This study establishes phylogenetic relationships among bee families and subfamilies with high levels of support. Our results unambiguously support the Melittidae-LT basal topology (Figs. 1 and 2; see Fig. 3, which is published as supporting information on the PNAS web site). The Colletidae basal topology is more widely accepted because of the perception that the bifid glossa of Colletidae is a plesiomorphic trait shared with apoid wasps. This hypothesis appears in numerous publications but is rarely supported by characters other than the overall appearance of the glossa (18–22). Although a number of morphological studies have questioned the Colletidae basal hypothesis (23–26), the morphological support for the Melittidae-LT basal hypothesis has been largely overlooked in the bee phylogenetic literature. Among the most convincing morphological characters that support the tree presented herein is the morphology of the midcoxa. Michener (32) discovered that in apoid wasps, Melittidae s.l., and LT bees, the midcoxa is exposed, whereas in the remaining ST bee families, the upper portion of the midcoxa is internal and hidden beneath the mesopleuron (a condition described as "hemicryptic"). The hemicryptic condition is a unique and unreversed character congruent with monophyly of Andrenidae, Halictidae, Colletidae, and Stenotritidae (Figs. 1 and 2), thus strongly supporting the Melittidae-LT basal topology.
Implications for Bee Historical Biogeography and Host–Plant Evolution. Melittidae-LT basal topology substantially alters prevailing hypotheses of bee phylogeny, biogeography, evolution, and early diversification. The hypothesis that Melittidaes s.l. represents the earliest branch(es) of bee phylogeny suggests an African rather than an Australian or South American origin for the bees. Melittidae s.l. is absent from Australia and South America, and Africa is the only continent where all major lineages (e.g., families) of Melittidae s.l. occur (20). Meganomiidae are restricted to Africa, and for Dasypodaidae and Melittidae sensu stricto (s.s.), Africa is the continent that hosts the greatest number of genera and species. Based on this distribution, Michener (20) hypothesized an African origin for all families of Melittidae s.l. Given their placement in our phylogenetic trees, this would suggest an African origin for bees in general. Disjunct biogeographic distributions in some "melittid" genera, such as Hesperapis (in the Dasypodaidae; ref. 9), provide further support for the antiquity of this group.
The placement of a paraphyletic Melittidae s.l. at the base of the phylogeny also supports the view that the earliest bees were narrow host–plant specialists. Host–plant specialization is widespread among the melittids as well as among many basal lineages in other families, including Rophitinae (Halictidae), Andreninae and Panurginae (Andrenidae), Colletinae (Colletidae), and Fideliinae (Megachilidae). Most species in Melittidae s.s. and Dasypodaidae are well known to be host–plant specialists. Female Hesperapis oraria, for example, are monolectic and forage for pollen exclusively on Balduina angustifolia (Asteraceae; ref. 33). Female H. trochanterata forage exclusively on plants in the genus Nama (Boraginaceae) and have elongate slender heads with specialized hairs on the mouthparts for extracting pollen from the tubular flowers (34). Other species of Hesperapis specialize on a small number of closely related host–plant species within diverse angiosperm families, including Polemoniaceae, Rosaceae, Zygophyllaceae, Onagraceae, Papaveraceae, Fabaceae, and Malvaceae. Host–plant specialization is widespread within Melittidae s.s., including Melitta, Rediviva, Redivivoides, and Macropis. All species of Macropis are narrow host–plant specialists on oil-producing plants in the genus Lysimachia (Primulaceae; ref. 35), and all species possess modified legs for collecting and manipulating viscous floral oils. Species of Rediviva are involved in an intimate host–plant association with plants in the oil-producing genus Diascia (Scrophulariaceae), in which variation in floral spur length in the host plants is paralleled by variation and extreme exaggeration in foreleg length in bees (36, 37). Given the placement of Melittidae s.l. as a paraphyletic group at the base of the tree, our results indicate that host–plant specialization is the primitive state for bees.
Implications for Understanding the Bee Fossil Record. The Melittidae-LT basal hypothesis may help explain the chronological appearance of bee families in the fossil record. If the Colletidae basal topology were indeed correct, one of the most puzzling aspects of the bee fossil record would be the abundance of Melittidae s.l., Apidae, and Megachilidae in the oldest deposits, such as Eocene (Baltic) amber (22, 38) and Cretaceous amber from New Jersey (39–41). Among the bees in Baltic amber deposits, 15 of 18 described genera are LT bees (Apidae and Megachilidae; ref. 22). Melittid bees are also well represented in the Eocene both from Baltic amber (Eomacropis; ref. 22) and French Eocene amber (Paleomacropis; ref. 38). The oldest fossil bee, Cretotrigona prisca, is an apid bee closely related to extant stingless bees (Meliponini; refs. 39–41). In contrast, ST bee families, such as Halictidae, are much less well represented in the Eocene, and representatives of Andrenidae and Colletidae are completely absent in the fossil record up until the Miocene (42, 43). The high proportion of Melittidae s.l. and LT bees in the Eocene fossil deposits has generally been interpreted as an artifact because of the poor fossil record of bees and possibly a bias toward resin collecting bees, most of which are LT bees (44). However, if one accepts the Melittidae-LT basal hypothesis, Melittidae s.l., Megachilidae, and Apidae represent early branches in the phylogeny of the bees and are therefore relatively old compared with some families of ST bees, such as Halictidae, Colletidae, and Stenotritidae.
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