroic and early at- Hymenoptera) with a relatively long proboscis. tempt to develop a natural classification based on Unfortunately, Linnaeus is foggy about his defi- visible structural characters, but on the other hand, nition. In Apis he lumped together typical short- it represented a step backward in that it entirely ne- tongued bees (Colletes, Hylaeus, Halictuss and An- glected established knowledge of the biology and life drena), some short-tongued wasps, e.g. Myrmosa history of bees. The conflict between these two barbaraa (Linnaeussample 1758) (Mutillidae), Sapyga clavi- methods pages of classifying bees – artificiallyy according to corniss (Linnaeus 1758) (Sapygidae), the long- their biology and habits or naturallyy according to tongued bees and some long-tongued wasps, e.g. their morphology or genetics – continues to the pre- Bembix rostratuss (Linnaeus 1758) (Sphecidae). Fur- sent day, in particular, with regard to the relation- ther, some bees, e.g. Sphecodes gibbuss (Linnaeus ships between parasitic bees and their hosts. The cuckoo bumblebee (Psithyruss), for example, was only 2 Thanks are due to Horst Aspöck, Vienna, for consultation regarding very recently admitted as a subgenus within Bombus, the translation of the neo-Latin passage. previously being recognized as a separate genus. Evolution and Phylogeny of Bees 13

Johan Christian Fabricius. Fabricius (1775, 1793) employed mouthpart morphology to subdivide the single Linnaean genus Apis. In particular, he expounded on the lingua inflexaa character, attribut- ing the presence of a pronounced proboscis not only to bees but to members of the genera Sphex, Scolia, Thynnus, Masaris and Bembix. He distinguished five genera of bees (Hylaeus, Andrena, Apis, Eucera and Nomada) primarily on how many parts of the proboscis project outward. Apiss is quinquefid, with reference to the paired galeae, labial palpi and the single glossa. Euceraa is septemfid, in addition to the previously mentioned parts both paraglossae are especially elongate. The proboscides of “Hylaeus” Fig. 7: A. Example of a trifid proboscis (Melitta); B. quinquefid proboscis (Bombuss), after Kirby (1802). (which actually referred to halictids), Andrenaa and Nomadaa are trifid, with reference to the paired galeae and the singular glossa. Linnaeus (1790) incorporated the mouthpart as belonging to Andrena; Sphecodes gibbaa was placed criteria devised by Fabricius into his 13th edition of in Nomada; and Andrena hattorfiana, a species with the System Naturae by splitting Apiss into two sub- a long glossa, was originally described as Nomada. groups, those in which the proboscis has five termi- Moreover, in the genus Prosopis, Fabricius placed nal parts (lingua quinquefida) and those with three forms with narrow and slender bodies, such as Cer- terminal parts (lingua trifida) (Fig. 7 A). Further- atina albilabris, Lasioglossum nitidulum, Camptopoe- more, bees with a three-part proboscis were divided um frontale, as well as several true species of Hylaeus. into two categories, corresponding to the genera An- William Kirby. Kirby (1802) was at odds with drenaa and Nomada. The lingua trifidaa group, as con- the Linnaean definition of bees, as with others before ceived of by Fabricius and used by Linnaeus, con- him, such as Geoffroy (1762, 1785), Scopoli tained a diversity of species, such as Andrena, (1770, 1777), DeGeer (1773) and Illiger (1801), Agapostemon, as well as species of long-tongued bees, and he was compelled to further split up the genus e.g. Megachile, Osmia, Bombus, Xylocopa, Anthophora Apiss as conceived by Linnaeus. and Nomada, although the latter genera have five Kirby (1802) advanced the tradition of empha- terminal parts to the proboscis. Likewise, many sizing mouthpart criteria to classify bees and initiat- short-tongued bees were listed under lingua quinque- ed a major subdivision of bees (which he collectively fida. called “Apes”) into two large groups, Melittaa and Fabricius (1804) was very observant of bees. Apis. This subdivision approximates what are now He listed 16 genera, providing each with a defini- referred to as the short-tongued and long-tongued tion, yet he avoided any attempt at a higher classifi- bees, respectively (Table 4, Fig. 7 A, B). cation. In consideration of the sequence in which The defining character of Apiss continued to be they were described, we cannot be sure that Fabricius associated with the mouthparts: Lingua elongata, in- regarded the species of Hylaeuss (given as Prosopiss) to flexa. Further, Kirby maintained that the proboscis be bees. Some were to be found under Vespa (e.g. folds into three lengths to form the letter (Z) when Hyleoides concinna, Hylaeus hyalinatuss) and others viewed laterally, and that the glossa is covered by the within Prosopissample, which was listed between the labial palpi.pages The “genus” Melittaa was characterized masarine wasps and the spheciform wasps. by the fact that the glossa is short and not covered by It is evident that Fabricius relied on characters the labial palpi. Moreover, Kirby attributed a feature other than the mouthparts and that he attempted to to members of the “genus” Melitta, which DeGeer synthesize diverse features, such the general body had previously termed the rostrum porrectum. This form, coloration, hairiness and nest habits. Some refers to the first motion of the proboscis, since, species were assigned to a genus, despite the mouth- when it unfolds, the labium is pushed forward be- parts, for example, Fabricius described Osmia cyanea yond the mouth and maxillae, whereas in the “ge- 14 John D. Plant and Hannes F. Paulus

Table 4: Classification of bees, after Kirby (1802). Subdivision of “genera” Equivalent modern taxa MELITTA (Proboscis trifid, glossa short) * Glossa obtuse a. Glossa obtuse, apex bilobed Colletes b. Glossa obtuse, apex truncate Hylaeus * * Glossa acute a. Labrum modified, emarginate Sphecodes b. Labrum with a small modified appendage Halictus, Lasioglossum c. Labrum obtuse-angular, with tubercle Andrena, Melitta s.str., Dasypoda APIS (Proboscis elongate and folded) * Proboscis without flattened labial palpi a. Antenna subclavate in both sexes Panurgus b. Antenna filiform in both sexes Nomada * * Proboscis labial palpi (I and II) sheath-like a..Maxillary palpus 5-segmented. Labrum subquadrate Melecta b..Maxillary palpus 1-segmented. Labrum apically rounded Epeolus c. Labrum modified, elongate 1. Ventral female glabrous α. Abdomen of female conical and acute Coelioxys β. Abdomen of female subcylindrical Stelis 2. Ventral female hairy (scopal brushes) α. Maxillary and labial palpus with 2 palp-like segments Megachile β. Maxillary palpus 1-segmented Anthidium γ. Labial palpus with 1 palpus-like segment Chelostoma, Heriades δ. Maxillary palpus 4-segmented Hoplitis, Osmia d. Proboscis straight, maxillary palpus 6-segmented 1. Paraglossa developed, elongate Eucera 2. Paraglossae straight, short α. Labrum quadrate, unarmed Anthophora, Ceratina β. Labrum emarginate, with tubercle Xylocopa e. Proboscis partly curving, maxillary palpus 1-segmented 1. Body villous Apis 2. Body hirsute Bombus

nus” Apis, the first motion is to unbend the lower Epeolus, Anthophora, Eucera, Centris, Euglossa, Xylo- fold. copa, Bombus, Meliponaa and Apis. Kirby is little appreciated by modern historians Further developments. The tradition which for his efforts to subdivide each “genus” into “fami- recognized two groups of bees, based foremost on lies”. This is perhaps because he used the terms in a the elongation of the proboscis, continued after Kir- sense contrary to modern practice, also perhaps be- by for over a century. The two groups were elevated cause he assigned each family a set of symbols and to the family level–the Andrenidae and Apidae–in not a name. The “families” of Kirby are about 20 in the classification systems of Latreille (1802a, 1809, number and samplecorrespond to generic concepts. His 1811a, pages1829), Westwood (1839), Smith (1853, classification of the “families” and their modern 1854) and Taschenberg (1883). A two family sys- equivalent representatives is given in Table 4. The tem was revived nearly a century later by Warncke first “genus” Melittaa contained the “families” which (1977a). correspond to the following modern equivalents: By around 1890, the number of genera de- Colletes, Hylaeus, Halictus, Andrena, Dasypodaa and scribed drastically increased year for year (Michen- Melitta. In the “genus” Apis, Kirby recognized “fami- er 1997). The two-part division of bees was aban- lies” corresponding to Dasypoda, Nomada, Melecta, doned for the recognition of a larger number of 78 John D. Plant and Hannes F. Paulus

Parasitic Bees Bohart (1970) reckoned that there are 18 parasitic lineages consisting of 12 cleptoparasitic, 6 socially The great majority of bees collect nectar and parasitic and one robber bee taxa (Fig. 68). Rozen pollen to provision their young. About 15%, rough- (2000b) accounted for 26 independent origins of ly 2,765 species (unpublished data), are parasitic in cleptoparasitism in bees. Michener’s (2007) ap- some manner. Some earlier figures reported consid- proximated 31 origins of cleptoparasitic and 16 of erably higher percentages: 21% for USA and Canada socially parasitic bees. in Hurd (1979) and 19% for bees worldwide in According to the list of parasitic bees assembled O’Toole & Raw (2004). Bohart (1970) calculated in Table 16, cleptoparasitic lineages could have that 15% of North American bees (north of Mexico) arisen independently, at least, 32 times, social para- were parasitic and extrapolated that there should be sitism 16 times and robbers bees on three occasions. worldwide approximately 3,700 species of parasitic In many cases, the parasitic status of a taxa is pre- bees. sumed or based on circumstantial evidence and has This section briefly examines the efforts to re- not been demonstrated by nest excavation. solve the phylogenetic position of parasitic bees with Several recent cladistic studies focusing on pa- respect to non-parasitic bees. rasitic bees present a contrasting picture. The stud- The most common hypothesis for the evolu- ies of Straka & Bogusch (2007) (Fig. 69) using tionary development of parasitic bees is that they larval morphological data and of Cardinal, Stra- evolved from their hosts (Wheeler 1919, Grütte ka & Danforth (2010) (Fig. 70), Cardinal & 1935). In this theory, sometimes called Emery’s Danforth (2013) (Fig. 71 A) and Hedtke et all. (1909) rule, both host and parasite are derived from (2013) (Fig. 71 B) using molecular data, which will the same lineage (monophyletic theory of parasit- be discussed in detail later, drastically reduce the ism). Numerous examples of close relationship be- number of independent origins of parasitism in the tween parasite and host are known, e.g. Psithyrus- Apidae. Bombus. It is conceivable that parasites which undergo subsequent species radiation and host- switching end up being only remotely related to Antiquity of Bees their hosts, so that the monophyly of the original host and parasite becomes greatly obscured. Lastly is This section provides a review of the fossil his- the theoretical possibility that parasitism could arise tory of bees, family by family. It concludes with a de novo and that the initial host belonged to an en- presentation of a phylogeny of major clades of bees tirely unrelated lineage (polyphyletic theory of para- based on the results of the present analysis and in- sitism). cludes significant fossil findings. The origin of cleptoparasitism in bees, accord- Bees enjoy a relatively long evolutionary histo- ing to the monophyletic theory of parasitism, may ry. Although one cannot say with certainty when be ascribed in part to competition among conspe- they came into existence, consensus opinion holds cific females for adequate nest sites. In fact, there that this must have occurred during the late Creta- are ample signs that competition between nesting ceous period, about 100 to 125 million years ago females in a population occurs (nest take over, rob- (Michener 1979, Michener & Grimaldi bing larval provision), particularly when many 1988a,b, Grimaldi 1999, Engel 2000a, Grimaldi nests are crowded next to each other. Nesting fe- & Engel 2005, Ohl & Engel 2007). This esti- males leave their nests open when they occasionally mate is not based on the bee fossil record, but on go on foragingsample bouts, and their nests are vulnerable pages that of the flowering plants (angiosperms). Angio- to visitation and usurpation by neighbors during sperms are presumably much older than bees, and if these times, as well as by non-bee nest parasites. they are actually the sister group to the Gymno- Nonetheless, nest usurpation is not cleptoparasit- sperms they could have diverged from Gymno- ism, and reports of intra-specific cleptoparasitism sperms in the Jurassic period, approximately 200 are rare. million years ago (Stuessy 2004, Smith, Beaulieu Evolutionary biologists are interested in know- & Donoghue 2010). Early angiosperms were pre- ing how often parasitism has arisen among bees. sumably wind or insect pollinated with beetles, mi- Evolution and Phylogeny of Bees 79

Fig. 68: Phylogeneticsample relationships of bees, modified after Bohart (1970), withpages consideration of parasitic taxa (in boxes). 80 John D. Plant and Hannes F. Paulus

Fig. 69: Phylogeny of Apidae with emphasis on cleptoparasitic taxa, after Straka & Bogusch (2007) based on larval data. Out- group (Melittidae s.l. and Megachilidae) not shown. Cleptoparasitic taxa labeled gray.

cropterigid moths and flies playing dominant roles The initial adaptive radiation of the major line- as agents of pollination (Grimaldi 1999, Grimaldi ages of bees presumably occurred in conjunction & Engel 2005). with the expansion and radiation of modern angio- In a fossil calibrated analysis of major clades of sperms. This assumption finds support in recent bees, Cardinal & Danforth (2013) estimated the studies employing the relaxed molecular clock dat- age of bees to be between 113–132 million years ing method. Brady, Larkin & Danforth (2009) (based on their analysis 3). hand-aligned 18s and 28s RNA data for species of Modern angiosperms first appear in the fossil re- Aculeata and estimated that bees arose between 120 cord during the Cretaceous (Aptian, 125–112 mil- and 112 million years ago. lion years ago) (De Bodt, Maere & Van de Peer 2005), although using divergence time estimates their origin maysample be calculated as significantly older Fossi l recorpagesd of bees (Smith, Beaulieu & Donoghue 2010). The dra- Fossil material exists for 11 of 22 subfamilies of matic diversification of major angiosperms, in par- bees (recently reviewed in Michez, Vanderplanck ticular, the monocots and eudicots, began about 110 & Engel 2012). In the following, many of the im- million years ago (Doyle & Endress 2000, Crepet, portant fossils of the various bee lineages are briefly Nixon & Gandolfo 2004), and by about 90 mil- listed with numbers that correspond to those in Fig. lion years ago angiosperms became dominant in spe- 77 for the respective lineages. Fossils that are alleged cies numbers (Crepet 2008). to be bees, but not otherwise reliably determinable Evolution and Phylogeny of Bees 99

(Paleomelittidae) belongs in a separate family basal an evolutionary “tree” or cladogram in consideration to the Melittidae s.l., and (iii) that the Melittidae s.l. of ancestral vs. derived features with respect to an is paraphyletic and divided into three families (Da- outgroup. In the cladogram, groups are arranged in a sypodaidae, Melittidae s.str., Meganomiidae). hierarchical branching pattern based on shared derived characters. Cladograms are hypotheses on the phylogeny of the group considered. Part II: A Phylogenetic Study of Bees in Some of the most important terms in cladistics Light of Morphological Evidence will be briefly explained: Apomorphyy is a derived character (or character state). Plesiomorphyy is an ancestral or “primitive” character (or character state). Introduction Synapomorphyy is a shared derived character (or character state) that serves to unite two or more taxa into The higher level phylogenetic arrangements of a monophyletic group. Symplesiomorphyy is shared bees have not been acceptably resolved despite previ- ancestral character (or character state). ous comprehensive studies based on morphological The principles of cladistics or phylogenetic sys- data, one on the long-tongued bees (Roig-Alsina & tematics were established by the German entomolo- Michener 1993), and another on the short-tongued gist Willy Hennig in 1950 but did not become ac- bees (Alexander & Michener 1995). Several re- cessible to the international scientific community cent molecular studies have taken into consideration until the English translation of his work appeared a relatively wide range of higher bee taxa (Ascher, (Hennig 1966). Cladistics differs from other ap- Danforth & Ji 2001, Danforth, Fang & Sipes proaches of reconstructing evolution, such as phe- 2006, Danforth et al. 2006, Brady, Litman & netics which groups taxa according to their overall Danforth 2011, Debevec Cardinal & Danforth similarity (Sneath & Sokal 1963, 1973). Excellent 2012, Hedtke et al. 2013). Aspects of bee phyloge- introductions to the topic of cladistic practice and ny which have remained vexing are, for example, un- theory are Kitching et al. (1998) and Lipscomb certainty about the relationships of the basal groups (1998). to each other, the position of various cleptoparasitic As in most cladistic studies, the characters and taxa to their non-cleptoparasitic relatives, the posi- character states are described (see, List of Charac- tion of the Stenotritidae and Oxaeidae, the relation- ters). The distribution of the character states is given ships within the Apidae and Colletidae, the mono- in a data matrix (Table 17), whereby the number of phyletic or polyphyletic status of the Melittidae, the the characters corresponds to that in the List of basal groups of the Megachilidae and the placement Characters. of several isolated genera, e.g. Ancyla, Ctenoplectra, There are always at least two character states: Tarsaliaa and Pararhophites. The plesiomorphic and the apomorphic. The plesio- The main goal of this study is to reassess the morphic state is designated (0) and usually repre- higher phylogeny of bees utilizing a fresh set of char- sents the primary plesiomorphic state, but, in some acters based largely on morphological data in com- cases, it infers a secondary reversion to primary ple- puter-assisted cladistic analyses using several meth- siomorphic state. The apomorphic state or states are ods (parsimony, successive reweight, implied weight, assigned the numbers (1), (2), (3), etc. depending on Bayesian and neighbor-joining). The study includes how many apomorphic states have been determined. members from all seven families, all 22 subfamilies For convenience, characters and character states are and 48 of the 58 tribes of bees recognized by notated in the text by the character number followed Michener (2007sample). by the state;pages for example, character 7 (state 2) is given as character 7.2. Methods The results of the present cladistic analysis are displayed as cladograms which show character support for each node. An illustrative example is given Cladistics and tree representation in Fig. 78, which is based on the hypothetical data Cladisticss is a method of analyzing evolutionary set in Table 17. The character number is given above relationships of taxa that leads to the construction of the branching line and the character state below the 100 John D. Plant and Hannes F. Paulus

Table 17: Example of a data set, showing the distribution of the character states for 11 characters across five taxa. Taxa Characters 1234567891011 Outgroup 0 0 0 0 0 0 0 0 0 0 0 Taxon 1 11001001101 Taxon 2 11000120101 Taxon 3 10110201010 Taxon 4 10100011110

line. Solid circles represent unique apomorphies that has only two branches diverging from it. However, a occur only once in the cladogram, empty circles in- taxon can has multiple sister taxa, if the node forms dicate non-unique apomorphies that also occur else- a polytomy, and the branching is polytomous, i.e. has where in the cladogram. more than two branches diverging from it. In the cladogram figured below, character 1.1 Monophylyy refers to a natural group, or clade, (i.e. character 1, state 1) unites the ingroup, since all that includes the single common ancestor and all ingroup taxa share the same apomorphic state. It is descendants. thus a synapomorphy of the entire ingroup. In contrast, paraphylyy and polyphylyy refer to arti- Character 3.1 is shared only by taxon 3 and 4, ficial groupings. They occur when the monophyl- and is an unique synapomorphy for clade B. etic status of a group, which was previously under- Character 5.1 occurs only in a single terminal stood or declared, cannot be demonstrated and is taxa (taxon 1); it is an unique autapomorphy of that refuted. taxon, and as such provides no information about A group is paraphyletic when not all of its mem- phylogenetic relatedness. bers have the same single common ancestor. The Character 8.1 serves as a non-unique synapo- classical example of a paraphyletic taxa are the “Di- morphy of clade B, since it also occurs in taxon 1. nosaurs”, since they contain descendants which are Some common terms used to describe phyloge- not (called) dinosaurs, i.e. birds. netic relationships are the following. Sister groupss are A group is polyphyletic when all members lack a two taxa which are more closely related to each other single most recent common ancestor. For example, than to other taxa. A taxon has only one sister group, bees would be polyphyletic if it turned out that they if the node from which it emerges is dichotomous, i.e. originated from wasps on more than one occasion.

Unique autapomorphy outgroup Non-unique autapomorphy

5 8

2 9 11 Taxon 1 1 1

6 7 Clade A 1 1 1

1 Taxon 2 Character number 1 2

sample4 6 pagesIngroup Character state 1 3 8 10 Taxon 3 1 2

Basal node 7 9 Clade B 1 1 1 Taxon 4 Unique synapomorphy 1 1 Non-unique synapomorphy

Fig. 78: Cladogram resulting from data set in Table 17. Evolution and Phylogeny of Bees 101

The “most basal clade” in a cladogram is con- Cleptoparasitic bees ventionally represented as the one placed closest to Cleptoparasitic and social parasitic bees from the outgroup, and it is sister to the remaining clades most groups were examined and included in some of of the ingroup. In Fig. 78 that would be clade A. the cladistic analyses. Their inclusion creates meth- The expression “most basal clade” is convenient odological problems. The evolutionary transition when describing the branching hierarchy of a clad- from a solitary to a cleptoparasitic life style is accom- ogram; however, technically it is incorrect (Krell & panied by a loss of numerous habits and structures, Cranston 2004), since there are always at least two especially those associated with pollen collection and branches at the most basal node, thus two most basal nest construction, as well as by the acquisition of clades. The branching at each node can be rotated new behaviors and morphological adaptations asso- and which clade is place higher has no relevance in a ciated with cleptoparasitism, such as a hard cuticula, cladogram. That clade A is positioned above clade B strong mandibles, protective structures, such as a does not mean that clade A occurred first, rather long labrum, and adaptations for placing eggs in the both originated at the same time. host cell. In short, the cleptoparasitic bees probably exhibit too many strong structural convergencies Taxon Selection among themselves and are too different from pollen- collecting bees to expect reasonable results in a parsi- The species sampled and included in the data set mony analysis based on adult external morphology. were chosen in consideration of several criteria, since Since it is highly unlikely that obligate cleptopara- it is not feasible to include all known species of bees. sitic bees would give rise to bees with pollen-provi- Representative: Taxa selected were intended to re- sioning habits, their exclusion from one part of the present members from as many of the higher groups analysis is justified. of bees as possible. Exemplar: One or several mem- Representatives of the following parasitic tribes bers were chosen to reflect a genus or other category were either not included or not available for exami- of classification. Characters were coded according to nation: Sphecodini (Halictidae) and Protepeolini those species. Additional material from the same ge- (Apidae), as well as Brachynomadini, Caenoprosopi- nus or related genera was consulted when possible. dini, Hexepeolini and Townsendiellini (Nomadi- Diversity: In some cases several species from the nae). same genus warranted separate coding in order to encompass diversity of characters within a genus or genus s.l. (e.g. Leioproctus, Apis, Ceratina, Dufourea). Outgroup assignment Basal taxa: It was attempted to include or at least The presumed common ancestor of bees and examine taxa, which previous studies have pointed spheciform wasps probably existed in the late Creta- out as possessing “primitive” features, or which in ceous period. However, it is not known which con- previous phylogenetic studies were indicated as as- temporary spheciform wasp can be considered the suming a basal position among bees (e.g. Euryglossi- most closely related to bees. Two sets of outgroups nae) or other higher group (e.g. Manuelia, Corynura, were selected for the cladistic analysis: the Pemphre- Deltoptila). Problematic or phylogenetically isolat- doninae (Diodontus, Pemphredon, Passaloecus, Psen, ed taxaa were also included, such as Ancyla, Cteno- Psenuluss) and the Philanthinae (Philanthus, Aphilan- plectra, Tarsalia, Pararhophites, representatives of thops, Cerceris). Both subfamilies are placed in the Stenotritidae and Oxaeidae. Not available or not family Sphecidae by Menke (1997); however, in the includedd: Non-parasitic taxa that were not available family Crabronidae by Melo (1999). Pemphredoni- or not included samplein the examination were members of nae wasps pages are generally non-flower visitors; they usu- the tribes Dissoglottini (Diphaglossinae, Colletidae), ally obtain liquid nourishment by squeezing or bit- Calliopsini (Panurginae), several monotypic tribes of ing prey (aphids, leafhoppers) or by licking the Panurginae: Protomeliturgini (Protomeliturga), honeydew. The proboscis is generally not specialized Mermiglossini (Meroglossa), Nolanomelissini (Nola- for nectar uptake; it is small to minute in size com- nomelissa) and Neffapini (Neffapiss), as well as the pared to the mouthparts of some Philanthinae which monotypic subtribe Eucerinodina (Eucerini, Api- may be well-developed and adapted to nectar feed- dae). ing, thus permitting a greater comparison to struc- 102 John D. Plant and Hannes F. Paulus

tures in bees. The polarity of morphological charac- a comparative morphological study or because it ters was predominantly determined by comparison would require extensive dismemberment of speci- with the outgroups. mens.

Character choice Character coding & definition As a general guideline, characters were included There are two opposing approaches to coding that appeared to have some relevance for deciphering morphological characters for cladistic analysis. They the higher phylogeny of bees. About 200 characters primarily concern when and how the polarity of the are defined, most pertain to adult morphology: characters should be determined, either before or af- mouthparts, head, metasoma, mesosoma, wings, ter the analysis. Here, character polarity was deter- legs, genitalia and pollen collecting structures are mined a priori, i.e. before the parsimony analysis by also utilized. The morphological characters and cod- comparison with the outgroups in accord with Hen- ing of their states are based on my own observations. nigian principles. Unless otherwise stated, only those characters which As mentioned previously, the ancestral or plesio- I was able to observe, judge and evaluate were ac- morphic state for a character is assigned the state cepted. When applicable, consideration was paid to zero (0). The character states (1), (2), (3), etc. repre- characters used in previous studies of adult external sent apomorphic character states. The question mark morphology and cladistics of bees. The numerous (?) indicates data is not known or too difficult to new characters based on comparative morphological specify. Inapplicable data is indicated by a dash (–) in observations provide fresh substance to the data ma- the Nona software program and by a question mark trix. Five non-morphological characters concern as- (?) in Paup. The apomorphic variables in multistate pects of nest biology, the data for which was culled characters represent in most cases hypothesized ho- from the literature. mologies that are mutually exclusive of each other. Numerous characters of all kinds were rejected The secondary absence of a character state caus- from previous analyses that showed strong inconsist- es problems when coding characters for cladistic encies (i.e. high homoplasy, high variation), that re- analyses (Bleidorn 2007, Fitzhugh 2008). We are lied on fine quantifiable measurements of propor- sometimes forced to code the presumable secondary tions, or that showed a continuous range of variation. loss of a structure with the same value as its primary Further, characters with unknown polarity or sub- absence, due to the morphologically identical ap- stantial missing data were avoided. pearance. If there is any direct morphological indica- Some characters were omitted from the analysis tion suggesting that a secondary absence has oc- because they were considered to have little value for curred (e.g. is structure not entirely reduced in all the interpretation of higher phylogenetics, for exam- taxa or the structure is recognizable to a slight degree ple, hair color, integument color, facial color mark- in some taxa) then we regard it as justifiable to at- ings, surface sculpturing and punctation. These tempt to code according to a proposed hypothesis of characters may be useful in a more restricted analy- evolutionary sequence in which the secondary ab- sis. Several characters susceptible of being related to sent is coded separately from primary absence. large or small-body size (wing venation) also were One methodological feature which is recom- discarded. mendable but regrettably absent in all parsimony Since a comparative morphological study of software programs is the ability to disallow the use of male bee intromittent organs that could lead to a de- reversals as valid synapomorphies. One way to get termination ofsample homologies is currently lacking, only around pagesthis deficiency and negate the influence of two male genitalia characters were utilized. Male coding secondary losses (reversals) as apomorphic in genitalia and related characters are of course widely the software programs Paup and Nona is to code used on the species and generic levels. each instance of a reversal with a separate apomor- The full richness of the morphology of bees has phic state, as long as there are enough states available yet to be tapped for phylogenetic purposes. Many (maximally nine apomorphic states are permitted). pertinent morphological characters exist but were Lastly, the definitions of character variables are not examined due to the time-consuming process of not always intended to be as specific as possible, i.e. Evolution and Phylogeny of Bees 103

they do not necessarily accord to a hard morphology. ferred to as “Nona”), Win PeeWee versions 2.8 and Character definitions are chosen according to the de- 3.0 (Goloboff 1993–1997b) (referred to as gree of detail required. Equivocal or ambiguous defi- “Piwe”), Win XPeeWee version 1.3 (Goloboff nitions that are subject to more than one interpreta- 1997) (referred to as “XPiwe”), WinPaup* beta ver- tion are, of course, not intended to confuse or sions 4.0b8 and 4.0b10 (Swofford 2003) (referred mislead, but are legitimate attempts to encompass a to as “Paup”), MrBayes 3.2.1 (Ronquist, Huelsen- range of insignificant variations within one value. beck & van der Mark 2007) and TNT version 1.1 (January 2010) (Goloboff, Farris & Nixon 2008). Relaxation of bee specimens For convenience of operation, including the op- To remove the mouthparts and genitalia from timization of characters and display of tree topology, dried bees, the quick and easy relaxation procedure the computer program WinClada beta version described in Plant & Dubitzky (2008) was used. 1.00.08 (Nixon 2002) proved valuable. Paup was In this method, the bees are placed on a piece of Sty- used in combination with the shell program PaupUp rofoam, which serves as a float and which is put into version 1.031 beta (Calendini & Martin 2005), a a cooking pot or plastic food container partly filled graphical interface for Paup. Additionally, TreeView with boiling water for about 30 minutes with a tight- version 1.6.6 (Page 2001) was used to convert trees ly closed lid (Fig. 79). in the Paup format to the Hennig format for examination in WinClada. Morphology Removed parts, such as the proboscis, genitalia Types of analyses or legs, were stored in small vials with 90% alcohol. Several types of analyses were performed on the They were not treated beforehand with potassium data – maximum parsimony, weighted analysess (succes- hydroxide (KOH), which in some cases can lead to sive weightt and implied weightt), Bayesian and neigh- the formation of structural artifacts. The parts were bor-joiningg analyses. examined and dissected under the stereo-micro- The parsimony methodd is character based and scope; some were placed on temporary glass slides seeks to find a tree with the fewest number of evolu- and viewed with light-microscopy. Permanent glyc- tionary steps. Parsimony analyses were implemented erin preparations were not prepared, so that it would in Nona and some in Paup, with all characters treat- be possible to view the same parts from different an- ed unordered and with equal weight. gles and positions. To find the most parsimonious tree or trees using Nona, the following heuristic search strategy was Computer Programs selected. The algorithm used for branch-swapping was multiple TBR + TBR (tree bisection reconnec- Cladistic analyses were computed using the fol- tion) (i.e. mult*max*). Various settings were used for lowing software programs: WinNona versions 1.8 the maximum number of trees to hold (hold 1200– and 2.0 (Goloboff 1993–1997a) (hereafter re- 10,000), the number of replications (mult20–200) sample pages

Fig. 79: Diagram of relaxing-chamber system utilizing steaming water, after Plant & Dubitzky (2008). 250 John D. Plant and Hannes F. Paulus

Table 37: Classification of subgenera of Xylocopaa after Minckley (1998) and Hurd & Moure (1963). Right column, general biogeographic region: A Australian, E Ethiopian, N Nearctic, Ne Neotropical, O Oriental, P Palearctic, Po Polynesian.

MINCKLEY (1998) HURD & MOURE (1963) Region MINCKLEY (1998) HURD & MOURE (1963) Region Old World subgenera New World subgenera Lestis as a separate genus A Cirroxylocopa Cirroxylocopa N Proxylocopa Proxylocopa s.str P Dasyxylocopa Dasyxylocopa N Ancylocopa P Diaxylocopa Diaxylocopa N Copoxyla Copoxyla P Monoxylocopa Monoxylocopa N Ctenoxylocopa Ctenoxylocopa EPO Nanoxylocopa Nanoxylocopa N Gnathoxylocopa Gnathoxylocopa E Notoxylocopa Notoxylocopa NNe Nyctomelitta Nyctomelitta O Schonnherria Schonnherria NNe Maaiana - P Ioxylocopa N Rhysoxylocopa group Xylocospila N Biluna Biluna O Xylocopoda Xylocopoda N Nodula Nodula O Xylocopoides Xylocopoides Rhysoxylocopa Rhysoxylocopa PE Xylocopsis Xylocopsis N Xylomelissa Xylomelissa E Neoxylocopa group Ne Acroxylocopa Neoxylocopa Neoxylocopa NNePo Apoxylocopa Megaxylocopa N Dinoxylocopa Stenoxylocopa Stenoxylocopa N Epixylocopa Xylocopina Euxylocopa Perixylocopa Ethiopian group Review of phylogeny of Xylocopini. Accord- Alloxylocopa Alloxylocopa PO Bomboixylocopa Bomboixylocopa P ing to Michener (1944) the Xylocopini contained Mimoxylocopa three genera––Mesotrichia, Lestis and Xylocopa. Hurd Koptortosoma Koptortosoma EOPA & Moure (1963) in their comprehensive study of Afroxylocopa E the Xylocopini differentiated Xylocopaa into 48 sub- Cyaneoderes O genera (Table 37). They reduced Mesotrichia, which Cyphoxylocopa A contains some of the largest carpenter bees, to a sub- Oxyxylocopa E genus of Xylocopa. In addition, they confirmed the Lieftinckella A generic status of Proxylocopa, with two subgenera. Mesotrichia Mesotrichia EP The authors thus regarded the tribe to contain three Hoplitocopa A genera: Xylocopa, Lestis and Proxylocopa. Hoploxylocopa O Cunha (1983) performed a phenetic analysis in Platynopoda OPA consideration of 82 characters for males and 75 for Prosopoxylocopa Prosopoxylocopa E females, plus 32 head measurements, based on de- Xenoxylocopa E Xylocopa P scriptions in Hurd & Moure (1963). The study Zonohirsuta O encompassed 42 subgenera of Xylocopaa (Lestis and Proxylocopaa were not included) and two groups of subgenera emerged. One group contained all New World subgenera plus many Old World subgenera, where it is the exclusive species of bee (Cockerell while the second group contained only Old World 1935a). Theresample are about 520 species and subspecies subg enera.pages (unpublished data). Some estimates are as high as Minckley’s (1998) phylogenetic analysis of the 700 species worldwide (Griswold, Parker & Han- genera and subgenera of the tribe Xylocopini was son 1995). The genus contains 31 subgenera, in- based on 55 morphological characters coded for cludingg Lestis and Proxylocopaa (Minckley 1998, adult males and females of 51 ingroup species. Some Michener 2007), which have generated particular associations uncovered in Cunha’s study were con- phylogenetic interest since they have been previously firmed by Minckley, for example the Neoxylocopa regarded as separate genera. group of Minckley (1998) and the (Xylocopoidess + Evolution and Phylogeny of Bees 251

Xylocopaa by Hedicke (1938), then raised to generic level by Maa (1954) who ascribed to it the subgenus Ancylocopa. Minckley (1998) considered both Prox- ylocopaa and Lestiss as subgenera of Xylocopaa to avoid paraphyly of that genus, a viewpoint which was adopted by Michener (2000a, 2007), Leys (2000) and Leys, Cooper & Schwarz (2000, 2002). Thus only one generic name is presently necessary for the Xylocopini. Leys, Cooper & Schwarz (2002) performed a phylogenetic analysis on species of 22 subgenera of Xylocopaa using molecular data from two nuclear genes, EF-1α and PEPCK, combined with two previously published mitochondrial genetic sequences (COI, cyt B) and the morphological data set of Minckley (1998). In the Bayesian analysis three clades of subgenera resulted (Fig. 168): (i) a New World group with the subgenera Nyctomelittaa (Ori- Fig. 167: Phylogenetic relationships of subgenera of Xylocopa, ental) and Proxylocopaa (Palearctic) as sister taxa, (ii) a summarized after Minckley’s (1998) analysis 3 (equal weight geographically dissimilar group (Xylocopa s.l.) and and unordered characters, strict consensus tree, fig. 11B). The (iii) an Ethiopian – Oriental group of subgenera. genera belonging to the respective groups are given in Table 37. The Oriental subgenus Biluna was recovered at the * Xylocopoidess is Neotropical in distribution. base of the genus closely followed by the African

Calloxylocopa) clade (Table 37). However, Cunha’s division of the subgenera of Xylocopaa into two subgroups was not supported. Group two of Cunha (1983), which contained only Old World subgenera, corresponded only partially to the “Ethiopian” group of Minckley (1998). A simplified version of Minckley’s strict consensus tree of analysis 3 (characters equal weight and unordered, fig. 11B) shows the clade of Proxylocopa and the “Ethiopian” group of subgenera as the sister to the remaining subgenera (Fig. 167). Previously, both Lestiss and Proxylocopaa have been allocated to the generic level. Lestiss includes two species from Australia that are metallic green or blue (Leys 2000). It may represent an isolated ancient group of Australian Xylocopaa bees since it is not closely related tosample southern Asian species (Michener pages 2007: 606). However, in Minckley’s analysis they occurred neither at nor near the base of the Xylocopini. Proxylocopaa contains about 16 mostly Palearctic species. They nest in the ground and some species are adapted to nocturnal flight and forage before Fig. 168: Phylogenetic relationships of subgenera of Xylocopa, sunrise and after sunset (Gottlieb et al. 2005). after Leys, Cooper & Schwarz (2002, fig. 4), Bayesian analy- Proxylocopaa was originally proposed as a subgenus of sis. Koptortosoma s.str. was paraphyletic. 252 John D. Plant and Hannes F. Paulus

subgenus Perixylocopa. The Oriental region was con- Michener (1987), Michener (2007) and Minck- sidered to be the place of origin for the genus. ley (1998) and discussed with respect to the evolu- Results of the present cladistic study. Repre- tion of the genus. sentatives of three subgenera (Proxylocopa, Lestis, Basitibial Plate – Homology Problems. The and Xylocopa s.str.) were included in the study. Xylo- phylogenetic importance of Proxylocopaa has been copa s.str. was basal to the Proxylocopa plus Lestis discussed on previous occasions (Malyshev 1931, node in the parsimony (1.P), successive weight (1. Hurd & Moure 1963, Daly et al. 1987, Minckley SW) and Bayesian analyses; while in the implied 1998, Michener 2007: 592, 597). Since Proxyloco- weight (1.IW, 1.IWx) and neighbor-joining analy- paa is the only ground-nesting Xylocopaa and has py- ses, Proxylocopa was basal to Lestis plus Xylocopa gidial and basitibial plates which are commonly s.str. Due to the limited number of subgenera inves- found in ground-nesting bees, it has been argued tigated, no conclusions should be drawn regarding that Proxylocopaa should represent an ancestral or ba- the intrageneric phylogenetic arrangements of Xylo- sal group with respect to the remaining Xylocopa copa. (Malyshev 1931, Hurd & Moure 1963). The al- Synapomorphies of Xylocopa (Fig. 165, Node ternative interpretation is that Proxylocopaa is a subge- D): Numerous synapomorphies support the mono- nus of Xylocopa, since they share a large number of phyly of the genus Xylocopa: Labrum basally exposed common traits. This implies that Proxylocopaa sec- (character 28.1). Base of labrum elevated, also pre- ondarily acquired ground nesting habits and related sent in Manuelia (character 29.2). Lateral sides of structures (Daly et al. 1987, Minckley 1998, apical labrum flanged (character 31.1). Lorum and Michener 2007: 597). mentum separated (character 53.1). Membrane be- In Minckley’s (1998) cladistic analysis of Xylo- tween mentum and prementum large (character copa, no members of the outgroup (Manuelia, Cer- 56.0). Apex of stipital sclerite expanded (character atinini, Allodapini, Megachilidae) possessed a well- 60.1). Stipital sclerite robust (character 61.1). Galeal developed, i.e. plesiomorphic, basitibial plate. velum long, narrow and stiff (character 79.5). Galeal Normally coding Proxylocopaa as plesiomorphic for inner surface with longitudinal row of hairs reduced the basitibial plate and pygidial plate would tend to (character 84.3). Posterior surface of flabellum with produce results with Proxylocopaa occurring as the ba- a cobblestone pattern (character 119.1). In addi- sal group of Xylocopa. However, based on morpho- tion, at the base of the flabellum is a bare shank logical evidence, such as the absence of lateral carina (Michener & Brooks 1984, Michener 2007, fig. on the plates, Minckley (1998) regarded the condi- 86-la-c), which probably represents a further syna- tion of the basitibial and pygidial plates in Proxylo- pomorphy. Further characters include: Metanotum copaa as unique and derived with respect to the re- flat and vertical (character 133.2). Stigma of fore- mainder of the ingroup. In that study the five wing short (character 141.1). Wings papillate, alars characters associated with the basitibial plate and not haired (character 142.2). Jugal lobe of hindwing one for the pygidial plate were scored as missing for short (character 144.2). Arolia absent (character Proxylocopa. These results showed that Proxylocopa 145.1). Spine on forecoxae (character 151.1). Tibial was not located at the base of the genus, but always spur with very wide velum (character 161.2). Basiti- nested among the other subgenera of Xylocopa. The bial plate not emerging from tibial base (except phylogenetic position Proxylocopaa within the genus Proxylocopa) (character 172.2). Apex of hind basi- Xylocopaa was considered not conclusive. tarsus laterally offset and with short pointed process All Xylocopinae have either a reduced basitibial (character 188.1). This character is an ambiguous plate (lacking setal field, lacking a carina rim, slant- synapomorphysample since it is absent in the Ceratinini ing, swollenpages or descended, i.e. not emerging from and Allodapini but present in Manuelia. It is equal- base of tibia) or no plate at all (most Allodapini). ly parsimonious to assume that it developed conver- Although the presence and location of the basitibial gently in Xylocopaa and Manuelia. plate in Proxylocopaa are plesiomorphic, the specific Aspects of Xylocopaa evolution. Many aspects structure of the plate differs from the well-developed, of the external morphology of Xylocopa, such as the plesiomorphic condition in that it lacks a central basitibial and pygidial plates, have been extensively field of short setae surrounded by a bare and raised covered in Hurd & Moure (1963), Sakagami & rim. In Xylocopaa (Proxylocopa) andarabanaa and ol- Evolution and Phylogeny of Bees 253

ivieri the plate is swollen and convexly shaped. The the corol la of tubular flowers to access nectar (nec- apical margin (carina) is raised. The central area is tar robbing) (Schremmer 1972). Xylocopa does not more or less bare with some scattered short stubs or use the mandibles to cut a hole in the flower, as hairs. In an unidentified specimen of Proxylocopa bumblebees do. from Greece, which probably belongs to the olivieri Transport of pollen in crop. A curious behav- group, the basitibial plate is somewhat hairy and not ioral trait of female Xylocopa is the increased reli- swollen. The hairs, however, are not restricted to the ance on transporting pollen in the crop. This phe- plate and appear like other hairs on the outer tibia. nomenon has been described and discussed on The condition of the basitibial plate in Proxylocopaa is several occasions (Bischoff 1927; Schremmer thus not typical with those in most ground-nesting 1959, 1972; Jander 1976; Anzenberger 1977, bees. Gerling, Hurd & Hefetz 1983). Although Xylo- The reduction and eventual loss of the basitibial copa females possess a scopal apparatus on the hind plate in Xylocopinae is associated with an evolution- tibia and basitarsus, and some also the femur as in ary switch from ground nesting to nesting in wood Proxylocopa, bees with a pollen load in the leg scopa and stem. It is conceivable that the switch occurred are not commonly encountered in the field or in once in the Xylocopinae. In this scenario the reduced museum collections. Schremmer (1972) showed plate in Proxylocopaa would have secondarily re-ac- by dissection of Xylocopa bees that the crop may be quired its position at the base of the tibia in connec- full with pollen while the leg scopa would be emp- tion with secondary ground nesting habits. The de- ty. Schremmer demonstrated the importance of the scended basitibial plate would be a synapomorphic stipital comb on the mouthparts of Xylocopa for for Xylocopaa (with a reversion to the plesiomorphic cleaning the foreleg and thus for the consumption position in Proxylocopa). The argument that Proxylo- of pollen. The stipital comb is well-developed in copa is a secondary ground nester is quite convinc- Xylocopa, although it is common to most Apidae. ing; however, the present cladistic analysis remains Schremmer concluded that Xylocopa utilizes both ambiguous on this matter. crop and scopal transport depending on whether Noteworthy is the presence of scopa on the hind pollen from the flower is initially transferred to the trochanter and femur in Proxylocopaa which may also dorsall side of the bee’s thorax and wings, or to the indicate the retention of a plesiomorphic condition ventrall surfaces of the thorax and abdomen. not found in other subgenera of Xylocopa. Schremmer postulated that pollen dust on the dor- Nest habits and body hair. Hairlessness in sal surfaces is scraped by the middle legs then trans- wood or stem nesting bees, such as Ceratina, Hy- ferred to the forelegs and mouthparts where it is laeus, enables them to easily move backward in the swallowed, while pollen dust on the bee’s ventral nest. Anzenberger (1977) observed that Xylocopa surfaces are brushed by the scopal hairs of the basi- with a hairy coat seldom crawled backwards. Pre- tarsus, where they remain and are carried back to sumably, the distal tibial spines on all pairs of legs in the nest. Schremmer was, furthermore, of the im- males and females assist in maneuvering inside the pression that European Xylocopa relied more on burrow. crop transport than Neotropical species. Proboscis as wedge. The functional morphol- Anzenberger’s (1977) observations on several ogy of the mouthparts were treated by Schremmer species of Xylocopaa in Tanzania revealed that pollen (1972). Like the bee itself, the proboscis of Xylocopa which is brushed from the head by the forelegs is is exceptionally robust. The galeae, in particular, swallowed and carried in the crop, while pollen are strongly sclerotized and interlock with each brushed by the midlegs is transferred to the scopae of other along a lonsamplegitudinal groove formed by the the hindle pagesgs. No midleg to foreleg transfer of pollen galeal velum and midrib. This is apparently com- was observed, as put forward in Schremmer (1972). mon to all species of Xylocopa and is not found to Furthermore, such pollen transfer is not reported to this degree in other bees. It is approached in some occur in the pollen collecting activities of other bees Melittidae, and particularly evident in Dasypoda ar- which have been closely examined (Michener, gentata ssp. hispanica. The stiff galeae in Xylocopa Winston & Jander 1978). are stable enough to pry open parts of a flower to Crop transport in Xylocopaa cannot be denied, gain access to nectar, as well as to pierce a hole in and indeed, museum species of Xylocopaa with pollen 254 John D. Plant and Hannes F. Paulus

laden hindlegs are generally rare. Nonetheless, I have observed laboratory-kept Xylocopaa (Ctenoxylocopa) sulcatipess eagerly collect pollen from a dish onto their hindlegs. An increased reliance on crop transport of pollen may favor the social interactions of the mother bee with her juvenile offspring in the nest. In some species of the genus, the mother under certain cir- cumstances remains in the nest along with her prog- eny. In this situation, she forages while the young remain in the nest. Upon return they solicit her to be fed by mouth to mouth food transfer (Anzen- berger 1977, Gerling, Hurd & Hefetz 1981, 1983).

Tribe Manueliini The tribe contains a single genus, Manuelia, with three species, from Chile and Argentina, two of which were examined. Synapomorphies of the Manueliini resulting Fig. 169: Molecular phylogeny of subgenera of Ceratina, after from the present study (Fig. 165, Node E): Base of Rehan et al. (2010, fig. 2) labrum elevated, also present in Xylocopa (character 29.2). Base of labial palpus segment I incised (character 123.1). Metanotum flat or slanting not more than 45 degrees (character 133.1). Jugal lobe of as phylogenetically intermediate between Xylocopini hindwing very short (character 144.3). Basitibial and Ceratinini. Daly (1985) placed Megaceratinaa in plate flange-like, lacking surface hairs and without the Ceratinini. carina margin (character 172.1). Apex of hind basi- In the first extensive phylogenetic study to ex- tarsus laterally offset and with short pointed process amine members of the tribe Ceratinini, Rehan et al. (also present in Manuelia) (character 188.1). Basitar- (2010) included 71 species from 15 subgenera in a sal scopal hairs plumose (character 180.2). Sternum molecular Bayesian analysis using data from se- 8 of male with single apical projection and lateral quences of two mitochondrial genes (COI, cyt B) arms (character 211.0). and one nuclear gene (F2 copy of EF-1α). Neocer- atinaa and Megaceratinaa appeared at the base of the tree (Fig. 169). Tribe Ceratinini Results of cladistic analysis. Representatives of The tribe contains one genus, Ceratina, which is two subgenera were included in the present analysis cosmopolitan in distribution with about 352 species (Euceratina, Simioceratina). Specimens of Megacer- in 22 subgenera. Some of the subgenera have been atinaa were not available for the present study. previously regarded as genera: Megaceratina (e.g. Hi- Synapomorphies of the Ceratinini include the rashima 1971; Daly 1985), Pithitiss (Hirashima following characters (Fig. 165, Node F): Hypostom- 1969; Daly 1983sample), Neoceratina (Michener 1944) al carina pages elevated (character 18.1). Inner process of and Simioceratina (Daly 1988). Until recently, the apical cardo curving inward (character 45.1). First subgenus Megaceratinaa with one species in tropical segment of labial palpus with membranous margin Africa was traditionally recognized at the generic (character 125.1). Scopa present on hind trochanter level. (character 170.1). Scopa present on hind femur Review of the phylogeny of the Ceratinini. (character 171.1). Basitibial plate scale-like and pro- Hirashima (1971) reported that Megaceratinaa pos- jecting, not at base of tibia but descended (character sesses an abdominal scopa and regarded the species 172.2). Evolution and Phylogeny of Bees 255

Other probable synapomorphies of Ceratinini Review of the phylogeny of the Allodapini. mentioned in the literature concern: (i) The presence Several cladistic studies have been devoted to the Al- of wax glands on S2 and S3 of females (Daly 1966, lodapini. The phylogeny of Allodapini was reviewed fig. 6, Sakagami & Michener 1987, char. 23). They by Tierney et al. (2008). are discernible as conspicuous crescent shaped areas. Michener (1977b) manually constructed a (ii) The strongly concave lateral margins of the cl- cladogram in consideration of 20 characters (11 lar- ypeus (Sakagami & Michener 1987, char. 2a). (iii) val, 4 morphological and 5 biological characters) and The abruptly narrowed shape of the mandible (Sak- 14 genera and subgenera of allodapine bees (Fig. agami & Michener 1987, char. 62) as opposed to 170 A). The information given in Michener tapering or the less abruptly narrowed condition in (1977b) was assembled into a data set and subjected the Allodapini. (iv) The lack of pygidial fimbria and to a computer assisted parsimony analysis in Nona; pygidial plate (Sakagami & Michener 1987, char- three most parsimonious trees were obtained (length acters 21, 22), which however are features largely 29, ci 75, ri 87). Only one largely corresponds to the similar to the Allodapini. cladogram presented by Michener (1977b, fig. 1). The consensus tree is shown in (Fig. 170 B). The cladistic analysis of Reyes (1998, cited in Tribe Allodapini Reyes, Cooper & Schwarz 1999) was based on 22 The tribe Allodapini contains about 235 species characters (9 larval, 10 adult morphology, and 3 be- in 14 genera. Most are distributed throughout south- havioral). Common to both studies is the monophy- ern Africa, Madagascar, the Oriental region and Aus- ly and basal position of the clade (Compsomelissaa + tralia. They are characterized by several distinctiven- Halterapiss) (Fig. 171 A). esting and biological features. They range from Bull, Schwarz & Cooper (2003) conducted solitary to subsocial and eusocial, and the larvae are an analysis in consideration of two mitochondrial progressively fed (Michener 1969), as opposed to genes (COI, cyt B) and one nuclear gene (F2 copy of mass provisioning which is typical for most bees. EF-1α) on 28 species of Allodapini (Fig. 171 B). No Various classifications systems of the Allodapini are members of the Allodapulaa group were included. compared in Table 38. Schwarz et al. (2006) utilized sequence data from two mitochondrial genes (COI, cyt b) and one nuclear gene (F2 copy of EF-1α) to analyze the phylogenetic relationships of the Allodapini (Fig. 171 Table 38: Classification of the Allodapini at the generic level. C). The study postulated that the Allodapini origi- MICHENER (1975) REYES (1998) MICHENER (2007) nated in Africa, and suggested that the Exoneura Compsomelissa Compsomelissa Compsomelissa Group reached Australia by migrating across the In- Halterapis Halterapis* dian Ocean on islands that no longer exist. Possible Exoneura Exoneura Exoneura dispersal routes via southern Asia or Antarctica were Brevineura discounted. Inquilina Inquilina Michener (2007: 628) regarded Halterapiss as a Exoneurella Exoneurella Exoneurella subgenus off Compsomelissa. However, more recently, Exoneuridia Exoneuridia Exoneuridia the species of subgenus from Madagascar were split Macrogalea Macrogalea Macrogalea off and placed in a new genus, Hasinamelissa, by Allodapula Allodapula Allodapula Chenoweth et al. (2008). Dalloapula Allodapulodes Smith et al. (2007) conducted a phylogenetic sampleanalysis ofpages the Allodapini using sequences of two mi- Eucondylops Eucondylops Eucondylops Braunsapis Braunsapis Braunsapis tochondrial genes (COI, cyt B) and one nuclear gene Effractapis** Effractapis (F2 copy of EF-1α). Results of the Bayesian analysis Nasutapis Nasutapis Nasutapis of 48 allodapine species are summarized at the generic Allodape Allodape Allodape and subgeneric level in Fig. 172 A. Macrogaleaa was * Species from Madagascar formerly placed in Halterapiss have been removed recognized at the base of the tribe followed by Exoneu- to a new genus, Hasinamelissaa (Chenoweth et al. 2008). ** Effractapiss was described in Michener (1977a) and is therefore absent in ra (sensu Michener 2007). The parasitic genus Nas- the first column. utapiss was nested within species of Braunsapis. Zoologica, Volume 161, 2016 John D. Plant & Hannes F. Paulus: Evolution and Phylogeny of Bees

Volume 161 of Zoologica reviews and analyses tested anew using an extensive dataset of selected the evolution and phylogeny of bees. morphological features. The study uses all com- It is subdivided into two parts. mon and current computer-aided techniques of Part One – A Preamble to the Evolution and Phy- cladistic analysis (parsimony, successive/implied logeny of Bees provides a complete and critical weight, Bayesian and neighbor-joining), which are review of all previous attempts to reconstruct the applied to representatives of all seven families, 22 phylogenetic tree of bees (Anthophila / Apiformes) subfamilies and 48 of 58 tribes of bees. The con- based on morphological, bionomic or molecular clusions drawn from this are evaluated for the ma- approaches and presented in chronological se- jor groups (i.e., short-tongued and long-tongued quence up to and including recent publications. bees), as well as separately for the families, sub- At the same time, the introductory part examines families and tribes in each case. trends in the classification of bees and compares In a world currently dominated by molecular ge- available hypotheses of bee evolution. Part One netic approaches to phylogeny, this study clearly closes with a family-wise delineation of the fossil demonstrates that it is not anachronistic to engage history of bees. in morphological efforts, because progress can be Part Two – A Phylogenetic Study of Bees in Light significantly advanced and the pool of available of Morphological Evidence adds an experimental scientific arguments enriched. The diversity of the study to complement the bibliographical analysis object of investigation justifies a variety of meth- provided in Part One. The phylogenetic relation- ods. ships of the larger taxonomic units of bees are

This monograph is a much needed reference work of high practical value for all students of bee evolution, phylogeny and morphology. Further, it is ideally suited as good introductory reading material for university level students.

www.schweizerbart.de ISSN 0044-5088 ISBN 978-3-510-55048-7 Zoology 2016 E Zoologica vol. 161

John D. Plant and Hannes F. Paulus Evolution and Phylogeny of Bees Review and Cladistic Analysis in Light of Morphological Evidence (Hymenoptera, Apoidea) 2016. III, 364 pages, 232 gures, 49 tables, hardcover, 23 x 32 cm (Zoologica, Vol. 161) ISBN 978-3-510-55048-7 149.– € www.schweizerbart.com/9783510550487

Volume 161 of Zoologica reviews and analy- Part Two – A Phylogenetic Study of Bees in separately for the families, subfamilies and ses the evolution and phylogeny of bees. Light of Morphological Evidence adds an tribes in each case. experimental study to complement the bib- It is subdivided into two parts. In a world currently dominated by molecular liographical analysis provided in Part One. Part One – A Preamble to the Evolution and genetic approaches to phylogeny, this study The phylogenetic relationships of the larger Phylogeny of Bees provides a complete and clearly demonstrates that it is not anachronis- taxonomic units of bees are tested anew us- critical review of all previous attempts to re- tic to engage in morphological efforts, because ing an extensive dataset of selected morpho- construct the phylogenetic tree of bees (An- progress can be significantly advanced and the logical features. The study uses all common thophila / Apiformes) based on morphological, pool of available scientific arguments enriched. and current computer-aided techniques of bionomic and molecular approaches and pre- The diversity of the object of investigation justi- cladistic analysis (parsimony, successive/im- sented in chronological sequence up to and in- fies a variety of methods. plied weight, Bayesian and neighbor-joining), cluding recent publications. At the same time, which are applied to representatives of all This monograph is a much needed reference the introductory part examines trends in the seven families, 22 subfamilies and 48 of 58 work of high practical value for all students classification of bees and compares available tribes of bees. The conclusions drawn from of bee evolution, phylogeny and morphology. hypotheses of bee evolution. Part One closes this are evaluated for the major groups (i.e., Further, it is ideally suited as good introductory with a family-wise delineation of the fossil his- short-tongued and long-tongued bees), and reading material for university level students. tory of bees.

Table of contents Part II: A Phylogenetic Study of Bees Family Colletidae ...... 202 in Light of Morphological Evidence ...... 99 Family Melittidae ...... 218 Abstract ...... 1 Introduction ...... 99 Long-Tongued Bees ...... 229 Zusammenfassung ...... 2 Methods ...... 99 Family Megachilidae ...... 231 Part I: A Preamble to the Evolution and Species Investigated ...... 108 Family Apidae ...... 244 Phylogeny of Bees ...... 4 List of Characters ...... 108 Summary ...... 317 ntroduction ...... 4 Data Matrix ...... 143 Acknowledgements ...... 327 Trends in Bee Classification ...... 7 Results and Discussion ...... 143 References ...... 327 Theories on the Evolution of Bees ...... 16 Statistical Results and Cladograms 1. . . . .43 Appendix A: Wasp Ancestry and Bee Classification . . .35 Major Divisions of Bees ...... 174 Family-Group Names of Bees ...... 359 Morphological Phylogeny of Bees ...... 50 Short-Tongued Bees ...... 175 Appendix B: Molecular Phylogeny of Bees ...... 66 Family Halictidae ...... 177 Description of New Family-Group Parasitic Bees ...... 78 Family Andrenidae ...... 187 Names ...... 362 Antiquity of Bees ...... 78 Family Stenotritidae ...... 201

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