Author Queries Journal: Proceedings of the Royal Society B Manuscript: Rspb20110365
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Author Queries Journal: Proceedings of the Royal Society B Manuscript: rspb20110365 SQ1 Please supply a title and a short description for your electronic supplementary material of no more than 250 characters each (including spaces) to appear alongside the material online. Q1 Please clarify whether we have used the units Myr and Ma appropriately. Q2 Please supply complete publication details for Ref. [23]. Q3 Please supply publisher details for Ref. [26]. Q4 Please supply title and publication details for Ref. [42]. Q5 Please provide publisher name for Ref. [47]. SQ2 Your paper has exceeded the free page extent and will attract page charges. ARTICLE IN PRESS Proc. R. Soc. B (2011) 00, 1–8 1 doi:10.1098/rspb.2011.0365 65 2 Published online 00 Month 0000 66 3 67 4 68 5 Why do leafcutter bees cut leaves? New 69 6 70 7 insights into the early evolution of bees 71 8 1 1 2,3 72 9 Jessica R. Litman , Bryan N. Danforth , Connal D. Eardley 73 10 and Christophe J. Praz1,4,* 74 11 75 1 12 Department of Entomology, Cornell University, Ithaca, NY 14853, USA 76 2 13 Agricultural Research Council, Private Bag X134, Queenswood 0121, South Africa 77 3 14 School of Biological and Conservation Sciences, University of KwaZulu-Natal, Private Bag X01, 78 15 Scottsville, Pietermaritzburg 3209, South Africa 79 4 16 Laboratory of Evolutionary Entomology, Institute of Biology, University of Neuchatel, Emile-Argand 11, 80 17 2000 Neuchatel, Switzerland 81 18 Stark contrasts in clade species diversity are reported across the tree of life and are especially conspicuous 82 19 when observed in closely related lineages. The explanation for such disparity has often been attributed to 83 20 the evolution of key innovations that facilitate colonization of new ecological niches. The factors under- 84 21 lying diversification in bees remain poorly explored. Bees are thought to have originated from apoid wasps 85 22 during the Mid-Cretaceous, a period that coincides with the appearance of angiosperm eudicot pollen 86 23 grains in the fossil record. The reliance of bees on angiosperm pollen and their fundamental role as 87 24 angiosperm pollinators have contributed to the idea that both groups may have undergone simultaneous 88 25 radiations. We demonstrate that one key innovation—the inclusion of foreign material in nest construc- 89 26 tion—underlies both a massive range expansion and a significant increase in the rate of diversification 90 27 within the second largest bee family, Megachilidae. Basal clades within the family are restricted to deserts 91 28 and exhibit plesiomorphic features rarely observed among modern bees but prevalent among apoid wasps. 92 29 Our results suggest that early bees inherited a suite of behavioural traits that acted as powerful evolution- 93 30 ary constraints. While the transition to pollen as a larval food source opened an enormous ecological 94 31 niche for the early bees, the exploitation of this niche and the subsequent diversification of bees only 95 32 became possible after bees had evolved adaptations to overcome these constraints. 96 33 97 34 Keywords: bees; key innovation; diversification; Megachilidae; nesting biology; bee–flower relationships 98 35 99 36 100 37 1. INTRODUCTION or stems [6,7]. The absence of nest-lining in this group 101 38 Bees provide a mixture of pollen and nectar as food for was originally attributed to a behavioural loss associated 102 39 their developing larvae. To protect these provisions from with above-ground nesting [8], but the phylogenetic 103 40 microbial infection or liquefaction that may result from position of Lithurgini at the base of Megachilinae [9] 104 41 exposure to moisture, most bees coat the inside of their suggests that it represents an ancestral trait [10]. Bees 105 42 brood cells with a hydrophobic lining secreted by Dufour’s of the subfamily Fideliinae build unlined nests that they 106 43 gland [1,2]. By contrast, megachilid bees use an eclectic excavate in sandy soil [11–14]. Two distinct tribes of fide- 107 44 array of foreign material to line their cells. The French nat- liine bees are recognized, Fideliini and Pararhophitini, 108 45 uralist, Jean-Henri Fabre, commented extensively on the which are both entirely restricted to deserts; the absence 109 46 nesting habits of megachilids and posed the following ques- of cell lining in these bees may be related to the arid con- 110 47 tion: ‘...the Osmiae make their partitions with mud or with ditions of their habitats, which may make nest-lining 111 48 a paste of chewed leaves; the Mason-bees build with unnecessary [15]. It remains unclear, however, whether 112 49 cement; ...the Megachiles made disks cut from leaves cell-lining behaviour, using either secretions or foreign 113 50 into urns; the Anthidia felt cotton into purses; the Resin- material, has been secondarily lost in these lineages or 114 51 bees cement together little bits of gravel with gum;...Why whether the absence of cell lining represents an ancestral 115 52 all these different trades...?’ [3]. state. To answer these questions, we present a robust mol- 116 53 It has been demonstrated that the foreign material ecular phylogeny of Megachilidae and trace the evolution 117 54 used by megachilid bees is hydrophobic and shows anti- of nesting biology within the family. We demonstrate that 118 55 microbial activity [4,5], thus serving a similar function the use of foreign material in nest construction was a key 119 56 to the secreted cell lining in other bee groups. Not all innovation that triggered both range expansion and diver- 120 57 megachilids, however, use foreign material in nest con- sification in megachilid bees and also propose that the 121 58 struction. Bees of the tribe Lithurgini do not line their ancestral biology of this family, which is still reflected in 122 59 nest cells at all; instead, they excavate burrows in wood several extant megachilid lineages, mirrors the ancestral 123 60 behaviour of bees in general. Similarities in the biology 124 61 of the early megachilid lineages pertaining to nesting 125 62 * Author for correspondence ([email protected]). and foraging behaviour are numerous, conspicuous 126 63 Electronic supplementary material is available at http://dx.doi.org/10. and challenge our understanding of the evolution and 127 64 SQ1 1098/rspb.2011.0365 or via http://rspb.royalsocietypublishing.org. diversification of bees. 128 Received 16 February 2011 Accepted 25 March 2011 1 This journal is q 2011 The Royal Society rspb20110365—1/4/11—18:12–Copy Edited by: L. Shobana ARTICLE IN PRESS 2 J. R. Litman et al. Evolutionary history of Megachilidae 129 2. MATERIAL AND METHODS GTR I G model; substitution models were unlinked 193 þ þ 130 (a) Taxon sample across partitions. We used an uncorrelated lognormal 194 131 We selected 98 ingroup taxa representing all seven tribes of relaxed-clock model with a Yule tree prior. Trees were 195 132 the family Megachilidae. Our ingroup includes 12 Fideliini, sampled every 2000 generations. We randomly chose a start- 196 133 two Pararhophitini, eight Lithurgini, three Dioxyini, 23 ing tree from the posterior distribution of trees from the 197 134 Anthidiini, 17 Osmiini and 33 Megachilini. We chose 31 out- MRBAYES analysis; we used TREEEDIT v. 1.0 [26] to scale 198 135 group taxa to represent the diversity of the rest of the bees the root height to 130 Myr in order to conform to the con- 199 136 including one Colletidae, one Halictidae, one Andrenidae, straints imposed by prior distributions on divergence times. Q1 200 137 five Melittidae and 23 Apidae. Electronic supplementary Ten independent analyses were run for a total of 300 000 201 138 material, table S1 lists the DNA voucher numbers and collec- 000 generations. An appropriate burn-in was discarded 202 139 tion localities for each of the specimens used in this study. We from each analysis using TRACER [23], leaving 217 068 000 203 140 sampled more densely in the families Melittidae and Apidae total post-burnin generations. In order to ensure indepen- 204 141 to accommodate the placement of fossil calibration points. dent sampling of trees, we sampled every third tree from 205 142 Voucher specimens are deposited in the Cornell University the post-burn-in posterior distribution of trees using LOG- 206 143 Insect Collection. COMBINER v. 1.6.1 [24] and then used TREEANNOTATOR 207 144 v. 1.6.1 [24] to build a maximum clade credibility tree 208 Datasets and alignment 145 (b) from this posterior distribution of trees (electronic sup- 209 146 We sequenced fragments from four protein-coding genes: plementary material, figure S3). 210 147 CAD (882 bp), NAK (1489 bp), EF1-alpha (1111 bp) and 211 LW rhodopsin (673 bp) and one ribosomal gene (28S; 148 (e) Calibration of internal nodes and root node in 212 1306 bp), following the DNA extraction and sequencing pro- 149 BEAST 213 tocols outlined by Danforth et al.[16]. All taxa and GenBank 150 We used fossils to time-calibrate seven internal nodes on our 214 accession numbers are listed in electronic supplementary 151 tree. Five of these calibration points were assigned a lognor- 215 material, table S2. PCR primers and conditions are listed 152 mal prior distribution, while two were assigned a normal 216 in electronic supplementary material, table S3. The four 153 prior distribution. We present the details of these calibration 217 protein-coding genes were aligned using MAFFT [17] and 154 points, as well as a discussion of fossils that were unusable for 218 then adjusted by eye in MacClade [18]; all introns were 155 the purposes of calibrating our phylogeny, as the electronic 219 removed.