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The History of Early Bee Diversification Based on Five Genes Plus Morphology

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The History of Early Bee Diversification Based on Five Genes Plus Morphology The history of early bee diversification based on five genes plus morphology Bryan N. Danforth†, Sedonia Sipes‡, Jennifer Fang§, and Sea´ n G. Brady¶ Department of Entomology, 3119 Comstock Hall, Cornell University, Ithaca, NY 14853 Communicated by Charles D. Michener, University of Kansas, Lawrence, KS, May 16, 2006 (received for review February 2, 2006) Bees, the largest (>16,000 species) and most important radiation of tongued (LT) bee families Megachilidae and Apidae and the pollinating insects, originated in early to mid-Cretaceous, roughly short-tongued (ST) bee families Colletidae, Stenotritidae, Andreni- in synchrony with the angiosperms (flowering plants). Under- dae, Halictidae, and Melittidae sensu lato (s.l.)ʈ (9). Colletidae is standing the diversification of the bees and the coevolutionary widely considered the most basal family of bees (i.e., the sister group history of bees and angiosperms requires a well supported phy- to the rest of the bees), because all females and most males possess logeny of bees (as well as angiosperms). We reconstructed a robust a glossa (tongue) with a bifid (forked) apex, much like the glossa of phylogeny of bees at the family and subfamily levels using a data an apoid wasp (18–22). set of five genes (4,299 nucleotide sites) plus morphology (109 However, several authors have questioned this interpretation (9, characters). The molecular data set included protein coding (elon- 23–27) and have hypothesized that the earliest branches of bee gation factor-1␣, RNA polymerase II, and LW rhodopsin), as well as phylogeny may have been either Melittidae s.l., LT bees, or a ribosomal (28S and 18S) nuclear gene data. Analyses of both the monophyletic group consisting of both. The most recent morpho- DNA data set and the DNA؉morphology data set by parsimony logical analysis of family-level phylogeny in bees (17) obtained two and Bayesian methods yielded a single well supported family-level different tree topologies based on alternative coding of relatively tree topology that places Melittidae as a paraphyletic group at the few mouthpart characters. One tree topology places Colletidae as base of the phylogeny of bees. This topology (‘‘Melittidae-LT sister to the rest of the bees (‘‘Colletidae basal’’), whereas the other basal’’) is significantly better than a previously proposed alterna- places Melittidae s.l.ϩLT bees as sister to the rest of the bees tive topology (‘‘Colletidae basal’’) based both on likelihood and (‘‘Melittidae-LT basal’’). The major difference between the Col- Bayesian methods. Our results have important implications for letidae basal and Melittidae-LT basal topologies involves the place- understanding the early diversification, historical biogeography, ment of the root node of bees (27). Placing the root between host–plant evolution, and fossil record of bees. The earliest Colletidae and the rest of the bees yields the Colletidae basal branches of bee phylogeny include lineages that are predomi- topology, whereas placement of the root node near or within nantly host–plant specialists, suggesting that host–plant specificity Melittidae s.l. yields the Melittidae-LT basal topology. The biolog- is an ancestral trait in bees. Our results suggest an African origin ical implications of these alternative topologies are radically differ- for bees, because the earliest branches of the tree include pre- ent. The Colletidae basal topology implies an Australian and͞or dominantly African lineages. These results also help explain the South American origin for bees and suggests the earliest bees were predominance of Melittidae, Apidae, and Megachilidae among the a mix of floral generalists and specialists. Melittidae-LT basal earliest fossil bees. implies an African origin for bees and indicates that the earliest bees were likely to have been floral specialists. These alternative topol- bee phylogeny ͉ bee evolution ͉ molecular evolution ͉ ogies also have implications for understanding the fossil record and molecular systematics ͉ coevolution antiquity of bees. To resolve the root node of bees, we combined Ͼ4,000 bp of ngiosperms (flowering plants), with an estimated 250,000– DNA sequence data with the previous morphological data set of A260,000 species (1), represent the largest and most diverse Alexander and Michener (17). We report here the results of an lineage of vascular plants on earth. To Darwin, the rapid analysis of the largest molecular and morphological study to date on emergence and early diversification of the angiosperms was an ‘‘abominable mystery’’ (ref. 2 and refs. therein). Among the most Author contributions: B.N.D. and S.S. designed research; B.N.D., S.S., J.F., and S.G.B. important traits attributable to the explosive radiation of the performed research; S.G.B. contributed new reagents͞analytical tools; B.N.D. analyzed angiosperms is animal-mediated pollination (3–7). Insects are by data; and B.N.D. wrote the paper. Ϸ far the most important animal pollinators ( 70% of angiosperm The authors declare no conflict of interest. species are insect pollinated; ref. 8) and among insects, bees are Freely available online through the PNAS open access option. the most specialized and important pollinator group. All of the Ͼ Abbreviations: ST, short-tongued; LT, long-tongued; GTR, general time-reversible; IϩG, 16,000 species of bees living today (9) rely virtually exclusively gamma distribution plus a proportion of invariant sites; s.l., sensu lato; s.s., sensu stricto. on angiosperm products, including pollen and nectar for adult Data deposition: The sequences reported in this paper have been deposited in the GenBank and larval nutrition (10), floral oils for larval nutrition (11, 12), database (accession nos. listed in Table 4, which is published as supporting information on floral waxes and perfumes that serve as sexual attractants (13), the PNAS web site). The data matrix has been deposited in the TreeBASE database, and resins for nest construction (14). Bees are morphologically www.treebase.org (accession nos. M2878 and S1599). adapted to collecting, manipulating, carrying, and storing pollen †To whom correspondence should be addressed. E-mail: [email protected]. and other plant products (15, 16), and many bee species are ‡Present address: Department of Plant Biology, Life Science II 420, Mailcode 6509, Southern specialists on one or a few closely related host plants (10). Illinois University, Carbondale, IL 62901-6509. One step toward resolving Darwin’s ‘‘abominable mystery’’ is to §Present address: Department of Physiology, P.O. Box 245051, University of Arizona, develop a better understanding of the role that bees played in the Tucson, AZ 85724-5051. evolutionary history and diversification of the angiosperms. A ¶Present address: Department of Entomology and Laboratories of Analytical Biology, Smithsonian Institution, Suitland, MD 20746. robust phylogeny of bees would allow us to infer attributes of the ʈMelittidae in the sense of Michener (9) is a paraphyletic group based on our results. We early bees and to reconstruct the types of interactions that existed refer to the three melittid subfamilies as families, following an earlier suggestion by between the earliest bees and their angiosperm hosts. Higher-level Alexander and Michener (17). The three families are Melittidae (s.s.), Dasypodaidae, and (family- and subfamily-level) bee phylogeny is poorly understood. Meganomiidae. Currently, bees are divided into seven extant families: the long- © 2006 by The National Academy of Sciences of the USA 15118–15123 ͉ PNAS ͉ October 10, 2006 ͉ vol. 103 ͉ no. 41 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0604033103 Downloaded by guest on September 28, 2021 Cerceris sp. 77 Stigmus sp. 69 95 Clypeadon sp. 86 Philanthus gibbosus 80 Ochleroptera bipunctata 100 Bicyrtes ventralis 83 100 Bembix americana 100 98 100 Xerostictia sp. 97 100 Sceliphron caementarium Isodontia mexicana 100 99 61 100 Podalonia sp. 51 79 Anacrabro ocellatus 99 Plenoculus sp. 81 99 Tachysphex sp. 100 96 100 Hesperapis richtersveldensis 100 Hesperapis larreae 100 100 Hesperapis regularis 100 Dasypodaidae 100 75 Haplomelitta griseonigra 100 Dasypoda argentata 68 Dasypoda hirtipes 100 74 Dasypoda visnaga Meganomia binghami Meganomiidae 99 100 Macropis europaea 98 100 Macropis nuda 77 100 Rediviva mcgregori 88 100 100 Redivivoides simulans Melitta eickworti Melittidae s.s. 100 100 79 Melitta arrogans 100 100 Melitta leporina (A) 79 100 Melitta leporina (B) Fideliopsis major 100 51 Anthidium oblongatum Bees 100 98 66 Chelostoma fuliginosum Megachilidae 96 Lithurgus echinocacti 86 100 Megachile pugnata 90 84 100 Anthophora montana 100 Pachymelus peringueyi 94 98 Centris rhodopus 72 Ctenoplectra albolimbata 92 98 81 Apis mellifera Leiopodus singularis 56 Ceratina calcarata Apidae 58 Holcopasites ruthae LT bees 59 63 Paranomada velutina 73 Triepeolus robustus 100 EVOLUTION 78 Thyreus delumbatus 100 Zacosmia maculata 86 Protoxaea gloriosa 100 Megandrena enceliae 60 60 100 Alocandrena porteri 99 56 Andrena brooksi 99 100 Melitturga clavicornis Andrenidae 100 100 Panurgus calcaratus 100 100 Calliopsis pugionis 100 Calliopsis anthidia 100 Calliopsis fracta 97 Dieunomia nevadensis 87 98 98 Pseudapis unidentata 98 Nomioides facilis 64 88 79 Augochlorella pomoniella 100 91 97 72 Agapostemon tyleri 100 95 Halictus rubicundus 100 Conanthalictus wilmattae Halictidae 85 Penapis penai 98 Xeralictus bicuspidariae 88 65 91 100 Rophites algirus 62 60 90 100 Dufourea mulleri 72 Systropha curvicornis Stenotritus sp. 100 Diphaglossa gayi Stenotritidae
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