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Phylogeny of the Bee Family Megachilidae (Hymenoptera: Apoidea) Based on Adult Morphology

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Phylogeny of the Bee Family Megachilidae (Hymenoptera: Apoidea) Based on Adult Morphology 1 Phylogeny of the bee family Megachilidae (Hymenoptera: Apoidea) based on adult morphology 2,3 VICTOR H. GONZALEZ1 ,TERRYGRISWOLD1 ,CHRISTOPHE J.PRAZ , 2 B RYA N N. D A N F O RT H 1USDA-ARS, Bee Biology and Systematics Laboratory, Utah State University, Logan, UT, U.S.A., 2Department of Entomology, Cornell University, Ithaca, NY, U.S.A. and 3Laboratory of Evolutionary Entomology, University of Neuchatel, Neuchatel, Switzerland Abstract. Phylogenetic relationships within the bee family Megachilidae are poorly understood. The monophyly of the subfamily Fideliinae is questionable, the relation- ships among the tribes and subtribes in the subfamily Megachilinae are unknown, and some extant genera cannot be placed with certainty at the tribal level. Using acladisticanalysisofadultexternalmorphologicalcharacters,weexploretherela- tionships of the eight tribes and two subtribes currently recognised in Megachilidae. Our dataset included 80% of the extant generic-level diversity, representatives of all fossil taxa, and was analysed using parsimony. We employed 200 characters and selected 7 outgroups and 72 ingroup species of 60 genera, plus 7 species of 4 extinct genera from Baltic amber. Our analysis shows that Fideliinae and the tribes Anthidiini and Osmiini of Megachilinae are paraphyletic; it supports the monophyly of Megachilinae, including the extinct taxa, and the sister group relationship of Lithurgini to the remaining megachilines. The Sub-Saharan genus Aspidosmia,a rare group with a mixture of osmiine and anthidiine features, is herein removed from Anthidiini and placed in its own tribe, Aspidosmiini, new tribe.Protolithurgini is the sister of Lithurgini, both placed herein in the subfamily Lithurginae; the other extinct taxa, Glyptapina and Ctenoplectrellina, are more basally related among Megachilinae than Osmiini, near Aspidosmia,andarehereintreatedatthetriballevel. Noteriades,agenuspresentlyintheOsmiini,ishereintransferredtotheMegachilini. Thus, we recognise four subfamilies (Fideliinae, Pararhophitinae, Lithurginae and Megachilinae) and nine tribes in Megachilidae. We briefly discuss the evolutionary history and biogeography of the family, present alternative classifications, and provide arevisedkeytotheextanttribesofMegachilinae. Introduction 1972; Michener, 2007; Pitts-Singer & Cane, 2011). Megachilid bees are found in a wide diversity of habitats on all conti- Megachilidae is the second largest bee family, containing nents except Antarctica, ranging from lowland tropical rain more than 4000 described species worldwide (Michener, 2007; forests to deserts to alpine environments. The diversity of nest- Ascher & Pickering, 2011). These solitary bees are both ing biology and floral relationships of Megachilidae is also ecologically and economically relevant; they include many astonishing. Diverse materials are used in nest building, includ- pollinators of natural, urban and agricultural vegetation. For ing mud, petals, leaves (intact pieces or macerated to a pulp), example, Megachile rotundata (Fabricius) has been introduced resin, soil particles, gravel and plant trichomes. The inclusion to many parts of the world as a pollinator of alfalfa (Bohart, of these foreign materials in nest construction may have pro- moted a massive range expansion and diversification within Correspondence: Victor H. Gonzalez, USDA-ARS, Bee Biology the family (Litman et al., 2011). Equally diverse are nesting and Systematics Laboratory, Utah State University, Logan, UT 84322- site choices: surfaces of walls, stones and tree branches; inside 5310, U.S.A. E-mail: [email protected] pre-existing cavities in the ground, wood, stems, galls and snail 2 shells; excavated in soil, wood or even in arboreal termite value of megachilid bees, their higher level classification and nests (e.g. Messer, 1984; Cane et al., 2007; Michener, 2007). phylogeny remain poorly understood. Some megachilid genera, subgenera or species are oligolec- tic (e.g. Wcislo & Cane, 1996), collecting pollen exclusively from related plant species or genera, and frequently exhibiting Classification and phylogeny unique associated morphological and behavioral adaptations The most widely accepted classificatory proposal for bees (e.g. Muller,¨ 1996; Thorp, 2000; Muller¨ & Bansac, 2004). (Michener, 2007) recognises seven extant families, although Other interesting adaptations are related to nesting biology. other proposals exist (for a discussion see Michener, 2007). In For example, females in several genera in the Anthidiini, com- Michener’s classification, Megachilidae is organised into two monly known as wool carder bees, make cotton wool-like subfamilies, eight tribes (one extinct), two extinct subtribes and brood cells from plant hairs or trichomes that they collect with 76 genera. An alternative proposal is that of Engel (2005), in their multidentate mandibles; also, some of them have a dense which some tribes are given subfamilial rank, some tribes are tomentum on the outer surfaces of their basitarsi, which help treated as subtribes and new tribes are proposed (Table 1). Two them absorb extrafloral trichome secretions that are then added taxa, now placed in the subfamily Fideliinae, were considered to those plant hairs to waterproof the cell, facilitate manipula- for a long time either as a distinct family or included within the tion, prevent microbial attack and to deter nest-robbing arthro- Apidae owing to a number of plesiomorphic features relative pods (Muller¨ et al., 1996; Michener, 2007). Megachilidae not only to Megachilidae, but also to other long-tongued bees also contains a large number of cleptoparasitic bees (cuckoo (Engel, 2002; Michener, 2007). However, the discovery of the bees). Nineteen genera, including an entire tribe (Dioxyini), immature stages as well as studies on their nesting biology and are cleptoparasites of other bees, thus making Megachilidae ethology suggested their closer affinity to the Megachilidae an important group for testing hypotheses on the origins of, (Rozen, 1970, 1973, 1977; McGinley & Rozen, 1987). and adaptations to, cleptoparasitic behaviour amongst bees. Roig-Alsina & Michener (1993), in their study of the long- Megachilids are also notable as the primary source of inva- tongued bees using both larval and adult external and internal morphological characters, provided the first exploration of sive bees, including multiple species in the genera Anthidium the phylogenetic relationships of Megachilidae. Fideliinae was Fabricius and Megachile Latreille (e.g. Cane, 2003; Michener, recovered as the sister group of the remaining megachilids in 2007). For instance, A. manicatum (Linnaeus) is perhaps the their analyses, but the subfamily appeared paraphyletic when most widely distributed unmanaged bee species in the world. both larval and adult characters were combined. Fideliinae is It was unintentionally introduced to North America in the late a small group with a disjunct distribution in the xeric areas of 1960s from Europe; and it is now established transcontinen- Asia, Africa and South America. The subfamily is segregated tally as well as in South America, New Zealand and the Canary into two very distinct tribes: Fideliini containing 14 species in Islands (Jaycox, 1967; Smith, 1991; Miller et al., 2002; Hoe- two genera, and Pararhophitini with three species in a single beke & Wheeler, 2005; Maier, 2005; Zavortink & Shanks, genus (Engel, 2002, 2004; Michener, 2007). 2008; Gibbs & Sheffield, 2009; Strange et al., 2011). Despite The other six tribes are currently grouped into the subfamily the ecological importance, evolutionary interest and economic Megachilinae. The distinctive nature of one tribe, Lithurgini, Table 1. Hierarchical suprageneric classifications of Megachilidae, including two proposals discussed in the text. Michener (2007) Engel (2005) Proposal 1 Proposal 2 (preferred) Subfamily Fideliinae Cockerell, 1932 Fideliinae Fideliinae Fideliinae Tribe Fideliini Cockerell, 1932 Fideliini Pararhophitinae Pararhophitinae Tribe Pararhophitini Popov, 1949 Neofideliini Engel, 2004 Megachilinae Lithurginae Subfamily Megachilinae Latreille, 1802 Pararhophitinae Anthidiini Lithurgini Tribe Anthidiini Ashmead, 1899 Lithurginae Aspidosmiini, new tribe Protolithurginia Tribe Dioxyini Cockerell, 1902 Lithurgini Ctenoplectrellinia Megachilinae Tribe Lithurgini Newman, 1834 Protolithurginia Dioxyini Anthidiini Tribe Megachilini Latreille, 1802 Megachilinae Glyptapinia Aspidosmiini, new tribe Tribe Osmiini Newman, 1834 Anthidiini Lithurgini Ctenoplectrellinia Subtribe Osmiina Newman, 1834 Anthidiina Megachilini Dioxyini Subtribe Ctenoplectrellina Engel, 2001a Dioxyina Osmiini Glyptapinia Subtribe Glyptapina Cockerell, 1909a Ctenoplectrellinia Protolithurginia Megachilini Tribe Protolithurgini Engel, 2001a Glyptapinia Osmiini Megachilini Osmiini Osmiina Heriadina Michener, 1941 a Extinct taxa. 3 possessing numerous plesiomorphic as well as distinctive apo- in the classification of Urban & Moure (2007). Some sub- morphic characters, resulted in subfamilial rank in the past (e.g. genera are monotypic or contain a few species with unusual Michener, 1944, 1983; Engel, 2005). Lithurgini is a small tribe, characters related to adaptations for pollen collecting (e.g. with 61 species and 3 genera, found on all continents except modified hairs on the mouthparts) or secondary sexual char- Antarctica. The monophyly of the group is not questioned. acters (e.g. spines on the hind coxa of the male) (Gonzalez & Except for the sister group relationship of Lithurgini
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