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The History of Early Bee Diversification Based on Five !"#$%&'()*+$),$-.*/+$0##$1&2#*'&,&3.(&)4$0.'#5$)4$6&2#$7#4#'$8/9'$:)*;")/)<+ =9(")*>'?@$0*+.4$AB$1.4,)*("C$D#5)4&.$D&;#'C$E#44&,#*$6.4<C$D#F4$7B$0*.5+ D)9*3#@$8*)3##5&4<'$),$("#$A.(&)4./$=3.5#G+$),$D3&#43#'$),$("#$H4&(#5$D(.(#'$),$=G#*&3.C I)/B$JKLC$A)B$MJ$>N3(B$JKC$OKKP?C$;;B$JQJJRSJQJOL 89T/&'"#5$T+@$National Academy of Sciences D(.T/#$HUV@$http://www.jstor.org/stable/30051512 =33#''#5@$JMWKXWOKJK$JM@QJ Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/action/showPublisher?publisherCode=nas. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. National Academy of Sciences is collaborating with JSTOR to digitize, preserve and extend access to Proceedings of the National Academy of Sciences of the United States of America. http://www.jstor.org The history of early bee diversificationbased on five genes plus morphology Bryan N. Danfortht, Sedonia Sipes*, Jennifer FangS, and Sean 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 radiationof tongued (LT) bee families Megachilidaeand Apidae and the pollinating insects, originated in early to mid-Cretaceous,roughly short-tongued(ST) bee familiesColletidae, Stenotritidae, Andreni- in synchrony with the angiosperms (flowering plants). Under- dae, Halictidae,and Melittidaesensu lato (s.l.)II(9). Colletidaeis standing the diversification of the bees and the coevolutionary widelyconsidered the mostbasal family of bees (i.e.,the sister group history of bees and angiosperms requires a well supported phy- to the restof the bees),because all femalesand most males possess logeny of bees (as well as angiosperms). We reconstructeda robust a glossa(tongue) with a bifid(forked) apex, much like the glossaof phylogeny of bees at the family and subfamily levels using a data an apoidwasp (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 hypothesizedthat the earliestbranches of bee gation factor-la, RNApolymerase II,and LWrhodopsin), as well as phylogenymay have been either Melittidaes.l., LT bees, or a ribosomal (285 and 185) nuclear gene data. Analyses of both the monophyleticgroup consisting of both. The most recentmorpho- DNA data set and the DNA+morphology data set by parsimony logicalanalysis of family-levelphylogeny in bees (17) obtainedtwo and Bayesian methods yielded a single well supported family-level differenttree topologiesbased on alternativecoding of relatively tree topology that places Melittidae as a paraphyleticgroup at the few mouthpartcharacters. One tree topologyplaces Colletidae as base of the phylogeny of bees. This topology ("Melittidae-LT sisterto the restof the bees ("Colletidaebasal"), whereas the other basal") is significantly better than a previously proposed alterna- places Melittidaes.l.+LT bees as sister to the rest of the bees tive topology ("Colletidae basal") based both on likelihood and ("Melittidae-LTbasal"). The majordifference between the Col- Bayesian methods. Our results have important implications for letidaebasal and Melittidae-LT basal topologies involves the place- understanding the early diversification, historical biogeography, ment of the root node of bees (27). Placingthe root between host-plant evolution, and fossil record of bees. The earliest Colletidaeand the rest of the bees yields the Colletidaebasal branches of bee phylogeny include lineages that are predomi- topology,whereas placementof the root node near or within nantly host-plant specialists, suggesting that host-plant specificity Melittidaes.l. yieldsthe Melittidae-LTbasal topology. The biolog- is an ancestral trait in bees. Our results suggest an African origin icalimplications of these alternativetopologies are radicallydiffer- for bees, because the earliest branches of the tree include pre- ent. The Colletidaebasal topologyimplies an Australianand/or dominantly African lineages. These results also help explain the SouthAmerican origin for bees andsuggests the earliestbees were predominance of Melittidae, Apidae, and Megachilidae among the a mix of floral generalistsand specialists.Melittidae-LT basal earliest fossil bees. impliesan African origin for bees andindicates that the earliestbees were likelyto havebeen floralspecialists. These alternativetopol- bee phylogeny I bee evolutionI molecularevolution I ogiesalso have implications for understandingthe fossilrecord and molecularsystematics I coevolution antiquityof bees. To resolvethe root node of bees, we combined>4,000 bp of (floweringplants), with an estimated250,000- DNA sequencedata with the previousmorphological data set of Angiosperms260,000 species (1), representthe largestand most diverse Alexanderand Michener(17). We reporthere the resultsof an lineage of vascular plants on earth. To Darwin, the rapid analysisof the largestmolecular and morphological study to dateon emergence and early diversificationof the angiospermswas an "abominablemystery" (ref. 2 andrefs. therein).Among the most traits attributableto Author contributions: B.N.D. and 5.5. designed research; B.N.D., 5.5., J.F., and S..B. important the explosive radiationof the performed research; S.G.B. contributed new reagents/analytical tools; B.N.D. analyzed angiospermsis animal-mediatedpollination (3-7). Insectsare by data; and B.N.D. wrote the paper. far the most importantanimal pollinators ("70% of angiosperm The authors declare no conflict of interest. species are insect pollinated;ref. 8) and amonginsects, bees are Freely available online through the PNAS open access option. the most specializedand All of the importantpollinator group. Abbreviations: ST, short-tongued; LT, long-tongued; GTR, general time-reversible; I+G, >16,000 speciesof bees livingtoday (9) relyvirtually exclusively gamma distribution plus a proportion of invariant sites; s.l., sensu lato; s.s., sensu stricto. on angiospermproducts, including pollen and nectar for adult Data deposition: The sequences reported in this paper have been deposited in the GenBank and larvalnutrition (10), floral oils for larvalnutrition (11, 12), database (accession nos. listed in Table 4, which is published as supporting information on floral waxes and perfumesthat 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 51599). adaptedto collecting,manipulating, carrying, and storingpollen tTo 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 11420, Mailcode 6509, Southern specialistson one or a few closely related host plants (10). Illinois University, Carbondale, IL62901-6509. One toward Darwin's"abominable is SPresent address: Department of Physiology, P.O. Box 245051, University of Arizona, step resolving mystery" to AZ 85724-5051. developa betterunderstanding of the role thatbees playedin the Tucson, and diversificationof the A qPresent address: Department of Entomology and Laboratories of Analytical Biology, evolutionaryhistory angiosperms. Smithsonian Institution, Suitland, MD 20746. robustphylogeny of bees wouldallow us to infer attributesof the IlMelittidae in the sense of Michener (9) is a paraphyletic group based on our results. We earlybees and to reconstructthe typesof interactionsthat existed refer to the three melittid subfamilies as families, following an earlier suggestion by betweenthe earliestbees andtheir angiosperm hosts. Higher-level Alexander and Michener (17). The three families are Melittidae (s.s.), Dasypodaidae, and (family-and subfamily-level)bee phylogenyis poorlyunderstood. Meganomiidae. Currently,bees are dividedinto seven extantfamilies: the long- C 2006 by The National Academy of Sciences of the USA 15118-15123 I PNAS I October 10,2006 I vol.103 I no. 41 www.pnas.org/cgi/doi/10.1073/pnas.0604033103 Cerceris sp. 77 Stigmus sp. 69 95 Clypeadon sp. 86 I Philanthus gibbosus 80 Ochleroptera bipunctata 100 Bicyrtes ventralis 100 0 Bembix americana 979-83 100 Sceliphron caementarium eo mexicana 997 100 199Isodontia10Podalonia sp. 51 79 61 Anacrabro ocellatus 8 99 Plenoculus sp. 51 99 Tachysphex sp. 100 96 100 Hesperapis richtersveldensis 100 Hesperapislarreae
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