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Phylogeny of the Xeromelissinae (Hymenoptera: Colletidae) Based Upon Morphology and Molecules*

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Phylogeny of the Xeromelissinae (Hymenoptera: Colletidae) Based Upon Morphology and Molecules* Apidologie 39 (2008) 75–85 Available online at: c INRA/DIB-AGIB/ EDP Sciences, 2008 www.apidologie.org DOI: 10.1051/apido:2007063 Original article Phylogeny of the Xeromelissinae (Hymenoptera: Colletidae) Based upon Morphology and Molecules* Eduardo A.B. Almeida1,3,LaurencePacker2,BryanN.Danforth1 1 Comstock Hall, Department of Entomology, Cornell University, Ithaca, NY, 14853 USA 2 Department of Biology, York University, Toronto, Ontario, M3J 1P3, Canada 3 Current address: Departamento de Zoologia, Universidade Federal do Paraná, Cx. Postal 19020, CEP: 81531-980, Curitiba, P.R. Brazil Received 18 June 2007 – Revised 15 October 2007 – Accepted 30 October 2007 Abstract – We present the results of a combined analysis of 248 morphological characters and sequences from 3 genes for 29 species of Xeromelissinae and 7 outgroup taxa including representatives of the colletid subfamilies Colletinae, Euryglossinae, Hylaeinae, Paracolletinae, and Scrapterinae. The paracolletine genus Trichocolletes was used to root the tree. The results agree with most of those obtained in an earlier, entirely morphological analysis. Noteworthy are (1) the paraphyly of Chilimelissa in relation to Xeromelissa,and(2) the lack of sister group relationship between Hylaeinae and Xeromelissinae. Other than minor rearrange- ments resulting from swapping adjacent nodes, the only major difference is the placement of one species of Chilicola, C. aenigma, which no longer groups within C. (Chilioediscelis), but instead appears to be closer to Xenochilicola. The influence upon phylogenetic results caused by highly morphologically autapomorphic taxa is discussed. bee / Colletidae / phylogeny / Neotropical / Xeromelissinae 1. INTRODUCTION There are four currently recognized genera, the phylogenetic relationships among which, ac- Xeromelissinae is a subfamily of Colletidae cording to Packer’s (2008) analysis of a large of moderate size (approximately 200 species) number of morphological characters, are sum- all of which are restricted to the New World. marized in Figure 1. As the name implies, these bees are generally Only Chilicola has been considered large found in xeric habitats, mostly in temperate ar- and/or diverse enough to warrant division into eas of southern South America. Xeromelissine subgenera, of which there are now fifteen. bees are typically small to minute, and gener- Chilimelissa, as commonly recognized (e.g. ally slender. Michener, 2000) is comparatively speciose The taxonomy of Xeromelissinae has had and diverse, although no formal subdivision a complex history, summarized by Packer into subgenera has yet been made as phy- (2008). No tribal divisions are currently ac- logenetic analysis of it remains incomplete. cepted within the subfamily: the previous Xenochilicola comprises three species, and tribal level classification having been dis- Xeromelissa is monotypic and only includes X. pensed with by Michener and Rozen (1999). wilmattae Cockerell. Packer (2008) found Xe- Corresponding author: Eduardo A.B. Almeida, romelissa to render Chilimelissa paraphyletic, [email protected] and as a consequence proposed a revised * Manuscript editor: Bryan Danforth generic classification for Xeromelissinae. Online material is available at: The purpose of the present paper is to test http://www.apidologie.org Packer’s classification of the Xeromelissinae Article published by EDP Sciences and available at http://www.apidologie.org or http://dx.doi.org/10.1051/apido:2007063 76 E.A.B. Almeida et al. Figure 1. Summary of phylogenetic relationships among xeromelissinae genera according to the analysis of the morphological data set by Packer (2008: Figs. 1 and 2). by comparing results among morphological, we use the paracolletine genus Trichocolletes to molecular and total evidence analyses. root the entire tree, including Colletes. This deci- sion is based upon results of a higher level phy- logeny of the entire Colletidae (Almeida, 2007). 2. METHODS In instances where only one sex is known for a species that was used in the molecular data set, that 2.1. Taxon sampling sex was coded for the morphological characters and a closely related species was used for the other sex. Different taxa were available in a form suitable This was necessary twice: females of Chilicola tri- for DNA sequencing than were used in the pre- carinatoides Packer and males of Cc. liliana Packer vious morphological analysis. Consequently, there are unknown. Females of Cc. tricarinata Packer and are fewer representative subgenera of Chilicola,but males of Cc. olmue Toro and Moldenke, respec- more species of Chilimelissa, than in the earlier tively, were used in their place. Similarly, there are a study and the remaining two genera are represented few cases where the species that was sequenced was by only a single species each. Chilicola is abbrevi- very closely related to one that was studied mor- ated as “Cc.”, Chilimelissa as “Cm.”, and Colletes phologically, these taxa were combined in the to- as “Co.”. There are also differences in the outgroups tal evidence analysis. Thus Cc. unicarinata Packer used for molecular and morphological analyses. In and Cc. chubutense Packer; Cc. andina Toro and some cases (such as Hylaeus affinis (Smith)), the Moldenke and Cc. araucana Toro and Moldenke; same outgroups available for DNA were scored Cc. mantagua Toro and Moldenke and Cc. vicugna for the morphological characters. In others, only Toro and Moldenke; Cc. brzoskai Michener and Cc. congeners could be used, with the result that Col- (Oroediscelis) sp. were used for morphological and letes cunicularius L., Scrapter nitida Friese, Euh- molecular data, respectively. esma halictoides (Rayment), and Callohesma cal- In total, 36 taxa were included in the analyses, liopsiformis (Cockerell) were used for morphology 7 representing outgroups. The complete list of taxa whereas Co. bicolor Smith, S. niger Lepeletier and and their provenances are provided in Table S1 (on- Serville, E. crabronica (Cockerell), E. platyrhina line material). (Cockerell), and Ca. calliopsella (Cockerell) were sequenced. Packer (2008) used Colletes to root the entire tree (which included representatives of three 2.2. Morphological characters other subfamilies related to the Xeromelissinae – Hylaeinae, Euryglossinae, and Scrapterinae1). Here We simply scored all exemplars for the same 1 The choice of usage of Scrapterinae Melo and characters as were used by Packer (2008) and do not Gonçalves over Scraptrinae Ascher and Engel is reiterate the characters or their states here. In cases discussed in Appendix 1 (online material). where additional character states were required for Phylogeny of Xeromelissinae 77 the different suite of species used, these are de- low melting point agarose gels (FMC, Rockland, scribed in Appendix 2 (online material). Similarly, Maine) overnight at 4 ◦C. DNA was recovered from we only present the data matrix for those taxa not gel slices using the Promega Wizard PCR Preps included in the previous analysis (Appendix 3: on- DNA Purification kit. Gel purification was unneces- line material). sary for PCR products that produced a single prod- uct: both fragments of 28S rRNA and the upstream 1100 bp fragment of EF-1α. Automatic DNA se- 2.3. Choice of molecular data quencing was performed using the Applied Biosys- tems Automated 3730 DNA Analyzer employing Molecular data were collected from three gene Big Dye Terminator chemistry and AmpliTaq-FS loci that have been providing robust results for in- DNA Polymerase at Cornell University Life Sci- sect phylogenetic studies (Danforth, 1999; Danforth ences Core Laboratories Center. et al., 2004). Elongation factor-1 alpha, F2 copy (EF-1α) and the large subunit 28S rRNA locus (28S rRNA), regions D1–D5 were chosen to resolve 2.5. Data analysis deeper relationships among outgroup and ingroup taxa, and within Xeromelissinae as well. These 2.5.1. Alignment genes have been used to successfully recover Ter- tiary to Cretaceous age divergences in bee phylo- Alignments were generated using similarity cal- genies (e.g., Danforth et al., 1999, 2004, 2006a, culated at the nucleotide level (“-n”) with DI- b). EF-1α has been the most widely used nuclear ALIGN 2.2 (Morgenstern, 1999) and corrected protein-coding gene for insect phylogenetics (see manually for obvious alignment errors using Mac- Danforth et al., 2004, pp. 310–311 for comments on Clade v. 4.08 OSX (Maddison and Maddison, 2005) this gene) The third gene sampled was cytochrome and Winclada 1.00.08 (Nixon, 2002). For EF-1α, oxidase 1 (COI), a mitochondrial protein-coding the honey bee (Apis mellifera) sequence was used gene known for its utility in species-level phyloge- to establish reading frames and intron/exon bound- netic studies of insects (e.g. Danforth, 1999). aries. In cases where multiple sequences were avail- Primer information for each gene is presented in able for the same species, the sequences were Table S2 (online material). merged after being resolved in the same clade in preliminary analyses and resulting partial polymor- phisms were kept as such. 2.4. DNA extraction, PCR, and sequencing 2.5.2. Phylogenetic analyses using Genomic DNA was extracted using phenol- parsimony chloroform protocols (Doyle and Doyle, 1990, adapted by Danforth, 1999) but without use of liq- Raw data files were edited with Winclada uid nitrogen and RNase. Tissue was taken from the (Nixon, 2002) and this program was used to ex- thoracic musculature and/or legs depending on the port to TNT version 1.1 (Goloboff et al., 2004). Se- rarity and size of
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