(PDF) Phylogeny of colletid bees (Hymenoptera: Colletidae) inferred from four nuclear genes - DOKUMEN.TIPS (2024)

(PDF) Phylogeny of colletid bees (Hymenoptera: Colletidae) inferred from four nuclear genes - DOKUMEN.TIPS (1)

Molecular Phylogenetics and Evolution 50 (2009) 290–309

Contents lists available at ScienceDirect

Molecular Phylogenetics and Evolution

journal homepage: www.elsevier .com/locate /ympev

Phylogeny of colletid bees (Hymenoptera: Colletidae) inferredfrom four nuclear genes

Eduardo A.B. Almeida a,b,*, Bryan N. Danforth a

a Cornell Univ., Dept. Entomol., Ithaca, NY 14853, USAb Depto. de Zoologia, Universidade Federal do Paraná, Lab. Biol. Comparada Hymenoptera, Caixa Postal 19020, CEP 81531-980, Curitiba, Paraná, Brazil

a r t i c l e i n f o

Article history:Received 8 May 2008Revised 12 August 2008Accepted 23 September 2008Available online 22 October 2008

Keywords:ColletidaeBee phylogenyMolecular phylogenyMolecular evolutionGondwanaSystematics

1055-7903/$ - see front matter � 2008 Elsevier Inc. Adoi:10.1016/j.ympev.2008.09.028

* Corresponding author. Address: Depto. de ZooloParaná, Lab. Biol. Comparada Hymenoptera, Caixa PCuritiba, Paraná, Brazil. Fax: +55 41 3361 1763.

E-mail address: [emailprotected] (E.A.B. Alm

a b s t r a c t

Colletidae comprise approximately 2500 species of bees primarily distributed in the southern continents(only two colletid genera are widely distributed: Colletes and Hylaeus). Previously published studies havefailed to resolve phylogenetic relationships on a worldwide basis and this has been a major barrier to theprogress of research regarding systematics and evolution of colletid bees. For this study, data from fournuclear gene loci: elongation factor-1a (F2 copy), opsin, wingless, and 28S rRNA were analyzed for 122species of colletid bees, representing all subfamilies and tribes currently recognized; 22 species belongingto three other bee families were used as outgroups. Bayesian, maximum likelihood, and parsimony meth-ods were employed to investigate the phylogenetic relationships within Colletidae and resulted in highlycongruent and well-resolved trees. The phylogenetic results show that Colletidae are monophyletic andthat all traditionally recognized subfamilies (except Paracolletinae) are also strongly supported as mono-phyletic. Our phylogenetic hypothesis provides a framework within which broad questions related to thetaxonomy, biogeography, morphology, evolution, and ecology of colletid bees can be addressed.

� 2008 Elsevier Inc. All rights reserved.

1. Introduction

Colletidae are generally considered to constitute the most an-cient bee lineage, i.e., the sister-group to all other bees (e.g., Mich-ener, 1944, 1974, 1979; O’Toole and Raw, 1991; Engel, 2001). Thishypothesis is not ubiquitous, though, and its validity has beenquestioned (e.g., McGinley, 1980; Michener, 2007; Danforthet al., 2006a,b). The most comprehensive studies of bee phylogenywere those by Alexander and Michener (1995) and Danforth et al.(2006b). Alexander and Michener (1995) analyzed a morphologicalmatrix of adult and larval characters based on weighted and un-weighted parsimony. Their data firmly established the monophylyof many bee families, but their results were inconclusive about theoverall relationships among families. Tree topologies varied widelywith different analytical methods and nodal support was weak,especially at the base of the tree. Danforth et al. (2006b) incorpo-rated data from five nuclear genes and analyzed the data sepa-rately and in combination with Alexander and Michener’smorphological matrix. Their results strongly pointed to the rootof the bee clade being positioned among the lineages of ‘‘Melitti-dae” (sensu lato). Colletidae were placed far from the root nodeand statistical tests suggested that a basal placement of Colletidae

ll rights reserved.

gia, Universidade Federal doostal 19020, CEP 81531-980,


was significantly incongruent with the data (Danforth et al.,2006b).

1.1. Colletid monophyly

Some of Alexander and Michener’s (1995) analyses did notstrongly support the monophyly of Colletidae, even though thereare a number of unique traits, which appear to be synapomorphiesfor this family. The cellophane-like cell lining (e.g., Hefetz et al.,1979; Espelie et al., 1992; reviewed by Almeida, 2008a) has beenconsidered to be the strongest evidence for monophyly of the fam-ily because it is a unique and unreversed character found onlyamong colletid bees. McGinley (1980) presented a list of potentialsynapomorphies from mouthpart morphology. The most recentevidence for the monophyly of this family was given by a molecu-lar character: the presence of a unique intron in the F1 copy of thegene elongation factor-1a in all colletids sampled, but not inStenotritidae or any other bee family (Brady and Danforth, 2004).Additionally, Colletidae have been consistently recovered as astrongly supported monophyletic group based on several indepen-dent molecular data sets (Danforth et al., 2006a,b).

1.2. Diversity and classification of Colletidae

The Colletidae, as considered here, are currently divided into se-ven subfamilies: Colletinae, Euryglossinae, Hylaeinae, Paracolleti-


(PDF) Phylogeny of colletid bees (Hymenoptera: Colletidae) inferred from four nuclear genes - DOKUMEN.TIPS (2)





Colletinae s.str.







Colletinae s.str.








Colletinae s.str.Callomelitta (Paracolletinae)Paracolletinae (part)

EuryglossinaeScrapter (Paracolletinae)HylaeinaeXeromelissinae

other bee families






c d




Colletinae s.str.






Fig. 1. Historical account of attempts to describe relationships among subfamiliesand tribes of colletid bees as shown in summary trees of: (a) Michener (1944, p.230); (b) Michener (1974, p. 23); (c) Engel (2001, p. 156); (d) Alexander andMichener (1995, p. 398), consensus of four trees resulting from the analysis of thecomplete data set using implied weights parsimony. The African genus Scrapterused to be considered part of Paracolletinae when these four hypotheses werepresented. Stenotritidae is also included in the figures because, historically, it hasbeen considered to be part of Colletidae by several authors.

E.A.B. Almeida, B.N. Danforth / Molecular Phylogenetics and Evolution 50 (2009) 290–309 291

nae, Scrapterinae, and Xeromelissinae. These subfamilies corre-spond to the five subfamilies recognized by Michener (2007), ex-cept that the three tribes of Colletinae: Colletini, Paracolletini,and Scrapterini are treated as independent subfamilies. This classi-fication is also congruent with the classification by Melo and Gonç-alves (2005), except that those authors treat the subfamilies ofColletidae as tribes.

Colletid bees are diverse, ranging from small, slender, relativelyhairless bees (such as Euryglossinae) to large, robust, hairy bees(such as Diphaglossinae). Females carry pollen either externally,in a well-developed trochanteral and femoral scopa (Colletinaeand Diphaglossinae) or a scopa formed by sparse hairs on the hindlegs and long hairs primarily on the second abdominal sternum(Xeromelissinae); or internally in the crop (Euryglossinae, Hylaei-nae, and few Paracolletinae). There is only one known group of cle-ptoparasites (some Hawaiian species of the Hylaeus (Nesoprosopis)Perkins [Daly and Magnacca, 2003]). Floral relationships in Collet-idae range from polylectic (generalist) to oligolectic (specialist),with some taxa showing very narrow host-plant preferences(e.g., Wcislo and Cane, 1996). The highest diversity of colletid beesis observed in the temperate parts of southern South America andin Australia. Worldwide, there are 2485 available species names inColletidae (Ascher et al., 2008).

The Colletinae are widely distributed (they do not occur inAustralia, though) and comprise approximately 480 species. Col-letinae are morphologically hom*ogenous compared to theremainder of Colletidae, and their body size varies from 7 to16 mm in length. The Diphaglossinae include the largest colletidbees (up to 24 mm in length). These Neotropical bees are, ingeneral, fast flying, and many of them fly only early in the morn-ing or before and around dusk. There are 128 available speciesnames. This is the only colletid subfamily subdivided into tribes,and Michener (1986) resolved the tribal relationships as follows:(Caupolicanini, (Diphaglossini, Dissoglottini)). The Euryglossinaeare a subfamily occurring mostly in the Australian Region (onespecies has been introduced in South Africa) and comprise small,hairless bees. There are almost 400 species of Euryglossinae. TheHylaeinae comprise more species than any other subfamily ofColletidae, with about 900 available names. Morphological andtaxonomic diversity is highest in Australia where the group isthought to have originated; all species occurring outside theAustralian region belong in the genus Hylaeus. Their wasp-likeappearance and lack of external pollen-carrying structures madeHylaeinae candidates for the most primitive bees (e.g., Jander,1976; Michener, 1979; see also discussion in Michener, 2007,88–92). Females of Euryglossinae also lack pollen-carrying struc-tures (i.e., a scopa) and transport pollen internally. The Paracol-letinae are a morphologically diverse group of bees that rangesin size from 6 to 18 mm in length and there are over 400 de-scribed species, distributed throughout the Australian and Neo-tropical regions, mainly in subtropical and temperate drybiomes. The Scrapterinae are a monogeneric subfamily compris-ing 40 species of the endemic African genus Scrapter, most ofwhich are distributed in southern Africa, especially the Cape re-gion. One species was recently described from Kenya (Davieset al., 2005). Host-plant preferences and adult morphology arequite variable within this group of bees; body length varies from3.5 to 14 mm in length (Davies and Brothers, 2007). Research onthe taxonomy and biology of Scrapter (Rozen and Michener,1968; Eardley, 1996; Davies et al., 2005; Davies and Brothers,2007) makes it one of the best-studied groups of Colletidae. Un-til recently, Scrapter was considered as part of Paracolletinae. TheXeromelissinae are small, slender, and not very hairy, eventhough they have a small scopa on the hind leg and metasoma.Body length varies from 2.5 to 7.0 mm in length. There are al-most 120 described species with the highest diversity in temper-

ate regions of Chile and Argentina, but the group extendsthrough the Neotropical Region as far north as Mexico. Packer(2008) and Almeida et al. (2008) present results of two phyloge-netic studies of Xeromelissinae based on morphology and com-bined morphological and molecular data, respectively.

Although the composition of colletid subfamilies is largely set-tled, relationships among them are poorly understood. One of thefew points of agreement regarding the phylogenetic affinities with-in Colletidae is the grouping of Euryglossinae, Hylaeinae, and Xer-omelissinae. A graphical summary of four hypotheses of colletidphylogeny is presented in Fig. 1.

Alexander and Michener (1995) investigated the relationshipsamong the main lineages of bees based on a morphological dataset of adult and larval characters. Although a large number ofcolletid species were included in their analyses, the conclusionsone can draw from their results are limited by the extremelyvariable positioning of the groups depending on the way datawere analyzed. A summary of one of the consensus trees pre-sented by Alexander and Michener (1995) is shown in Fig. 1d.Examination of previous hypotheses of relationships among lin-eages of Colletidae based either on taxonomic experience andintuition of bee researchers (Fig. 1a–c), or on explicit data anal-ysis (Fig. 1d) reveals great uncertainty surrounding the relation-ships within this family.

The purpose of this study is to re-assess the phylogenetic rela-tionships within Colletidae. This was done using a novel source ofdata for this group: genetic sequence data from four nuclear geneloci. A better understanding of colletid phylogeny is essential forproviding the rationale of an improved classification of these bees,as well as for the reconstruction of their evolutionary and biogeo-graphical history.

(PDF) Phylogeny of colletid bees (Hymenoptera: Colletidae) inferred from four nuclear genes - DOKUMEN.TIPS (3)

292 E.A.B. Almeida, B.N. Danforth / Molecular Phylogenetics and Evolution 50 (2009) 290–309

2. Materials and methods

2.1. Taxon sampling

We assembled a data set that comprises a total of 144 terminalspecies; 122 species of Colletidae were sampled to represent alltraditionally accepted subfamilies and tribes of this family. Specialattention was paid to the Colletinae s.l. (sensu Michener, 2007; i.e.,Colletinae + Paracolletinae + Scrapterinae) because it is widely be-lieved to be para- or polyphyletic. Eighty species of Colletinae s.l.were included in the analysis (15 Colletinae s.str., 60 Paracolleti-nae, and 5 Scrapterinae). The remaining 42 species included repre-sentatives of the three tribes of Diphaglossinae [Caupolicanini (9spp.), Diphaglossini (4 spp.), and Dissoglottini (2 spp.)]; Eurygloss-inae (6 spp.); Hylaeinae (11 spp.); and Xeromelissinae (8 spp.).

Twenty-two representatives of three bee families were used asoutgroups for this analysis: Andrenidae (8 spp.), Halictidae (10spp.), and Stenotritidae (4 spp.). These represent the main lineagesof bees closely related to Colletidae according to the results of Dan-forth et al. (2006a,b). This choice of outgroups does not imply anagreement with a given placement of Colletidae relative to otherbee lineages. The analysis of a very similar molecular data set withtaxon sampling that intended to resolve the relationships amongbee families resulted in the following arrangement for the closestgroups to Colletidae: (Andrenidae (Halictidae (Colletidae, Stenotri-tidae))) (Danforth et al., 2006b). This means that the relationshipsamong bee families based on a data set of this sort are well-estab-lished. The purpose of outgroups is to establish the position of theingroup root node, and Andrenidae, Halictidae, and Stenotritidaeshould provide sufficient information for rooting Colletidae. Evenif Colletidae are indeed the earliest lineage of bees, the outgroupchoice still remains unproblematic. In Nixon and Carpenter’s(1993, 423) words: ‘‘[o]utgroup(s) need not be ‘‘primitive” relativeto the ingroup”.

Specimens used for sequencing were primarily preserved in 95%EtOH but recently collected pinned specimens and frozen speci-mens were also used. Pinned specimens older than 3–5 years werenot suitable for DNA extractions but those collected more recentlyprovided good quality, high-molecular weight DNA for PCR. Out-group and ingroup taxa included in this study, locality data, spec-imen voucher numbers, and GenBank Accession Nos. are listed inTable 1. The detailed generic classification adopted in this studyis presented in Appendix 1 (Supplementary materials). Voucherspecimens are housed in the Cornell University Insect Collectionor at the institutions that provided specimens for DNA extractions.Identification of various taxa included in the analyses was facili-tated by comparison to material deposited in entomological collec-tions and assistance of other bee taxonomists, especially J.S. Ascher(American Museum of Natural History, USA), T. Houston (WesternAustralian Museum, Australia), M. Kuhlmann (University of Muen-ster, Germany), G.A.R. Melo (Universidade Federal do Paraná, Bra-zil), and L. Packer (York University, Canada).

2.2. Data

Molecular data were collected from four nuclear loci that havebeen providing robust results for insect phylogenetic studies. Threeof them are nuclear protein-coding genes: EF-1a (elongation fac-tor-1a, F2 copy), opsin (long wavelength, green rhodopsin), andwingless (wg), and the fourth is a nuclear ribosomal RNA locus:the D1–D5 expansion regions and related core elements of thelarge subunit 28S rRNA (28S rRNA). Maps of the four gene lociand the relative positions of the primers used in this study areshown in Fig. 2, and primer information for each gene can be foundin Table 2. Each of these gene loci is referred to as a partition here-

after; introns and exons of EF-1a are treated as two separate par-titions. Five partitions are therefore recognized: exons and intronsof EF-1a, opsin (exons), wg (exons), and 28S rRNA.

Slowly evolving, nuclear genes are commonly used for phyloge-netic analysis in many groups of insects. They have been demon-strated to recover Cretaceous-age divergences (e.g., Danforthet al., 1999, 2004, 2006a,b; Wiegmann et al., 2000). Danforthet al. (2004, 310–311) reviewed the phylogenetic utility of EF-1a,opsin, and wg, and commented on the biological functions of theirgene products. Among these genes, EF-1a has been the mostwidely used nuclear protein-coding gene for insect phylogenetics.Despite alignment challenges of some ribosomal DNA regions,these genes cannot be distinguished from protein-coding genesregarding phylogenetic utility and nucleotide substitution patterns(Danforth et al., 2005). Among the various ribosomal gene loci, 18SrRNA tends to have the slowest rate of substitution (Hillis and Dix-on, 1991), while 28S rRNA has more variation and, therefore, morephylogenetic signal.

The three protein-coding genes used here comprised the dataset used by Danforth et al. (2004) to assess phylogenetic relation-ships within Halictidae, except that the exon of wg sampled for thepresent study is approximately 250 bp longer on the upstream (i.e.,50 end, Sipes, personal communication). The data set of Danforthet al. (2004) was robust enough to resolve relationships amonghalictid bees. Halictidae and the clade formed by Colletidae andStenotritidae are presumably roughly the same age, both havingoriginated between mid- and late-Cretaceous, are closely related,and have approximately the same species diversity. This providesthe basis for the initial assumption that this molecular data setshould have enough phylogenetic signal to resolve relationshipswithin either family.

2.3. DNA extraction

Genomic DNA was extracted using phenol–chloroform proto-cols (Doyle and Doyle, 1990, adapted by Danforth, 1999), but with-out use of liquid nitrogen and RNase. Tissue was taken from thethoracic musculature and/or legs depending on the rarity and sizeof available specimens. Samples were (1) macerated in individual1.5 ml Eppendorf tubes with 2� CTAB extraction buffer and100 mg Proteinase K; (2) incubated for 2–4 h at 55 �C; (3) extractedwith 24:1 chloroform–isoamyl alcohol, (4) extracted again with25:24:1 phenol–chloroform–isoamyl alcohol; and (5) 24:1 chloro-form–isoamyl alcohol.

The phenol–chloroform–isoamyl alcohol stage was performedin Phase-Lock Gel� 2.0 ml Eppendorf tubes to facilitate the separa-tion of phenol from the remainder and thus increase the final DNAyield. DNA was (1) precipitated with 2.5 volumes of ice-cold 100%ethanol and 0.1 volume 3 M sodium acetate; (2) washed with 80%ethanol; and (3) resuspended in 50 ml Tris–EDTA (pH 7.6) buffer.

2.4. PCR and sequencing

PCR amplifications of the genes listed above were done for 35cycles under the following conditions: an initial denaturation at94 �C for 60 s, followed by 35 cycles of denaturation at 94 �C for60–90 s, annealing at 48–58 �C, 60–90 s, and extension at 72 �C,60–90 s. Specific conditions for each locus amplified are listed inTable 2. Prior to sequencing, most PCR products were gel-purifiedin low melting point agarose gels (FMC, Rockland, Maine) over-night at 4 �C. DNA was recovered from gel slices using the PromegaWizard PCR Preps DNA Purification kit. Gel purification was unnec-essary for PCR products that produced a single product: both frag-ments of 28S rRNA and the upstream (1100 bp) fragment of EF-1a.Automatic DNA sequencing was performed using the Applied Bio-systems Automated 3730 DNA Analyzer employing Big Dye Termi-

(PDF) Phylogeny of colletid bees (Hymenoptera: Colletidae) inferred from four nuclear genes - DOKUMEN.TIPS (4)

Table 1List of species included in this study, taxonomic information, locality data, and GenBank Accession nos.

Species [voucher code] Classification Collecting data EF-1a Opsin Wingless 28S rRNA

Colletes bicolor Smith, 1879 [EA0082] Colletidae:Colletinae

Argentina: Tucumán. Amaicha del Valle.24.x.2004

DQ884650 DQ884549 DQ884802 DQ768539

Colletes compactus Cresson, 1868 [EA0014] Colletidae:Colletinae

USA: New York. Tompkins Co., Ithaca.29.ix.1998

DQ884642 DQ884542 DQ884794 DQ768531

Colletes distinctus Cresson, 1868 [EA0013]b Colletidae:Colletinae

USA: California. SC: Berkeley Co., Honey Hill.27.ii.2000

DQ884641 — DQ884793 DQ768530

Colletes floralis Eversmann, 1852 [EA0076] Colletidae:Colletinae

Mongolia: Arkhangay Aimag. 10.vii. 2004 DQ884649 DQ884548 DQ884801 DQ768538

Colletes furfuraceus Holmberg, 1886 [EA0108] Colletidae:Colletinae

Argentina: Prov. Tucumán. Amaicha del Valle.25–26.x.2004

DQ884651 DQ884550 DQ884803 DQ768540

Colletes gilvus Vachal, 1909 [EA0073] Colletidae:Colletinae

Chile: Region I. Murmuntani (near Putre).Iv.2004

DQ884648 DQ884547 DQ884800 DQ768537

Colletes inaequalis Say, 1837 [Coin450] Colletidae:Colletinae

USA: NY. Tompkins Co., Ithaca AY585123 DQ115542 DQ884804 AY654484

Colletes pascoensis co*ckerell, 1898 [EA0015] Colletidae:Colletinae

USA: California. Contra Costa Co., El Cerrito.14.iv.2001

DQ884643 — DQ884795 DQ768532

Colletes seminitidus Spinola, 1851 [EA0045] Colletidae:Colletinae

Chile: Region IV. PanAm N Los Hornos. 9.x.2002 DQ884647 DQ884546 DQ884799 DQ768536

Colletes simulans Cresson, 1868 [EA0016] Colletidae:Colletinae

USA: New York. Tompkins Co., Ithaca.21.viii.1997

DQ884644 DQ884543 DQ884796 DQ768533

Colletes skinneri Viereck, 1903 [Cosk632] Colletidae:Colletinae

USA: AZ. Cochise Co., Chiricahua Monument.14.ix.1999

AY230130 AY227912 DQ884805 AY654485

Colletes thoracicus Smith, 1853 [EA0017] Colletidae:Colletinae

USA: Florida. Alachua Co., Gainsville.15.iii.2002

DQ884645 DQ884544 DQ884797 DQ768534

Hemicotelles ruizii (Herbst, 1923) [EA0032] Colletidae:Colletinae

Chile: Region IV. El Equi, Las Placetas.14.x.2001

DQ884638 DQ884539 DQ884790 DQ768527

Rhynchocolletes mixtus (Toro and Cabezas, 1977)[EA0033]


Chile: Region IV. Pejerreyes. 19.x.2001 DQ884639 DQ884540 DQ884791 DQ768528

Xanthocotelles sicheli (Vachal, 1909) [EA0056] Colletidae:Colletinae

Chile: Region VII. Curicó, Laguna de Teno. 1–5.ii.2003

DQ884640 DQ884541 DQ884792 DQ768529

Caupolicana bicolor Friese, 1899 [EA0041] Colletidae:Diphaglossinae

Chile: Region II. Huasco, 4 km N Domeyko.10.xi.2000

DQ884576 DQ884484 DQ884718 DQ768465

Caupolicana quadrifasciata Friese, 1898 [EA0040] Colletidae:Diphaglossinae

Chile: Region IV. Fray Jorge Pq. Ntl. 11.x.2001 DQ884575 DQ884483 DQ884717 DQ768464

Caupolicana vestita (Smith, 1879) [Cpve848] Colletidae:Diphaglossinae

Chile: Region I. Arica Playa las Machas. AY585124 DQ115543 DQ884726 DQ872758

Caupolicana yarrowi (Cresson, 1875) [Cpya654] Colletidae:Diphaglossinae

USA: NM. Hidalgo Co., 20 mi S. Animas.24.ix.1999

— DQ115544 DQ884727 AY654487

Ptiloglossa sp. [EA0018] Colletidae:Diphaglossinae

Costa Rica: Prov. Guanacaste, Carmona.15.i.2003

DQ884573 DQ884481 DQ884715 DQ768462

Ptiloglossa tarsata (Friese, 1900) [EA0085] Colletidae:Diphaglossinae

Argentina: Salta. General Güemes. 11.xi.2004 DQ884581 DQ884488 DQ884723 DQ768470

Ptiloglossa thoracica (Fox, 1895) [EA0078] Colletidae:Diphaglossinae

Mexico: Jalisco. Res. Chamela. 06.ix.2004 DQ884579 — DQ884721 DQ768468

Willinkapis chalybaea (Friese, 1906) [EA0118] Colletidae:Diphaglossinae

Argentina: Catamarca. 40 km N Andalgalá.15.ii.2003

DQ884582 DQ884489 DQ884724 DQ768471

Zikanapis clypeata (Smith, 1879) [EA0119] Colletidae:Diphaglossinae

Mexico: Jalisco. Res.Biosfera (Manantlan).11.ix.2004

DQ884583 DQ884490 DQ884725 DQ768472

Cadeguala albopilosa (Spinola, 1851) [EA0036] Colletidae:Diphaglossinae

Chile: Region VIII. Cordillera, El Manzano.xii.2001

DQ884574 DQ884482 DQ884716 DQ768463

Cadeguala occidentalis (Haliday, 1836) [EA0047] Colletidae:Diphaglossinae

Chile: Region V. Colliguay. 19.x.2002 DQ884577 DQ884485 DQ884719 DQ768466

Cadegualina andina (Friese, 1925) [EA0048] Colletidae:Diphaglossinae

Colombia: Boyacá. El Níspero. 12.xii.2001-19.i.2002

DQ884578 DQ884486 DQ884720 DQ768467

Diphaglossa gayi Spinola, 1851 [Diga850] Colletidae:Diphaglossinae

Chile: Region X. Aquas Calientes. AY585125 DQ115545 DQ884728 DQ872759

Mydrosoma aterrimum (Friese, 1925) [EA0156] Colletidae:Diphaglossinae

Bolivia: La Paz, Prov. Coroico, Cerro Uchumachi.05.iv.2004

EF032902 EF032903 EF032905 EF028342

Mydrosoma fallax (Moure, 1953) [EA0081] Colletidae:Diphaglossinae

Argentina: Salta. General Güemes. 11.xi.2004 DQ884580 DQ884487 DQ884722 DQ768469

Callohesma calliopsella (co*ckerell, 1910) [Euca688] Colletidae:Euryglossinae

Australia: Victoria. Yan yaen. 20.xi.1999 AY585126 DQ115550 DQ884809 DQ872768

Euhesma aff. crabronica (co*ckerell, 1914) [EA0155] Colletidae:Euryglossinae

Australia: WA; Eurardy Stat. 09.x.2005 DQ884654 — DQ884808 DQ768543

Euhesma platyrhina (co*ckerell, 1915) [EA0148] Colletidae:Euryglossinae

Australia: WA; Kalbarri Ntl.Prk. 08.x.2005 DQ884652 — DQ884806 DQ768541

Euhesma sp. [EA0149] Colletidae:Euryglossinae

Australia: WA. 15 km ESE Southern Cross.23.ix.2005

DQ884653 — DQ884807 DQ768542

Euryglossina globuliceps (co*ckerell, 1918)[Eugl692]


Australia: Victoria. Colquhuon State Forest.26.xi.1999

AY585127 DQ115551 DQ884810 DQ872769

Xanthesma furcifera (co*ckerell, 1913) [Xnfu709] Colletidae:Euryglossinae

Australia: Victoria. Patchewollock. 10.xii.1999. AY585140 DQ115552 DQ884811 DQ872770

Amphylaeus (Agogenohylaeus) obscuriceps (Friese,1924) [KM264]


Australia: Queensland. Kawana Waters.10.xii.2002

DQ884687 DQ884564 DQ884857 DQ768597

Hylaeus (Euprosopis) disjunctus (co*ckerell, 1905)[KM252]


Australia: Queensland. Somerset Dam.14.xii.2002

DQ884677 DQ884563 DQ884848 DQ768586

(continued on next page)

E.A.B. Almeida, B.N. Danforth / Molecular Phylogenetics and Evolution 50 (2009) 290–309 293

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Table 1 (continued)

Species [voucher code] Classification Collecting data EF-1a Opsin Wingless 28S rRNA

Hylaeus (Euprosopis) elegans (Smith, 1853)[Hyel697]


Australia: South Australia. 10 km E Kimba.5.i.1999

AY585129 DQ115547 DQ884839 DQ872778

Hylaeus (Gnathoprosopis) amiculus (Smith, 1879)[Hyam698]


Australia: South Australia. 10 km E Kimba.5.i.1999

AY585128 DQ115546 DQ884838 DQ872777

Hylaeus (Macrohylaeus) alcyoneus (Erichson, 1842)[EA0129]


Australia: WA; Badgingarra Ntl.Prk. 11.x.2005 DQ884668 DQ884562 DQ884837 DQ768577

Hylaeus (Pseudhylaeus) aff. simplus Houston, 1993[EA0125]


Australia: WA; Boorabbin Ntl.Prk. 26.ix.2005 DQ884664 DQ884561 DQ884833 DQ768573

Hylaeus (Rhodohylaeus) proximus (Smith, 1879)[Hypr699]


Australia: South Australia. 10 km E Kimba.5.i.1999

AY585130 DQ115548 EF032906 DQ872779

Hyleoides concinna (Fabricius, 1775) [KM268] Colletidae:Hylaeinae

Australia: Queensland. South of Eukey.18.xii.2002

DQ884691 DQ884560 DQ884861 DQ768601

Meroglossa itamuca (co*ckerell, 1910) [KM271] Colletidae:Hylaeinae

Australia: Queensland. Noosa North Shore.10.i.2003

DQ884694 DQ884565 DQ884863 DQ768604

Palaeorhiza (Heterorhiza) sp. [KM275] Colletidae:Hylaeinae

Australia: Queensland. Kuranda. O4.i.2003 DQ884697 DQ884566 DQ884867 DQ768608

Palaeorhiza (Palaeorhiza) sp. [KM276] Colletidae:Hylaeinae

Australia: Queensland. Kawana Waters.10.xii.2002

DQ884698 DQ884567 DQ884868 DQ768609

Andrenopsis sp. [EA0094] Colletidae:Paracolletinae

Australia: WA; �18.4 km NE Menzies.24.ix.2005

DQ884624 DQ884529 DQ884772 DQ768513

Anthoglossa sp. [EA0115] Colletidae:Paracolletinae

Australia: WA; Boorabbin Ntl.Prk.25.ix.2005 DQ884585 DQ884492 DQ884730 DQ768474

Anthoglossa cfr. robustus (co*ckerell, 1929)[EA0116]


Australia: WA; Kalbarri Ntl.Prk. 08.x.2005 DQ884586 DQ884493 DQ884731 DQ768475

Baeocolletes minimus (Michener, 1965) [EA0095] Colletidae:Paracolletinae

Australia: WA; �72.6 km NE Menzies.27.ix.2005

DQ884608 DQ884514 DQ884756 DQ768497

Baeocolletes sp. [EA0096] Colletidae:Paracolletinae

Australia: WA; Eurardy Station. 09.x.2005 DQ884609 — DQ884757 DQ768498

Belopria nitidior Moure, 1956 [EA0027] Colletidae:Paracolletinae

Brazil: Paraná. 15 km S Bocaiúva do Sul.12.ix.2002

DQ884593 DQ884500 DQ884739 DQ768482

Brachyglossula communis Trucco-Aleman, 1999[EA0083]


Argentina: Catamarca. El Rodeo. 20.xi.2004 DQ884600 DQ884506 DQ884748 DQ768489

Callomelitta antipodes (Smith, 1853) [Cman687] Colletidae:Paracolletinae

Australia: NSW. Guyra, 74 km E. 5.xii.1999 AY585122 DQ115563 EF032907 DQ872767

Cephalocolletes isabelae Urban, 1995 [EA0012] Colletidae:Paracolletinae

Brazil: Santa Catarina. Laguna. 31.xii.2001. DQ884589 DQ884496 DQ884735 DQ768478

Cephalocolletes laticeps (Friese, 1906) [EA0086] Colletidae:Paracolletinae

Argentina: San Juan. 14 km W Media Agua.27.xi.2004

DQ884602 DQ884508 DQ884750 DQ768491

Chilicolletes delahozii (Toro, 1973) [Lesp568] Colletidae:Paracolletinae

Chile: Region IV. Llano de la Hignera. AF435392 AY227914 DQ884746 DQ872762

Colletellus aff. velutinus (co*ckerell, 1929) [EA0097] Colletidae:Paracolletinae

Australia: WA; Eurardy Stat. 09.x.2005 DQ884625 DQ884530 DQ884773 DQ768514

Edwyniana sp. [EA0071] Colletidae:Paracolletinae

Chile: Region IV. Guampulla SW Samo Alto.19.x.2001

DQ884598 DQ884504 DQ884745 DQ768487

Eulonchopria punctatissima Michener, 1963[EA0077]


Mexico: Jalisco. Carretera 200, km 55.02.ix.2004

DQ884599 DQ884505 DQ884747 DQ768488

Eulonchopria simplicicrus (Michener, 1989)[EA0009]


Brazil: Minas Gerais. Belo Horizonte. 06.v.2002 DQ884588 DQ884495 DQ884734 DQ768477

Euryglossidia sp.1 [EA0102] Colletidae:Paracolletinae

Australia: WA; Boorabbin Ntl.Prk. 25.ix.2005 DQ884611 DQ884516 DQ884759 DQ768500

Euryglossidia sp.2 [EA0103] Colletidae:Paracolletinae

Australia: WA; �6 km E Merredin 23.ix.2005 DQ884612 DQ884517 DQ884760 DQ768501

Euryglossidia sp.3 [EA0104] Colletidae:Paracolletinae

Australia: WA; Eurardy Station. 09.x.2005 DQ884613 DQ884518 DQ884761 DQ768502

Euryglossidia sp.4 [EA0151] Colletidae:Paracolletinae

Australia: WA; Badgingarra Ntl.Prk. 11.x.2005 DQ884618 DQ884523 DQ884766 DQ768507

Euryglossidia sp.5 [EA0152] Colletidae:Paracolletinae

Australia: WA; �5.8 km NE Menzies 24.ix.2005 DQ884619 DQ884524 DQ884767 DQ768508

Excolletes sp. [EA0098] Colletidae:Paracolletinae

Australia: WA; Kalbarri Ntl.Prk. 08.x.2005 DQ884626 — DQ884774 DQ768515

Glossurocolletes bilobatus (Michener, 1965)[EA0093]


Australia: WA; Kalbarri Ntl.Prk. 06.x.2005 DQ884623 DQ884528 DQ884771 DQ768512

Goniocolletes fimbriatinus (co*ckerell, 1910)[Lefm702]


Australia: Victoria. 12 km E Hattah. 6.i.1999 AY585131 DQ115554 DQ884786 DQ872763

Goniocolletes perfasciatus (co*ckerell, 1906)[Lepr704]


Australia: Victoria. 12 km E Hattah. 9.i.1999 AY585134 DQ115557 DQ884787 DQ872764

Halictanthrena malpighiacearum Ducke, 1907[EA0088]


Brazil: Minas Gerais. Serra do Salitre. 11.xi.2004 DQ884604 DQ884510 DQ884752 DQ768493

Hexantheda missionica Ogloblin, 1948 [EA0124] Colletidae:Paracolletinae

Brazil: Minas Gerais. Brumadinho. 12.i.2001 DQ884615 DQ884520 DQ884763 DQ768504

Hoplocolletes ventralis (Friese, 1924) [EA0021] Colletidae:Paracolletinae

Brazil: Minas Gerais. Florestal. 03.xii.2001 DQ884590 DQ884497 DQ884736 DQ768479

Kylopasiphae pruinosa (Michener, 1989) [EA0084] Colletidae:Paracolletinae

Argentina: Mendoza. 37 km SSE Uspallata. 29–30.xi.2004

DQ884601 DQ884507 DQ884749 DQ768490

294 E.A.B. Almeida, B.N. Danforth / Molecular Phylogenetics and Evolution 50 (2009) 290–309

(PDF) Phylogeny of colletid bees (Hymenoptera: Colletidae) inferred from four nuclear genes - DOKUMEN.TIPS (6)

Table 1 (continued)

Species [voucher code] Classification Collecting data EF-1a Opsin Wingless 28S rRNA

Lamprocolletes chalybeatus (Erichson, 1851)[EA0099]


Australia: WA. Boorabbin Ntl.Prk. 25.ix.2005 DQ884627 — DQ884775 DQ768516

Leioproctus conospermi Houston, 1989 [EA0110] Colletidae:Paracolletinae

Australia: WA; Kalbarri Ntl.Prk. 08.x.2005 DQ884632 DQ884534 DQ884780 DQ768521

Leioproctus irroratus (Smith, 1853) [Leir705] Colletidae:Paracolletinae

Australia: NSW. Hilltop. 2.xii.1999 AY585132 DQ115555 DQ884788 DQ872765

Leioproctus lanceolatus Houston, 1990 [EA0111] Colletidae:Paracolletinae

Australia: WA; �90 km E Leonora. 28.ix.2005 DQ884633 DQ884535 DQ884781 DQ768522

Leioproctus megachalcoides Michener, 1965[EA0112]


Australia: WA Eurardy Station. 09.x.2005 DQ884634 DQ884536 DQ884782 DQ768523

Leioproctus pappus Houston, 1989 [EA0109] Colletidae:Paracolletinae

Australia: WA; Badgingarra Ntl.Prk. 11.x.2005 DQ884631 — DQ884779 DQ768520

Leioproctus platycephalus (co*ckerell, 1912)[EA0113]


Australia: WA; North Tarin Rock Nat. Res.02.x.2005

DQ884635 DQ884537 DQ884783 DQ768524

Leioproctus plumosus (Smith, 1853) [Lepl706] Colletidae:Paracolletinae

Australia: Victoria. Torquay. 19.xi.1999 AY585133 DQ115556 DQ884789 DQ872766

Paracolletinae sp. [EA0123] Colletidae:Paracolletinae

Australia: WA. Badgingarra Ntl.Prk. 11.x.2005 DQ884637 DQ884538 DQ884785 DQ768526

Lonchopria (Biglossidia) robertsi Michener, 1989[EA0080]


Argentina: Mendoza. 6 km SSE Uspallata. 29–30.xi.2004

DQ884622 DQ884527 DQ884770 DQ768511

Lonchopria (Biglossidia) sp. [EA0070] Colletidae:Paracolletinae

Chile: Region I. Zapahuira (near Putre). Iv.2004 DQ884621 DQ884526 DQ884769 DQ768510

Lonchopria (Lonchopria) similis (Friese, 1906)[EA0069]


Chile: Region II. Pqe. Nacional Llanos de Challe.13.x.2000

DQ884620 DQ884525 DQ884768 DQ768509

Neopasiphae mirabilis Perkins, 1912 [EA0100] Colletidae:Paracolletinae

Australia: WA. �18.4 km NE Menzies.27.ix.2005

DQ884628 DQ884531 DQ884776 DQ768517

Niltonia virgilii Moure, 1964 [EA0087] Colletidae:Paracolletinae

Brazil: Santa Catarina. Maracajá. 04.x.2004 DQ884603 DQ884509 DQ884751 DQ768492

Nomiocolletes jenseni Friese, 1906 [EA0090] Colletidae:Paracolletinae

Argentina: Mendoza. 18 km SE Potrerillos. 29–30.xi.2004

DQ884606 DQ884512 DQ884754 DQ768495

Odontocolletes aff. asper (Maynard, 1997) [EA0105] Colletidae:Paracolletinae

Australia: WA. Eurardy Station. 09.x.2005 DQ884629 DQ884532 DQ884777 DQ768518

Odontocolletes pachyodontus (co*ckerell, 1915)[EA0106]


Australia: WA; �13 km NNE Eurardy Station.09.x.2005

DQ884630 DQ884533 DQ884778 DQ768519

Paracolletes cfr. crassipes Smith, 1853 [EA0019] Colletitidae:Paracolletinae

Australia: Queensland, Stanthorpe. 16.xii.2002 DQ884584 DQ884491 DQ884729 DQ768473

Perditomorpha laena (Vachal, 1909) [EA0024] Colletidae:Paracolletinae

Brazil: Minas Gerais. Santana do Riacho. 20/ii/2001.

DQ884592 DQ884499 DQ884738 DQ768481

Perditomorpha leucostoma (co*ckerell, 1917)[EA0091]


Argentina: Catamarca. Aconquija. 18.xi.2004 DQ884607 DQ884513 DQ884755 DQ768496

Perditomorpha neotropica (Friese, 1908) [EA0147] Colletidae:Paracolletinae

Argentina: Tucumán. 19 km SE Amaicha delValle. 17.ii.2003

DQ884616 DQ884521 DQ884764 DQ768505

Perditomorpha rufiventris (Spinola, 1851) [EA0046] Colletidae:Paracolletinae

Chile: Region IV. El Tofo. 23.x.2002 DQ884595 DQ884502 DQ884742 DQ768484

Perditomorpha stilborhina (Moure, 1954) [EA0107] Colletidae:Paracolletinae

Argentina: Prov. Tucumán. Amaicha del Valle.26.x.2004

DQ884614 DQ884519 DQ884762 DQ768503

Perditomorpha sp. [EA0068] Colletidae:Paracolletinae

Argentina: Chubut. 8 km N Sarmiento Hwy.24.26–27.xi.2003

DQ884597 DQ884503 DQ884744 DQ768486

Phenacolletes mimus co*ckerell, 1905 [EA0101] Colletidae:Paracolletinae

Australia: WA; �12 km SSE Dongara. 10.x.2005 DQ884610 DQ884515 DQ884758 DQ768499

Protomorpha aff. alloeopus (Maynard, 1991)[EA0114]


Australia: WA; Kalbarri Ntl.Prk. 08.x.2005 DQ884636 — DQ884784 DQ768525

Reedapis bathycyanea (Toro, 1973) [Lesp851] Colletidae:Paracolletinae

Chile: Region II. Santa Juana, E of Vallenar AY585141 DQ115553 DQ884741 DQ872761

Spinolapis caerulescens (Spinola, 1851) [EA0034] Colletidae:Paracolletinae

Chile: Region IV. Parque Nacional Talinay10.x.2001

DQ884594 DQ884501 DQ884740 DQ768483

Spinolapis sp. [EA0089] Colletidae:Paracolletinae

Argentina: Mendoza. 37 km SSE Uspallata. 29–30.xi.2004

DQ884605 DQ884511 DQ884753 DQ768494

Tetraglossula anthracina (Michener, 1989)[EA0023]


Brazil: Minas Gerais. Santana do Riacho.15.iv.2001

DQ884591 DQ884498 DQ884737 DQ768480

Trichocolletes (Trichocolletes) aff. venustus (Smith,1862) [EA0117]


Australia: WA; Boorabbin Ntl.Prk. 25.ix.2005 DQ884587 DQ884494 DQ884732 DQ768476

Trichocolletes (Trichocolletes) sp. [Trsp708] Colletidae:Paracolletinae

Australia: NSW. 53 km S Oberon. 30.xi.1999 AY585139 DQ115562 DQ884733 DQ872760

Scrapter algoensis (Friese, 1925) [Scal899] Colletidae:Scrapterinae

South Africa: NCP. 90 km ENE Sprinbok.10.ix.2001

EF032901 EF032904 DQ884812 DQ872771

Scrapter erubescens (Friese, 1925) [Scer901] Colletidae:Scrapterinae

South Africa: WCP. Pakhuis pass. Sept. 8.ix.2001 AY585135 DQ115558 DQ884813 DQ872772

Scrapter heterodoxus (co*ckerell, 1921) [Scht903] Colletidae:Scrapterinae

South Africa: WCP. 31 km S Clanwillian.7.ix.2001

AY585136 DQ115559 DQ884814 DQ872773

Scrapter niger Lepeletier and Serville, 1825[Scng905]


South Africa: WCP. 21 km N Hermanus.28.ix.2001

AY585137 DQ115560 DQ884815 DQ872774

Scrapter ruficornis (co*ckerell, 1916) [Scrc937] Colletidae:Scrapterinae

South Africa: WCP. Kunje Farm, near Citrusdal.23.ix.2001

AY585138 DQ115561 DQ884816 DQ872775

(continued on next page)

E.A.B. Almeida, B.N. Danforth / Molecular Phylogenetics and Evolution 50 (2009) 290–309 295

(PDF) Phylogeny of colletid bees (Hymenoptera: Colletidae) inferred from four nuclear genes - DOKUMEN.TIPS (7)

Table 1 (continued)

Species [voucher code] Classification Collecting data EF-1a Opsin Wingless 28S rRNA

Chilicola (Anoediscelis) herbsti (Friese, 1906)[EA0140]


Chile: Region IV. Liman, Chañar. 04.ix.2004 DQ884663 DQ884559 DQ884831 DQ768572

Chilicola (Oediscelis) vicugna Toro and Moldenke,1979 [EA0136]


Chile: Region IV. Elqui, Pangue. 11–30.ix.2004 DQ884661 DQ884557 DQ884828 DQ768569

Chilicola (Pseudiscelis) rostrata (Friese, 1906)[EA0137]


Argentina: Tucumán. 19 km SE Amaicha delValle. 17.ii.2003

DQ884662 DQ884558 DQ884829 DQ768570

Geodiscelis longiceps Packer, 2005 [EA0049] Colletidae:Xeromelissinae

Argentina: Tucumán. 19 km SE Amaicha delValle. 17.ii.2003

DQ884655 DQ884551 DQ884817 DQ768544

Xenochilicola mamigna Toro and Moldenke, 1979[EA0055]


Chile: Region II. Aguas Blancas (SSE San PedroAtacama)

DQ884660 DQ884556 DQ884827 DQ768558

Xeromelissa australis (Toro and Moldenke, 1979)[EA0051]


Chile: Region II. Panamerican Hwy., km 1005,NE Chanaral.

DQ884656 DQ884552 DQ884818 DQ768545

Xeromelissa irwini (Toro and Moldenke, 1979)[EA0053]


Chile: Region I. 83.5 km ESE Pozo Almonte. 8–20.iv.2004

DQ884658 DQ884554 DQ884821 DQ768547

Xeromelissa nortina (Toro and Moldenke, 1979)[EA0052]


Argentina: Santa Cruz. 20 km E Los Antiguos.17.xi.2003

DQ884657 DQ884553 DQ884820 DQ768546

Xeromelissa rozeni (Toro and Moldenke, 1979)[Chrz857]


Argentina: Santa Cruz. 25 km E Los Antiguos22.xi.2003

AY585120 DQ115549 DQ884826 DQ872776

Xeromelissa sp. [EA0138] Colletidae:Xeromelissinae

Chile: Region I. 83.5 km ESE Pozo Almonte.20.iv.2004

DQ884659 DQ884555 DQ884824 DQ768554

Alocandrena porteri Michener, 1986 [Alpo49] Andrenidae:Andreninae

Peru: Lima Dept. St. Bartholome. 21.x.1997 AY585099 DQ113659 — AY654473

Andrena brooksi Larkin, 2004 [Ansp643] Andrenidae:Andreninae

USA: NM. Hidalgo Co., 20 mi S Animas.17.ix.1999

AY230129 AF344618 AY222551 AY654474

Orphana wagenknechti Rozen, 1971 [Orph56] Andrenidae:Andreninae

Chile: Region IV. 7 km S Pisco Elqui DQ884568 DQ884476 DQ884709 DQ872755

Protoxaea gloriosa (Fox, 1893) [Pxgl226] Andrenidae:Oxaeinae

USA: AZ. Cochise Co., Portal AY585106 DQ113658 — AY654480

Nolanomelissa toroi Rozen, 2003 [Noto74] Andrenidae:Panurginae

Chile: Region II. 4 km N Domeyko DQ884569 DQ884477 DQ884710 DQ872756

Calliopsis (Nomadopsis) fracta (Rozen, 1952)[Cafr515]


USA: CA. Santa Cruz Co., San Antonio junction.28.v.1999

AY585101 AF344587 — AY654476

Panurgus (Panurgus) calcaratus (Scopoli, 1763)[Pnca514]


Italy: Rome. 07.vi.1998 AY585105 AF344612 — AY654479

Melitturga (Melitturga) clavicornis (Lattreille, 1806)[Mtcl959]


France: Herault. Causse de la Selle. 17.vi.2002 AY585104 DQ116703 — AY654478

Agapostemon tyleri (co*ckerell, 1917) [Agty230] Halictidae:Halictinae

USA: AZ. Cochise Co., Portal AF140320 AY227940 AY222577 AY654506

Augochlorella pomoniella (co*ckerell, 1915)[Aupo592]


USA: CA. Inyo Co., Big Pine. 15.vi.1999 AF435373 AY227935 AY222572 AY654507

Mexalictus arizonensis Eickwort, 1978 [Mxaz98] Halictidae:Halictinae

USA: AZ. Santa Cruz Co. AF140322 AY227959 AY222595 —

Halictus (Halictus) rubicundus (Christ, 1791)[Haru32]


USA: MT. Missoula Co., Missoula AF140335 DQ116674 AY222592 AY654510

Dieunomia (Epinomia) nevadensis (Cresson, 1874)[None207]


USA: AZ. Cochise Co., 1 mi E. Apache, 22.ix.1999 AF435396 AY227931 AY222568 AY654512

Conanthalictus wilmattae co*ckerell, 1936[Cowi351]


USA: CA. Riverside Co., 10 mi S Palm Desert.15.iii.1997

AF435378 AY227934 AY222553 AY654511

Dufourea mulleri (co*ckerell, 1898) [Dumu233] Halictidae:Rophitinae

USA: Michigan AF435383 AY227918 AY222555 AY654509

Penapis penai Michener, 1965 [Pnpe572] Halictidae:Rophitinae

Chile: Region II. N Vallenar AF435401 AY227921 AY222558 AY654513

Rophites (Rophites) algirus Perez, 1895 [Roal968] Halictidae:Rophitinae

France: Var. 5 km S Entrecasteaux. 14.vi.2002 AY585144 DQ116675 — AY654515

Systropha curvicornis (Scopoli, 1770) [Sycu350] Halictidae:Rophitinae

Austria: Vienna AF435411 AY227925 AY222562 AY654516

Ctenocolletes nigricans Houston, 1985 [EA0120] Stenotritidae Australia: WA; �18.4 km NNE Eurardy Station.05.x.2005

DQ884570 DQ884478 DQ884711 DQ768459

Ctenocolletes rufescens Houston, 1983 [EA0121] Stenotritidae Australia: WA. Boorabbin Ntl.Prk. 25.ix.2005 DQ884571 DQ884479 DQ884712 DQ768460Ctenocolletes smaragdinus (Smith, 1868) [EA0122] Stenotritidae Australia: WA. Boorabbin Ntl.Prk. 25.ix.2005 DQ884572 DQ884480 DQ884713 DQ768461Stenotritus sp. [Stsp1015] Stenotritidae Australia: WA. 23 km SW Coorow. 17.xi.1997 DQ141115 DQ115564 DQ884714 DQ872757

296 E.A.B. Almeida, B.N. Danforth / Molecular Phylogenetics and Evolution 50 (2009) 290–309

nator chemistry and AmpliTaq-FS DNA Polymerase at Cornell Uni-versity Life Sciences Core Laboratories Center.

GenBank Accession Nos. (Table 1) starting with ‘‘DQ7”, ‘‘DQ8”,and ‘‘EF0” are novel sequences. The remaining sequences were gen-erated by B.N. Danforth and co-workers (Danforth et al., 2004,2006a,b). The wingless sequence of Halictus quadricinctus (Fabricius)was used to represent that of Halictus rubicundus (Christ).

2.5. Alignment

Alignments for the individual gene data matrices were gener-ated using similarity calculated at the nucleotide level (‘‘�n’’)

with DIALIGN 2.2 (Morgenstern, 1999) and with the ClustalW(Lasergene DNA Star software package). The resulting alignmentswere then corrected manually for obvious alignment errors usingMacClade v 4.08 OSX (Maddison and Maddison, 2005) and WinC-lada 1.00.08 (Nixon, 2002). Regions of 28S rRNA and introns ofEF-1a where alignment was overly ambiguous were excludedfrom the phylogenetic analyses. Despite losing some information,the removal of problematic regions of the alignments potentiallyincreases the actual phylogenetic signal (see discussion by Talave-ra and Castresana, 2007). For the protein-coding genes, honey-bee(Apis mellifera Linnaeus) sequences were used to establish readingframes and intron/exon boundaries. Introns of the three protein-

(PDF) Phylogeny of colletid bees (Hymenoptera: Colletidae) inferred from four nuclear genes - DOKUMEN.TIPS (8)

(b) long wavelength (green) rhodopsin

620 bp 275 bp 250 bp

Intron 1(~210 bp)

HaF2For1 For3

F2Rev1 Cho10

(a) elongation factor-1 alpha (F2 copy)

1 2 3 6 7a 7b 8 10 1254





(c) wingless

(d) large subunit ribosomal RNA: 28S rRNA

length in bees = ~ 1500 bp



120010008006004002001 1400 1600

Intron 2(~230-500 bp)

Intron 1(~70-480 bp)

Intron 2(~60-1080 bp)

Intron 3(~60-750 bp)

Intron(~100-1400 bp)


Ops-Rev1b, (mod)

Ops-For4, 5Ops-For

Ops-For3, 3b, 3(mod)

210 bp 260 bp 170 bp 70 bp


175 bp 670 bp



Fig. 2. Maps of the gene loci sampled for this study. Primer sites (see Table 2 for a complete list of primer sequences), introns, and exons are indicated. Introns, when variable inlength, are represented on their lower limit of the range; length variation reported in the figure is observed in the sample of colletid bees included in this study; (a) elongationfactor-1a, F2 copy (adapted from Danforth et al., 2004), numbering based on Apis mellifera coding sequence (Walldorf and Hoverman, 1990, GenBank Accession AF015267); (b)long wavelength rhodopsin (adapted from Danforth et al., 2004), numbering based on A. mellifera coding sequence (Chang et al., 1996; GenBank Accession U26026); (c)wingless, numbering based on Drosophila melanogaster coding sequence (Uzvölgyi et al., 1988; GenBank Accession J03650); (d) 28S rRNA (adapted from Caterino et al., 2000),nucleotide numbering and region names based on D. melanogaster ribosomal genes (Hanco*ck et al., 1988; Linares et al., 1991; Tautz et al., 1988, GenBank Accession M21017).

E.A.B. Almeida, B.N. Danforth / Molecular Phylogenetics and Evolution 50 (2009) 290–309 297

coding genes sampled were initially aligned for all taxa. Introns ofopsin and wingless were subsequently excluded from the analysesbecause length variation and sequence variability observed inthese regions made them unalignable. Both EF-1a introns couldonly be aligned for colletid and stenotritid sequences (i.e., intronsfrom all other outgroup terminals were discarded to allow for theremaining to be alignable). The second EF-1a intron is more var-iable than intron 1 (Fig. 2), so was aligned separately for two setsof species: (1) representatives of Stenotritidae, Diphaglossinae,and Paracolletinae (excluding Callomelitta antipodes); and (2) ofColletinae s.str., Euryglossinae, Hylaeinae, Scrapterinae, Xerome-lissinae, plus Callomelitta antipodes. Selection of these blocks oftaxa was made based on groupings found in preliminary analysesof exon data plus the 28S sequences, and on sequence similarityfound among introns of the terminals. Although unusual, thisprocedure will not introduce phylogenetic artifacts. We are sim-

ply attempting to extract the maximum amount of informationfrom the largest regions of the non-coding partitions of the dataset.

In cases where multiple sequences were available for the samespecies, the sequences were merged after being resolved in thesame clade in preliminary analyses and resulting partial polymor-phisms were kept as such. Individual gene data sets were concate-nated with WinClada.

The combined data set in Nexus-format used in phylogeneticanalyses is available for download as Supplementary information.

2.6. Phylogenetic analyses

Bayesian phylogenetic inference was used to estimate the treetopology. Metropolis-coupled MCMC, as implemented in the serialversion of MrBayes 3.1.2 (Altekar et al., 2004; Huelsenbeck and

(PDF) Phylogeny of colletid bees (Hymenoptera: Colletidae) inferred from four nuclear genes - DOKUMEN.TIPS (9)

Table 2Primer sequences for EF-1a (F2 copy), opsin, wingless, and 28S rRNA used for PCR assays of bees.

Locus Primer Sequence Position Reference

EF-1aa HaF2For1 50-GGG YAA AGG WTC CTT CAA RTA TGC-30 511 Danforth et al. (1999)For3rho 50-GGY GAC AAY GTT GTT TTY AAY G-30 1496 Danforth et al. (1999)F2-rev1 50-A ATC AGC AGC ACC TTT AGG TGG-30 1600 Danforth et al. (1999)Cho10-Rev(mod) 50-AC RGC VAC KGT YTG HCK CAT GTC-30 1887 Danforth et al. (1999)

Opsinb Opsin-For [=LWRhFor)] 50-AAT TGC TAT TAY GAR ACN TGG GT-30 398 Mardulyn and Cameron (1999)

Opsin-For3 [=LWRhFor3] 50-AGA TAC AAC GTR ATC GTS AAR GGT-30 512 Danforth et al. (2004)

Opsin-For3(mod) 50-TTC GAY AGA TAC AAC GTR ATC GTN AAR GG-30 506 Danforth (unpublished)

Opsin-For3b 50-AGA TAC AAC GTR ATY GTN AAR GGT-30 512 Almeida (unpublished)Opsin-For4 50-GAG AAR AAY ATG CGB GAR CAA GC-30 803 Danforth et al. (2004)Opsin-For5 50-ATG CGN GAR CAR GCN AAR AAR ATG AA-30 812 Danforth (unpublished)Opsin-Rev (=LWRhRev) 50-ATA TGG AGT CCA NGC CAT RAA CCA-30 946 Mardulyn and Cameron (1999)

Opsin-Rev1b 50-RTA YGG RGT CCA NGC CAT RAA CCA-30 946 Almeida (unpublished)Opsin-Rev(mod) 50-ATA NGG NGT CCA NGC CAT GAA CCA-30 946 Danforth (unpublished)Opsin-Rev4 50-GGT GGT GGT RCC GGA RAC GGT G-30 1147 Danforth et al. (2004)Opsin-Rev4b 50-GGT RCC GGA RAC GGT GGA DGT NGC RTC-30 1147 Danforth (unpublished)

Winglessc Bee-wg-For2 50-GGC AGC ATY CAG TCS TGY TCC TGC GA-30 445 Sipes (unpublished)Wg-Collet-For 50-CAC GTG TCB TCB GRG ATG MGR SAG GA-30 670 Almeida (unpublished)Lep-Wg2a-Rev 50-ACT ICG CAR CAC CAR TGG AAT GTR CA-30 1336 Brower and DeSalle (1998)

28S rRNAd A-28S-For 50-CCC CCT GAA TTT AAG CAT AT-30 3318 Ward and Brady (2003)Bel28S-For (D2-3665F) 50-AGA GAG AGT TCA AGA GTA CG TG-30 3665 Belshaw and Quicke (1997)Mar28S-Rev (D3-4283R) 50-TAG TTC ACC ATC TTT CGG GTC CC-30 4283 Mardulyn and Whitfield (1999)28SD4-Rev (D5-4749R) 50-GTT ACA CAC TCC TTA GCG GA-30 4749 Danforth et al. (2006a)

a PCR conditions. HaF2For1/F2-rev1: 94 �C for 1 min, 48–52 �C for 1 min, 72 �C for 1.5 min (35 cycles); For3rho/Cho10-Rev(mod): 94 �C for1 min, 54–56 �C for 1 min, 72 �Cfor 1 min (35 cycles). Positions based on the 50 end of the primer in Apis mellifera (Walldorf and Hoverman, 1990; GenBank Accession No. AF015267).

b PCR conditions. Opsin-For/Opsin-Rev: 94 �C for 1 min, 50–54 �C for 1 min, 72 �C for 1.5 min (35 cycles); Opsin-For3/Opsin-Rev: 94 �C for 1 min, 52–54 �C for 1 min, 72 �Cfor 1 min (35 cycles); Opsin-For3(mod)/Opsin-Rev(mod): 94 �C for 1 min, 52–54 �C for 1 min, 72 �C for 1 min (35 cycles); Opsin-For3 b/Opsin-Rev1 b: 94 �C for 1 min, 50–54 �C for 1 min, 72 �C for 1 min (35 cycles); Opsin-For4/Opsin-Rev4: 94 �C for 1 min, 55–58 �C for 1 min, 72 �C for 1 min (35 cycles); Opsin-For5/Opsin Rev4b: 94 �C for 1 min,55 �C for 1 min, 72 �C for 1 min (35 cycles). Positions based on the 50 end of the primer in Apis mellifera (Chang et al., 1996; GenBank Accession No. U26026).

c PCR conditions. Bee-wg-For2/Lep-wg2a-Rev: 94 �C for 1 min, 54–58 �C for 1 min, 72 �C for 1.5 min (35 cycles); Wg-Collet-For/Lep-wg2a-Rev: 94 �C for 1 min, 56 �C for1 min, 72 �C for 1 min (35 cycles). Positions based on the 50 end of the primer in Drosophila melanogaster (Uzvölgyi et al., 1988; GenBank Accession No. J03650).

d PCR conditions. A-28S-For Mar28S-Rev: 94 �C for 1 min, 58 �C for 1 min, 72 �C for 1.5 min (35 cycles); Bel28S-For/28SD4-Rev: 94 �C for 1 min, 58 �C for 1 min, 72 �C for1.5 min (35 cycles). Positions based on the 50 end of the primer in Drosophila melanogaster (Tautz et al., 1988; Linares et al., 1991; GenBank Accession No. M21017).Numbering corresponds to the expansion regions as proposed by Hanco*ck et al. (1988).

298 E.A.B. Almeida, B.N. Danforth / Molecular Phylogenetics and Evolution 50 (2009) 290–309

Ronquist, 2005), was used to estimate the posterior probability dis-tribution. The gamma distribution of rate variation across sites wasapproximated by a discrete distribution with four rate categories,each category being represented by its mean rate. All chains, includ-ing coupled chains in the same run, were started from different, ran-domly chosen trees. Searches were run for 2 � 106 generations ontwo sets of 10 chains each, through the Computational Biology Ser-vice Unit at the Cornell Theory Center (http://cbsu.tc.cornell.edu/).Convergence was assessed by the standard deviation of split fre-quencies of the two independent MrBayes runs, by the convergencediagnostic for individual parameters employing potential scalereduction factor (Gelman and Rubin, 1992, uncorrected), and bythe achievement of stationarity of the log likelihood values of thecold chain. Trees were saved every 100 generations. The initial1000–3000 trees were discarded after examining the variation inlog likelihood scores over time. Models for the five partitions of theconcatenated data set (EF-1a [exons], EF-1a [introns], 28S rRNA, op-sin [exons], and wg [exons]) were individually selected and imple-mented. Partitioned analyses were run with MrBayes applyingmodels selected by different methods (see below), in order to testthe effect of various levels of model complexity.

The best-fit model of evolution for each of the five partitionswas statistically tested. Model selection is one of the most contro-versial fields of statistics (Burnham and Anderson, 2002), and thisis not different in the field of phylogenetics (e.g., Posada andCrandall, 2001; Nylander et al., 2004; Posada and Buckley, 2004;Sullivan and Joyce, 2005). The four approaches most commonlyused for model selection in phylogenetics are hierarchical likeli-hood ratio test (hLRT), Akaike information content (AIC), Bayesianinformation content (BIC), and decision theory (DT) (Posada andBuckley, 2004; Sullivan and Joyce, 2005). Four programs were used

to shed light on the best-fit model(s) for the data: (1) DT-ModSel(Minin et al., 2003—DT model selection); (2) ModelTest 3.7 (Posadaand Crandall, 1998—hLRT, AIC, BIC; a set to 0.05); (3) MrModelTest(Nylander, 2004b—hLRT, AIC); and (4) MrAIC.pl 2.2 (Nylander,2004a—AIC and BIC). In addition to statistical tests for model selec-tion, highly complex models were tested in MrBayes for the com-bined data matrix, to check the effects of higher model-realismin the phylogenetic results: GTR + I + C and GTR + SSR for each par-tition, with all parameters unlinked across partitions.

For comparison with the Bayesian analysis, the data set wassubjected to maximum likelihood analysis and equal weights par-simony analyses. Maximum likelihood searches were done usingGarli v0.951 (Zwickl, 2006). Garli does not allow for data set parti-tioning, so the complete concatenated matrix was analyzed undera GTR + I + C model as a means to deal with the heterogeneitywithin the data. When analyzing individual genes, simpler modelswere used when that appeared to be a reasonable alternative, butvarious levels of complexity were tested. The termination condi-tion was set to 1 � 105 generations without significantly betterlikelihood scoring topology being found (‘‘genthreshfortopo-term = 100,000”); remaining settings were left unchanged fromthe defaults. Non-parametric bootstrap proportions were calcu-lated based on 1000 pseudo-replicates generated with Garli. Thefrequency of occurrence of each group present in the most likelytree topology was calculated using WinClada.

Parsimony analyses were conducted in PAUP� v4.0b10 (Swof-ford, 2002) using heuristic searches with tree bisection–reconnec-tion (TBR), 1000 random-taxon-addition replicates holding 50trees per replicate, and treating sequence indels as missing data.Branch support was assessed with 1000 bootstrap pseudo-repli-cates (Felsenstein, 1985). Each resampled matrix was searched

(PDF) Phylogeny of colletid bees (Hymenoptera: Colletidae) inferred from four nuclear genes - DOKUMEN.TIPS (10)

Table 3Overview of the partition and combined data sets.

Number ofcharacters



Information/numberof characters

EF-1a (exons 1151 427 7966 6.92EF-1a (introns) 1425 601 6174 4.33Opsin (exons) 707 324 5824 8.24wg (exons) 692 218 3862 5.5828S rRNA 1523 333 3352 2.32

Combined 5498 1903 27358 4.98

E.A.B. Almeida, B.N. Danforth / Molecular Phylogenetics and Evolution 50 (2009) 290–309 299

100 times and consensus trees found at each iteration were savedand used to calculate node support (percentage count) for eachclade present in the strict consensus of the most parsimonioustrees using WinClada.

2.7. Rate of substitution and parameters of molecular evolution

MrBayes was also used to explore some properties of the molec-ular data sets. Summarized parameters after discarding the initialtrees were used as estimates of base frequencies, rates of substitu-tion, and shape parameter (a) of the gamma distribution. Datawere analyzed with GTR + C models in which all parameters wereunlinked across partitions. This allowed base composition of eachgene and within partition rate variation (a) to be estimated. In or-der to estimate the rates of substitution, the data set was analyzedwith a site-specific rates model (GTR + SSR) with rate categoriescorresponding to each codon position within the protein-codinggene exons, to the intron of EF-1a, and to 28S rRNA.

2.8. Topological congruence between partition trees and the combinedtree

The phylogenetic signal of each partition was assessed by com-paring the Bayesian topology obtained for each gene analyzedalong with the topology obtained based on an analysis of all fivepartitions combined. Nodes present in the tree topology withinthe ingroup resulting from the five partitioned analyses were com-pared in a pair-wise manner to the combined tree and classified aseither congruent or not. A congruent node was one underpinning amonophyletic group of species found in the analysis of the com-bined data set or not contradicted by the results of the latter. ‘Con-gruent topological information’ (CTI) was a measure used here toapproximate concordance between the partitions and the com-bined tree topologies. CTI was calculated as the ratio betweennumber of congruent nodes and maximum number of resolvednodes for a given number of terminals.

2.9. Hypothesis testing

In order to compare alternative tree topologies, Kishino–Hase-gawa and Shimodara–Hasegawa tests (Kishino and Hasegawa,1989; Shimodara and Hasegawa, 1999) were performed with1000 bootstrap replicates using PAUP�. Likelihood was estimatedwith the RELL (resampling of estimated log-likelihood) method(Kishino et al., 1990), as an approximation of a computationallyintensive bootstrap (Felsenstein, 2004). Significance of likelihoodscore differences was assessed in a pair-wise manner using aone-tailed test, as suggested by Felsenstein (2004, 369). Addition-ally, a Bayesian approach to hypothesis testing was used for com-parisons among alternative topologies. Constrained tree topologieswere generated in MrBayes under a fixed model and their har-monic means were compared (Kass and Raftery, 1995; Nylanderet al., 2004). From the harmonic means, 2loge(B10) is calculatedby doubling the difference in the means of two topologies beingcompared and this quantity can be interpreted with the aid ofthe table from Kass and Raftery (1995, 277; a useful discussionabout the application of Bayes factors specifically to phylogeneticquestions is given by Nylander et al., 2004).

3. Results

3.1. Molecular data sets

The final combined data matrix contains 144 taxa and 5498aligned base pairs. Among those, 1903 are parsimony-informativecharacters. Information of a character is a quantity defined as its

maximum number of steps minus its minimum number of steps(denominator for the retention index [Farris, 1989]). The matrix’sinformation is simply the sum of the information of each of itscomponent characters. The information of the combined matrixwas equal to 27,358 steps (calculated with WinClada). The result-ing concatenated data matrix includes the exons of the three pro-tein-coding genes (EF-1a, opsin, and wg), both introns of EF-1a,and most of the sequences of 28S rRNA. After the 28S sequenceswere aligned, regions where alignment was judged to be ambigu-ous were deactivated. The total of excluded 28S aligned characterswas 371 steps, representing an information loss of 1928 steps. Thetotal number of characters and of informative characters per gene,and the information content of each partition are presented in Ta-ble 3.

3.2. Model selection and comparisons among genes

A summary of the results found with the different model selec-tion programs is presented in Table 4. The most complex modeltested by those programs, GTR + I + C was indicated as the mostappropriate one for each locus by at least one model selectionstrategy. Except for wg, all other genes had a model indicated tobe superior by some of the model selection methods, which wassimpler than GTR + I + C and implemented in MrBayes. The com-bined and unpartitioned data set was tested for one overall best-fit model and it was invariably GTR + I + C. MrBayes allows modelpartitioning and this is a desirable feature for allowing for a morerealistic phylogenetic approach (Nylander et al., 2004). Empiricaltests of evaluating the effects of using models with variable levelsof complexity to the Bayesian phylogenetic analyses (partitionedand combined) did not yield significantly different results; topolo-gies found for the data sets tended to be largely resilient to varia-tion in model complexity, with slight changes being observed inthe posterior probability values. All phylogenetic results shownare based on the simplest models considered adequate for the databy the model selection strategies tested.

The result of a characterization of the gene data is presented inFig. 3. Wingless and EF-1a (both exons and introns) present a devi-ation from equal base composition more noticeable than in theother two genes—the former has a slight G–C bias and the latteran A–T bias (Fig. 3a). This is reflected in the models found to bethe best-fit for each gene (Table 4). The simplest models shownto be adequate for opsin and 28S rRNA have equal base composi-tion (K80 and SYM, respectively), whereas wg and EF-1a requiremore complex models (Table 4).

Relative rates of substitution of each of the gene loci are shownin Fig. 3b and an approximation of how variable these rates arewithin each locus is given by the a parameter of the gamma distri-bution (Fig. 3c). High values of a (e.g., EF-1a introns) indicate rel-atively hom*ogeneous rates across sites, whereas low values of a(e.g., wingless exons) indicate high heterogeneity in among-siterate variation (Fig. 3c). Introns would be expected to show hom*og-enous rates relative to protein-coding exons because there se-

(PDF) Phylogeny of colletid bees (Hymenoptera: Colletidae) inferred from four nuclear genes - DOKUMEN.TIPS (11)















28S rRNA
















-1a (



-1a (














nt1 nt2 nt3

opsin (exons)

nt1 nt2 nt3

wingless (exons)

nt1 nt2 nt3

EF-1a (exons) EF-1




S rR



b c

Fig. 3. Comparisons among gene loci sampled for this study based on molecular parameters estimated by MrBayes: (a) frequencies of the nucleotide bases for each genelocus; (b) relative rates of substitution; (c) a parameter of the gamma distribution of rates.

Table 4Models for each gene as selected by different computer programs. Models in bold and italicized are implemented in MrBayes 3.1.2.

Gene locus Program: model selection test Model [number of free parameters]*

28S rRNA DT_ModSel; modeltest: BIC TVMef+I+C [4]MrAIC: AIC, AICc, BIC SYM+I+C [5]modeltest: hLRTs TrN+I+C [5]modeltest: AIC; MrModelTest: hLRTs, AIC GTR+I+C [8]

EF-1a (exons) DT_ModSel; modeltest: BIC; MrAIC: AIC*, AICc*, BIC* HKY+I+C [4]modeltest: hLRTs, AIC TrN+I+C [5]MrModelTest: hLRTs, AIC GTR+I+C [8]

EF-1a (introns) DT_ModSel; modeltest: AIC, BIC HKY+I+C [4]modeltest: hLRTs TVM+I+C [7]MrModelTest: hLRTs, AIC; MrAIC: AIC, AICc, BIC GTR+I+C [8]

Opsin (exons) DT_ModSel; modeltest: AIC, BIC K80+I+C [1]modeltest: hLRTs TrN+I+C [5]MrModelTest: hLRTs, AIC; MrAIC: AIC, AICc, BIC GTR+I+C [8]

wingless (exons) DT_ModSel; modeltest: AIC, BIC TrN+I+C [5]modeltest: hLRTs; MrModelTest: hLRTs, AIC; MrAIC: AIC*, AICc*, BIC* GTR+I+C [8]

* Number of free parameters for the model of substitution alone, this number does not include parameters associated with the gamma distribution (C) and the proportion ofinvariant sites (I).

300 E.A.B. Almeida, B.N. Danforth / Molecular Phylogenetics and Evolution 50 (2009) 290–309

quences should be under less selection than coding regions. In rel-ative terms, rates of substitution of first and second positions ofopsin are higher and of third positions are lower than those ob-

served in EF-1a and wg (Fig. 3b). The relative rate of the intronsof EF-1a fits in the range of rates of third positions of the exonsand that of 28S rRNA is similar to 1st positions of exons (Fig. 3b).

(PDF) Phylogeny of colletid bees (Hymenoptera: Colletidae) inferred from four nuclear genes - DOKUMEN.TIPS (12)

E.A.B. Almeida, B.N. Danforth / Molecular Phylogenetics and Evolution 50 (2009) 290–309 301

3.3. Phylogenetic relationships

Results of the Bayesian phylogenetic analysis are shown in Figs.4 and 5. Overall, topologies obtained with maximum likelihoodand parsimony analyses were very similar to those of the Bayesian













“Paracolletinae”(except Callomelitta and Paracolletes)





















Euryglossinae +Scrapterinae




Fig. 4. Majority-rule consensus tree resulting from mixed-model Bayesian analysis of 549(K80 + I + C), exons of wingless (GTR + I + C), and 28S rRNA (SYM + I + C) from 122 specidashed lines were not recovered in the Bayesian consensus and are based on the maxprobabilities; numbers below internodes indicate non-parametric bootstrap proportionsrecovered in one of the three analyses are indicated by ‘‘n.r.”. (a) Andrenidae, HalictidaCallomelitta and Paracolletes).

result (Figs. S1–S3, Supplementary materials). Because of this topo-logical congruence among the three analytical methods, the Bayes-ian tree is used to show node support values obtained usingbootstrap proportions of parsimony and ML, as well as Bayesianposterior probabilities (Fig. 4). As expected, Bayesian posterior

Alocandrena porteriAndrena brooksiOrphana wagenknechti

Nolanomelissa toroiCalliopsis fractaMelitturga clavicornisPanurgus calcaratus

Protoxaea gloriosa

Agapostemon tyleriMexalictus arizonensisHalictus rubicundusAugochlorella pomoniellaDieunomia nevadensisConanthalictus wilmattaeDufourea mulleriSystropha curvicornisRophites algirusPenapis penai

Ctenocolletes nigricansStenotritus sp.Ctenocolletes rufescensCtenocolletes smaragdinus

Zikanapis clypeataPtiloglossa tarsataPtiloglossa sp.Ptiloglossa thoracica

Willinkapis chalybaeaCaupolicana yarrowi

Caupolicana bicolorCaupolicana vestita

Caupolicana quadrifasciata

Cadegualina andinaCadeguala occidentalisCadeguala albopilosaDiphaglossa gayiMydrosoma fallaxMydrosoma aterrimumParacolletes cfr. crassipes

Hemicotelles ruizii

Colletes compactus

Colletes floralisColletes simulans

Colletes thoracicusColletes inaequalis

Colletes skinneriColletes pascoensis

Colletes distinctus

Colletes gilvusColletes furfuraceusColletes bicolor

Colletes seminitidusXanthocotelles sicheliRhynchocolletes mixtusCallomelitta antipodesEuhesma sp.Callohesma calliopsella

Euhesma platyrhinaEuhesma aff. crabronicaEuryglossina globulicepsXanthesma furciferaScrapter heterodoxusScrapter ruficornisScrapter nigerScrapter algoensisScrapter erubescens

Xeromelissa australisXeromelissa sp.Xeromelissa irwiniXeromelissa nortinaXeromelissa rozeniGeodiscelis longiceps

Xenochilicola mamignaChilicola (Anoediscelis) herbstiChilicola (Pseudiscelis) rostrataChilicola (Oediscelis) vicugnaHyleoides concinna

Meroglossa itamucaAmphylaeus (Agogenohylaeus) obscuricepsPalaeorhiza (Heterorhiza) sp.Palaeorhiza (Palaeorhiza) sp.

Hylaeus (Macrohylaeus) alcyoneusHylaeus (Euprosopis) disjunctusHylaeus (Euprosopis) elegansHylaeus (Rhodohylaeus) proximusHylaeus (Gnathoprosopis) amiculus

Hylaeus (Pseudhylaeus) aff. simplus





99 100





















36/n.r. 9685/44







n.r. 60/4590








100 100/100100












100/98100 100/100





n.r./n.r.73 n.r./n.r.





8 aligned bp of the exons and introns of EF-1a (model = HKY + I + C), exons of opsines of colletid bees and 22 species of other bee families. Branches represented withimum likelihood topology. Numbers above internodes indicate Bayesian posterior

for the for the likelihood analysis (left) and parsimony analysis (right). Nodes note, Stenotritidae, and most of the colletid subfamilies; (b) ‘‘Paracolletinae” (except

(PDF) Phylogeny of colletid bees (Hymenoptera: Colletidae) inferred from four nuclear genes - DOKUMEN.TIPS (13)

Anthoglossa sp.Anthoglossa cfr. robustus

Trichocolletes (T.) aff. venustusTrichocolletes (T.) sp.

Phenacolletes mimusEuryglossidia sp.4Euryglossidia sp.2

Euryglossidia sp.3Euryglossidia sp.1

Euryglossidia sp.5

Neopasiphae mirabilisAndrenopsis sp.Paracolletinae sp.Leioproctus megachalcoidesLamprocolletes chalybeataLeioproctus lanceolatusExcolletes sp.

Colletellus aff. velutinusGlossurocolletes bilobatusLeioproctus conospermiLeioproctus pappus

Goniocolletes fimbriatinusGoniocolletes perfasciatus

Protomorpha aff. alloeopus

Odontocolletes aff. asperOdontocolletes pachyodontus

Leioproctus platycephalusLeioproctus irroratusLeioproctus plumosus

Baeocolletes minimusBaeocolletes sp.

Halictanthrena malpighiacearumPerditomorpha neotropicaCephalocolletes laticepsCephalocolletes isabelaeReedapis bathycyanea

Nomiocolletes jenseni

Eulonchopria punctatissimaEulonchopria simplicicrusHoplocolletes ventralisSpinolapis sp.Spinolapis caerulescensBelopria nitidiorEdwyniana sp.Perditomorpha leucostomaPerditomorpha laenaTetraglossula anthracinaBrachyglossula communisHexantheda missionicaPerditomorpha rufiventrisPerditomorpha stiborhinaKylopasiphae pruinosaPerditomorpha sp.Niltonia virgiliiChilicolletes delahozii

Lonchopria (Biglossa) robertsiLonchopria (Biglossa) sp.Lonchopria (Lonchopria) similis













100/100100 77/61


























97/92 100







62 98/90100

80 99/99100


41/3786 96/95















Fig. 4 (continued)

302 E.A.B. Almeida, B.N. Danforth / Molecular Phylogenetics and Evolution 50 (2009) 290–309

probabilities were higher or equal to bootstrap proportions foundwith ML and with parsimony.

The most unanticipated results were the placement of Para-colletes and Callomelitta as two lineages independent of theremaining Paracolletinae. To facilitate communication, the cladeformed by all Paracolletinae except Paracolletes and Callomelittawill be referred to as ‘‘Paracolletinae” henceforth. For the mostpart, all three analytical methods found the same arrangementof subfamilies and tribes, with one noteworthy exception: MLplaced Callomelitta antipodes as sister-group to ‘‘Paracolletinae”,whereas Bayesian and parsimony analyses placed it as sister ofColletinae s.str.

Alternative phylogenetic arrangements regarding the place-ment of Paracolletes and Callomelitta were statistically tested. Thetopology favored by both parsimony and Bayesian analyses isshown in Fig. 6a; pair-wise comparisons of this tree to five alterna-tives (Fig. 6b–f) were done using Bayesian and likelihood-basedstatistics (Table 5). The only alternative topology considered tobe significantly different by both statistical measures was the sis-

ter-group relationship (or inclusive relationship) of Paracolletesand ‘‘Paracolletinae” (Fig. 6c).

The strict consensus of the most parsimonious trees (Fig. S3)was less resolved than the Bayesian and ML topologies. Relation-ships between Colletinae plus Callomelitta, ‘‘Paracolletinae”, andthe clade formed by Euryglossinae, Hylaeinae, Scrapterinae, andXeromelissinae form an unresolved trichotomy. The relationshipbetween ‘‘Paracolletinae” and its sister-clade was strongly sup-ported by the Bayesian analysis (100% posterior probability) butonly moderately supported by ML (66% bootstrap support). All col-letid subfamilies, except Paracolletinae, were very well-supportedby the data as monophyletic. Furthermore, the grouping of Eury-glossinae, Scrapterinae, Hylaeinae, and Xeromelissinae, as well asthe sister-group relationships between [Euryglossinae + Scrapteri-nae], and [Hylaeinae + Xeromelissinae] all received fairly highbootstrap and Bayesian posterior probability endorsem*nt. Thelevels of support for groupings within Colletidae based on the dif-ferent gene partitions and the combined results can be comparedin Table 6.

(PDF) Phylogeny of colletid bees (Hymenoptera: Colletidae) inferred from four nuclear genes - DOKUMEN.TIPS (14)

E.A.B. Almeida, B.N. Danforth / Molecular Phylogenetics and Evolution 50 (2009) 290–309 303

The sister-group relationship between Colletinae (with or with-out Callomelitta) and the clade formed by Euryglossinae, Hylaeinae,Scrapterinae, and Xeromelissinae is weakly supported (Figs. 4a, S1

0.05 changes

AAndrena br

Orphana wagenknec


Systropha curvicoRophites algirus


Ctenocolletes nigricansStenotritus sp.

Ctenocolletes rufescensCtenocolletes smaragdinus



Caupolicana quad

Cadegualina aCadeguala oCadeguala a

Diphaglossa gayiMydro

MydParacolletes cfr. crassipes




ScrScrapter niger

Scrapter aScrapter erubesce

Anthoglossa sp.Anthoglossa cfr. robustus

Trichocolletes (T.) aff. venuTrichocolletes (T.) sp.

Phenacolletes mEuryglossidia sp.4Euryglossidia sp.2

Euryglossidia sp.3Euryglossidia sp.1Euryglossidia sp.5




Colletellus affGlossuroLeio


Leioproctus platyceLeioproctus irror

Leioproctus pl

Baeocolletes mBaeocolletes

Halictanthrena malpPerditomorpha neotropCephalocolletes latice

Cephalocolletes isaReedapis bathycyanea


EulonHoplocolletes vent

Spinolapis sp.Spinolapis caerulesBelopria nitidior

Edwyniana sp.Perditomorpha leuco



Perditomorpha ruPerditomorpha stiborhiKylopasiphae pruinosa

Perditomorpha sp.Niltonia virgilii

Chilicolletes delahozii







Fig. 5. Majority-rule consensus phylogram resulting from mixed-model Bayesian analysisand 28S rRNA genes from 122 species of colletid bees and 22 species of other bee famil

and S3: 81% posterior probability; ML bootstrap = 50; parsimonybootstrap = 12). The Bayesian posterior probability value is lowerthan that for the majority of other clades, which are in general sup-

locandrena porteriooksihti

Nolanomelissa toroiCalliopsis fractaMelitturga clavicornis

Panurgus calcaratus

Protoxaea gloriosa

Agapostemon tyleriMexalictus arizonensis

Halictus rubicundusAugochlorella pomoniellaDieunomia nevadensis

us wilmattaea mullerirnis


Zikanapis clypeataPtiloglossa tarsata

Ptiloglossa sp.Ptiloglossa thoracica

Willinkapis chalybaeaupolicana yarrowi

olicana bicoloraupolicana vestitarifasciata


soma fallaxrosoma aterrimum

Hemicotelles ruizii

Colletes compactus

Colletes floralisColletes simulans

Colletes thoracicusColletes inaequalis

Colletes skinneriColletes pascoensis

Colletes distinctus

Colletes gilvusColletes furfuraceus

Colletes bicolor

Colletes seminitidusXanthocotelles sicheli

Rhynchocolletes mixtusallomelitta antipodes Euhesma sp.ohesma calliopsella platyrhinama aff. crabronica

Euryglossina globulicepsthesma furciferarapter heterodoxusapter ruficornislgoensisns

Xeromelissa australisXeromelissa sp.

Xeromelissa irwiniXeromelissa nortina

Xeromelissa rozeniGeodiscelis longiceps

Xenochilicola mamignaChilicola (Anoediscelis) herbsti

Chilicola (Pseudiscelis) rostrataChilicola (Oediscelis) vicugnaHyleoides concinna

Meroglossa itamucaAmphylaeus (Agogenohylaeus) obscuriceps

Palaeorhiza (Heterorhiza) sp.Palaeorhiza (Palaeorhiza) sp.

Hylaeus (Macrohylaeus) alcyoneusHylaeus (Euprosopis) disjunctus

Hylaeus (Euprosopis) elegansHylaeus (Rhodohylaeus) proximus

Hylaeus (Gnathoprosopis) amiculus

Hylaeus (Pseudhylaeus) aff. simplus



asiphae mirabilisrenopsis sp.acolletinae sp.proctus megachalcoidesprocolletes chalybeataproctus lanceolatuses sp.

. velutinuscolletes bilobatusproctus conospermi

Leioproctus pappusGoniocolletes fimbriatinus

Goniocolletes perfasciatusProtomorpha aff. alloeopus

aff. aspers pachyodontus


inimus sp.



chopria punctatissimaEulonchopria simplicicrusralis


stomaha laenasula anthracinaglossula communisda missionica


hopria (Biglossa) robertsihopria (Biglossa) sp.onchopria (Lonchopria) similis


of 5498 aligned bp of the EF-1a (exons and introns), opsin (exons), wingless (exons),ies.

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Table 6Support for the monophyly of Colletidae, colletid subfamilies, and clades formed by Euryglossinae, Hylaeinae, Scrapterinae, and Xeromelissinae, assessed using Bayesian posteriorprobabilities of individual gene loci (‘‘n.r.” is used to indicate clades not recovered by individual loci).

EF-1a, exons EF-1a introns Opsin Wingless 28S rRNA Combined

Colletidae 100 100 100 93 100 100Colletinae s.str. 100 100 100 97 100 100Diphaglossinae 85 93 100 82 63 100Euryglossinae 98 77 96 n.r. n.r. 100Hylaeinae 100 100 100 100 n.r. 100‘‘Paracolletinae”* n.r. n.r. 78 n.r. n.r. 100Scrapterinae 100 100 100 98 98 100Xeromelissinae 100 100 100 100 n.r. 100Euryglossinae + Scrapterinae 74 57 99 n.r. n.r. 100Hylaeinae + Xeromelissinae 93 89 n.r. n.r. n.r. 99Eurygl. + Scrapt. + Hylaei. + Xerom. 80 n.r. 100 n.r. n.r. 100

* Clade formed by all representatives of Paracolletinae except Callomelita antipodes and Paracolletes cfr. crassipes.










































































































































































e f



Fig. 6. Alternative tree topologies statistically compared using likelihood-based tests and Bayesian information content. The resulting topology of an unconstrained Bayesiananalysis of the combined data set (a) was compared in a pair-wise manner to five alternative topologies (b–f) with various placements of Callomelitta antipodes andParacolletes cfr. crassipes.

Table 5Results of comparisons among alternative topologies for Colletidae using maximum likelihood (Kishino–Hasegawa and Shimodaira–Hasegawa tests) and Bayesian approaches.ML tests, as implemented in PAUP� using a one-tailed test of significance (p-value for both tests was identical in all pair-wise comparisons made). Harmonic means from MrBayesanalyses and Bayes factor comparisons: 2loge(B10) stands for twice the log of the Bayes factor in the comparison between two topologies. All comparisons were made between theunconstrained tree topology and the alternative constrained topologies.

Tree topology �lnL Diff. �lnL p-Value Harmonic mean 2loge(B10)

Unconstrained tree topology (Fig. 7a) 85524.62207 �78986.35Paracolletes constraint 1 (Fig. 7b) 85531.55656 6.94 0.258 �79007.35 42.00***

Paracolletes constraint 2 (Fig. 7c) 85558.56353 33.93 0.020* �79023.13 73.56***

Callomelitta constraint 1 (Fig. 7d) 85527.1818 2.56 0.264 �78990.34 7.98**

Callomelitta constraint 2 (Fig. 7e) 85521.8022 2.82 0.335 �78990.34 7.98**

Callomelitta constraint 3 (Fig. 7f) 85524.10473 0.52 0.481 �78992.79 12.88***

* Statistically significant difference of likelihood scores at p = 0.05.** Strong evidence against null hypothesis, i.e., tree topologies equally likely—as proposed by Kass and Raftery (1995, 277).

*** Very strong evidence against null hypothesis (Kass and Raftery ibid).

304 E.A.B. Almeida, B.N. Danforth / Molecular Phylogenetics and Evolution 50 (2009) 290–309

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ported by values equal or higher than 90%. The three basal-mostnodes of ‘‘Paracolletinae” in the Bayesian and ML phylograms re-veals very short internodes (Figs. 5 and S2). These groupings areweakly supported by parsimony and ML bootstrap proportions,but are well-supported by Bayesian posterior probabilities. NeitherML nor parsimony analyses yield alternative arrangements of thetaxa shown as basal in the ‘‘Paracolletinae” clade.

The majority of the Paracolletinae were shown to form a well-supported clade, which comprises most groups traditionally com-prised in this subfamily, except Paracolletes, Callomelitta, Anthoglos-sa, Trichocolletes, and Lonchopria. This clade roughly corresponds toLeioproctus s.l. (e.g., Michener, 1965, 1989, 2007), although a num-ber of paracolletine genera recognized by Michener (2007) renderLeioproctus s.l. paraphyletic. Three main lineages recovered withinthis clade: (1) an entirely Australian clade which comprises Baeo-colletes, Goniocolletes and relatives; (2) a Neotropical clade that in-cludes Eulonchopria, Niltonia and related genera; and (3) anotherNeotropical group formed by Halictanthrena, Reedapis and relatedgenera. Relationships among these three groups are not firmlyestablished by any of the analytical methods employed for phylo-genetic estimation. The internodes on this part of the tree are veryshort (Figs. 5 and S2), making the recovery of unambiguous phylo-genetic information difficult. The above mentioned clade formedby Australian paracolletine bees contains a well-supported subc-lade which corresponds to Leioproctus s.str., Goniocolletes and re-lated genera. This unnamed clade not only contains enoughsequence synapomorphies to render high support values(Fig. 4b), but also has exceptionally long introns in the non-codingregions of EF-1a (intron 2) and opsin (intron 3) (Danforth and Al-meida, unpublished data).

Five partition trees, resulting from Bayesian analyses of theindividual partition data sets (introns and exons of EF-1a, exonsof opsin and wg, and 28S rRNA), are shown in Figs. S4–S8 (Supple-mentary materials). All five partitions, independently (Table 6), orcombined recovered colletid monophyly. The relationships be-tween Colletidae and outgroups agree with the molecular resultsobtained by Danforth et al. (2006a,b). Moreover, relationshipswithin Andrenidae and within Halictidae fully agree with more de-tailed studies of these two bee families conducted previously(Ascher, 2004; Danforth et al., 2004, respectively).

Additional investigation of the resolution power provided byeach gene showed a different (and more fundamental) role of EF-1a and opsin compared to wg and 28S rRNA in the phylogeneticanalyses (Fig. 7). The former two were particularly effective inresolving the earliest divergences among colletid lineages (Fig. 7:





1all nodes

Paracolletinaedeep nodes


















Fig. 7. Congruent topological information (CTI) of partition Bayesian trees incomparison to the combined Bayesian tree topology (see Section 2 for CTIcalculation). CTI was computed for (1) the complete set of possible relationshipswithin Colletidae (‘‘all nodes”); (2) 17 deeper nodes within the ingroup (list ofnodes in Supplementary Appendix 2); and (3) nodes within ‘‘Paracolletinae”, toinfer on the capacity of the individual loci to recover more recent relationships.

‘‘deep nodes”). Opsin and EF-1a contained information to resolvemore recent divergences as well, as measured by the congruencebetween paracolletine nodes in each of the gene partition treesand the combined tree (Fig. 7: ‘‘Paracolletinae”). These two genesare highly informative as compared to the other data partitions(Table 3), and high information content appears to translate intophylogenetic signal needed to resolve different regions of the col-letid tree topology.

4. Discussion

Stable classifications are ultimately dependent on establishing awell-corroborated phylogenetic hypothesis for groups of organ-isms. For many taxonomically difficult groups of bees, much ofthe current classifications may be unsatisfying primarily becauseit is often not based on such a robust phylogenetic hypothesis.Molecular data can substantially clarify difficult and confusingphylogenetic matters. Colletidae and, specifically, Colletinae s.l.are examples of this. In Michener (2007, 136) words: ‘‘[i]t is clearthat the Colletinae includes diverse elements. A needed step is aphylogenetic study of the forms here placed in Colletinae”.

The continued addition of ideas and information to the discus-sion of relationships among lineages of Colletidae seems to haveprogressed in ways congruent with the results found by the cur-rent study. Rozen (1984) conjectured that Diphaglossinae shouldconstitute the sister-group to all other colletid bees. Rozen’shypothesis was based on diphaglossine bees being the only collet-ids known to spin a cocoon, and the interpretation that this behav-ior (and morphology associated with it) could hardly have re-evolved from non-cocoon-spinning ancestors (Rozen, 1984). Thesister-group relationship between Diphaglossinae and the remain-ing colletid subfamilies is strongly supported by the molecularphylogenetic results.

4.1. Molecular data and the phylogeny of Colletidae

The degree of phylogenetic resolution and the relatively strongsupport at many nodes obtained with the various methods testedin this study are very encouraging. This is the first phylogeneticstudy of Colletidae with extensive taxon sampling to provide awell-resolved hypothesis for the relationships on a worldwidescale. It is noticeable, however, that some regions of the trees arecharacterized by low support values. Future research may demon-strate that these weakly supported nodes are inherently hard to re-solve, instead of having been caused by insufficient data.Parametric branch lengths (Figs. 5 and S2) reveal very short inter-nodes at various parts of the tree of Colletidae, which suggest rapiddiversification among the early-diverging colletid lineages. Consid-ering that a relatively large amount of data was used and that thosedata came from genes appropriate for resolving the relationshipsamong colletid subfamilies, low support may indeed derive froma rapid radiation (Whitfield and Kjer, 2008).

The improved phylogenetic resolution obtained in the com-bined analysis of all gene data partitions as compared with theindividual partitioned analyses is readily appreciated when Figs.S4–S8 and Figs. 4, S1, and S3 are contrasted. In general, individualdata partitions are expected to provide lower resolution than asimultaneous analysis. Moreover, phylogenetic noise present inindividual partitions may obscure the true signal that is amplifiedwhen all data are combined (Nixon and Carpenter, 1996; Baker andDeSalle, 1997).

The phylogenetic signal present in EF-1a alone recovered therelationships among the major lineages of Halictidae (Danforth,2002), which largely agreed with the morphological results of Pes-enko (1999). Later, addition of genetic data from opsin and wg did

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not alter the deeper relationships for an analysis of basically thesame set of taxa, but resulted in increased support values for mostinternodes (Danforth et al., 2004). Phylogeny inferred from EF-1awas, among the genes sampled by Danforth et al. (2004), the mostresolved tree. Likewise, EF-1a alone was sufficient to resolve rela-tionships within Andrenidae (Ascher in Rozen, 2003, Fig. 37). Thisresult is strengthened by the high degree of observed congruencewith the morphological data set collected by Ascher (2004). And-renidae comprise approximately 2650 species, a wide distributionand a morphological diversity comparable to Colletidae. Ascher’stree based on this one locus was well-resolved and relationshipswere also well-supported by bootstrap proportions and Bremersupport values (Ascher, 2004, 43).

In our study too, EF-1a seem to provide most of the meaningfulphylogenetic signal for the analysis of colletid relationships (Fig. 7and Table 6), followed by opsin. The parameter a of the gammadistribution is a correlate of data set quality in empirical and sim-ulation studies (Yang, 1998; Lin and Danforth, 2004). It is higher inthe exons of EF-1a and opsin compared to those of wg and in 28SrRNA, reflecting less heterogeneity in among-site rate variation inEF-1a and opsin as compared to wingless and 28S (Fig. 3c).

Differences in the diverse measures of clade support assessmentwere expected given their differing natures. Parsimony relies onabsolute number of changes, whereas maximum likelihood andBayesian phylogenetics depend on the likelihood function. Eventhough phylogenetic estimates are expected to converge in certainsituations (Steel and Penny, 2000; Swofford et al., 2001), it is alsotrue that different phylogenetic methods may extract differentinformation from the same data set. Overall, the topologies foundby the three methods are almost identical, most of the differencebeing on support for certain clades.

Bootstrap and posterior probabilities are not easily compara-ble, despite the efforts of some researchers to find ways to linkthem (e.g., Wilcox et al., 2002; Alfaro et al., 2003; Huelsenbeckand Ranalla, 2004). The bootstrap has long been used as anassessment of support of clades in phylogenetic analyses; poster-ior probabilities are more recent and less well-understood (Huel-senbeck et al., 2002, 683–684 for a discussion). Huelsenbeck andRanalla (2004) used simulations to demonstrate that Bayesianposterior probabilities can be a useful measure of phylogeneticreliability as long as the substitution model is not violated.Empirical studies found Bayesian posterior probabilities to beuseful measures of support as well (e.g., Wilcox et al., 2002).Comparisons among various models of different levels of com-plexity in this study showed the topology to be very resilientto these changes. Posterior probabilities changed in some cases,usually varying by less than 10%. This serves as evidence thatthe Bayesian analysis of the current data set was not very sensi-tive to model misspecification and renders credible the posteriorprobability values obtained.

4.2. Monophyly of Colletidae

Colletid monophyly is well-established. Sequence data fromthis study and larger analyses of bee relationships (Danforthet al., 2006a,b) consistently support it. All colletids whose nestshave been studied line the brood cells with a polyester materialunique among bees (Hefetz et al., 1979; Espelie et al., 1992; Almei-da, 2008), and morphological characteristics of the colletid glossamay be associated with this lining (McGinley, 1980). Results alsoconfirm that Strenotridae do not belong within the Colletidae.Stenotritids are different from colletids in terms of their nest con-struction and bionomy (Houston and Thorp, 1984), as well as mor-phology (McGinley, 1980). Based on larval morphologicalcharacters alone, Paracolletinae and Stenotritidae were groupedtogether by McGinley (1981). Stenotritidae constitutes the sister-

group of Colletidae according to results of this analysis and in Dan-forth et al. (2006a,b).

4.3. Subfamilies of Colletidae

Historically, Colletes and other hairy colletid groups (generallyincluding Diphaglossinae) have been placed separately from Hyla-eus and relatives (e.g., Ashmead, 1899). It had been supposed thatHylaeinae, Xeromelissinae, and Euryglossinae formed a distinctgroup within the Colletidae, despite the enormous variation inways colletid subfamilies were imagined to relate to each other(Fig. 1). The presumed phylogenetic proximity of Hylaeinae, Xer-omelissinae, and Euryglossinae was encountered in analyses ofmorphological data (Alexander and Michener, 1995; McGinley,1981), but, despite their proximity, they do not form a naturalgroup unless Scrapter is also included. Accumulation of evidencethat Scrapter does not belong with the remaining Paracolletinaelead to the recent recognition of an independent monogeneric unit:Scrapterinae (Melo and Gonçalves, 2005; Ascher and Engel in En-gel, 2005; Ascher and Engel, 2006). A sister-group relationship be-tween Scrapter and Euryglossinae had been suggested by a variablebut interesting morphological character: some species of both taxapossess a unique (among bees) basitibial plate not delimited by acarina, ‘‘but by a ring of large tubercles probably which are a resultif subdivision of the normally elevated plate” (McGinley, 1981,160). Additionally some larval characters support the sister-grouprelationship between Scrapterinae and Euryglossinae (McGinley,1981; see comments by Engel, 2005; Ascher and Engel, 2006; Da-vies and Brothers, 2007), even though the analysis of the entire lar-val data set does not support this finding (McGinley, 1981). Resultspresented here unambiguously corroborate previous proposals ofplacing Scrapter in a separate subfamily and its close relationshipto the Euryglossinae, despite the morphological disparity betweenthem.

The results do not provide evidence for the grouping of Colleti-nae s.str. and Paracolletinae, contrary to the common and longused practice of uniting them (e.g. Michener, 1944, 1965, 1989,2007 treated these two groups as tribes comprised into Colletinaes.l.). The proposal of keeping the two subfamilies as separate taxa(e.g., Silveira et al., 2002; Engel, 2005; Melo and Gonçalves, 2005)is compatible with the phylogenetic findings presented here(Fig. 4).

The need for additional investigation to support the separationof Callomelitta and Paracolletes from Paracolletinae becomes evi-dent from the phylogenetic results. Although the phylogeneticaffinities of Callomelitta and Paracolletes to the colletid lineages re-main uncertain, there is strong evidence to assert that neither ar-ose from within one of the formally recognized subfamilies.According to the phylogenetic analysis and the statistical topolog-ical tests (Table 5), it is possible that Callomelitta should be placedas sister-group to all other Paracolletinae, but this is not necessar-ily the case. Based on these phylogenetic results and on the obser-vation of the distinctive morphology of these bees (Michener,2007), the recognition of a separate subfamily to harbor Call-omelitta would be a reasonable solution for the placement of thisgenus (Almeida, 2008b).

Colletinae s.str. is a clade subtended by a fairly long branch, rel-ative to other internodes of Colletidae (Figs. 5 and S2). It is possiblethat the attraction of Callomelitta to the proximity of Colletinae wasartifactual, a long branch effect. Other kinds of data are needed toelucidate this matter: morphological data should not be affected bya possible long branch effect in the same way as molecular data(Bergsten, 2005).

The placement of Paracolletes is another serious issue, because itentails the nomenclatural modification needed for the clade provi-sionally referred to by ‘‘Paracolletinae”. Paracolletes is the type

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genus of Paracolletinae and, therefore, its name-bearer taxon. Fam-ily-group names with the root ‘‘Paracollet-” must, as a result, in-clude Paracolletes.

4.4. Genus-level classification of the ‘‘Paracolletinae”

Michener (2007, 145) states his awareness that Leioproctus s.l.most certainly does not constitute a natural group, but he acknowl-edges its usefulness as a diagnosable taxonomic unit. Leioproctuss.l. is a group recognizable on the basis of superficial similarity ofits subgenera and the lack of synapomorphies present in othergroups, such as Neopasiphae or Eulonchopria. Michener (2007,141–142) resorted to caution in changing the classification:‘‘[u]ntil more species are known and cladogeny is better studied,especially in the diverse Australian fauna, there is no point inattempting a new classification, for new combinations that wouldlast only until the next revision would be the result”.

Leioproctus s.l. (e.g. Michener, 2007) is rendered paraphyletic bya number of lineages that arise from within it. Its distinction hasbeen traditionally made on the basis of symplesiomorphies, andthe remaining groups being characterized by synapomorphies. Itis not surprising, then, to find highly modified (morphologicallyautapomorphic) lineages arising from within it and being recog-nized as distinct genera, e.g., Brachyglossula, Eulonchopria, Neopa-siphae, Phenacolletes. Part of the problem is resolved by elevatingthe subgenera of Leioproctus to the status of genus. This view hasbeen long adopted by most South American bee taxonomists,who have traditionally treated all supra-specific taxa of SouthAmerican Paracolletinae as separate genera (e.g., Moure et al.,2007; Silveira et al. 2002). In this case, the genus Leioproctus is re-stricted to the Australian region. However, the classification ofParacolletinae will require future adjustments at the generic levelbecause the phylogenetic results very clearly show that at leasttwo large genera constitute artificial assemblages: Perditomorphaand Leioproctus s.str. even when many subgenera are raised to gen-eric rank.

4.5. Biogeography

Colletidae are distributed primarily in the southern hemisphereand comprise various endemic groups in Australia, South America,and Africa. As discussed elsewhere, the current distribution ofcolletid bees suggests the occurrence of various events of Austra-lian-South American interchanges in the past (Almeida et al.,unpublished results). Paracolletinae is formed by various clades,some endemic to the Australian region, some South American. Ina similar fashion, Hylaeinae and Xeromelissinae form a clade inwhich the former is primarily Australian and the latter occurs fromsouthern South America up to Central America.

Note added on proof

Publication of the article by Almeida (2008b) while the presentpaper was in press made available the name Andrenopsis micheneri-anus Almeida for the species referred to as ‘‘Paracolletinae sp.” inTable 1, and Figs. 4b, 5, S1–S8.


Our thanks for comments on earlier versions of this paper toLaurence Packer, James K. Liebherr, and Richard G. Harrison. Dis-cussions with Charles Michener, John Ascher, Terry Houston, GlynnMaynard, Gabriel Melo, and Gregg Davies contributed to the devel-opment of this research. Seán Brady, Jenn Fang, Karl Magnacca, andSedonia Sipes provided valuable advice concerning the molecular

work. We are indebted to all who supplied specimens used forDNA extraction: Antonio Aguiar, Isabel Alves dos Santos, JohnAscher, Torsten Dikow, Martin Hauser, Terry Houston, Karl Magna-cca, Gabriel Melo, Claus Rasmussen, Jerome Rozen, Andrew Short,Lorenzo Zanette, and Amro Zayed. We are mostly indebted to Lau-rence Packer for his generosity in providing samples of a largenumber of rare colletid species. We are grateful for the bee taxon-omists listed in the methods section for assistance with the identi-fication of taxa included in the present study. Assistance for fieldtrips was given by Paulo Almeida, Ricardo Ayala, Ricardo Botelho,Guillermo Debandi, Mariano Devoto, Eduardo Dominguez, ConnalEardley, Dimitri Forero, Terry Houston, Laurence Packer, CharlotteSkov. Collecting permits in Argentina and Australia were facilitatedby the competent work of Roberto Salinas (Servicio de Fauna Sil-vestre, Catamaca, Argentina); Gustavo Solá (Dirección de RecursosNaturales Renovables, Mendoza, Argentina); Ing. Ana Inés Arce(Secretaría de Medio Ambiente y Desarollo Sustentable, Salta,Argentina); Lic. Claudia Perez Miranda (Dirección de RecursosNaturales y Suelos, Tucumán, Argentina), and Mr. Danny Stefony(CALM Wildlife Branch, Western Australia). The majority of fund-ing for this research came from a National Science Foundation Re-search Grant in Systematic Biology to B.N. Danforth and E.A.B.Almeida (DEB-0412176). Additional funding was provided by theA.C.Rawlins Endowment (Cornell University); Grace Griswold Fund(Cornell University); Tinker Foundation & Latin American StudiesProgram (Cornell University). E.A.B. Almeida is grateul to Fundaçãode Coordenação de Aperfeiçoamento de Pessoal de Nível Superior(CAPES: Brazilian Ministry of Education) for a Ph.D. scholarship(BEX-0967/01-7) and to CNPq for a post-doctoral fellowship(PDJ-150626/2007-0).

Appendix A. Supplementary data

Supplementary data associated with this article can be found, inthe online version, at doi:10.1016/j.ympev.2008.09.028.


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