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Phylogeny of the Bee Genus Halictus (Hymenoptera: Halictidae) Based on Parsimony and Likelihood Analyses of Nuclear EF-1␣ Sequence Data Bryan N

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Phylogeny of the Bee Genus Halictus (Hymenoptera: Halictidae) Based on Parsimony and Likelihood Analyses of Nuclear EF-1␣ Sequence Data Bryan N Molecular Phylogenetics and Evolution Vol. 13, No. 3, December, pp. 605–618, 1999 Article ID mpev.1999.0670, available online at http://www.idealibrary.com on Phylogeny of the Bee Genus Halictus (Hymenoptera: Halictidae) Based on Parsimony and Likelihood Analyses of Nuclear EF-1␣ Sequence Data Bryan N. Danforth,* Herve´Sauquet,† and Laurence Packer‡ *Department of Entomology, Cornell University, Comstock Hall, Ithaca, New York 14853-0901; †c/o Dr. A. Le Thomas, E.P.H.E., Laboratoire de Biologie et Evolution des Plantes vasculaires, Museum National d’Histoire, Naturelle, 16, rue Buffon, 75005 Paris, France; and ‡Department of Biology and Faculty of Environmental Studies, York University, 4700 Keele Street, Toronto, Ontario, M3J 1P3, Canada Received December 23, 1998; revised April 8, 1999 INTRODUCTION We investigated higher-level phylogenetic relation- ships within the genus Halictus based on parsimony Halictid bees (Halictidae) are model organisms for and maximum likelihood (ML) analysis of elongation studying the evolution of social behavior in insects. Of factor-1␣ DNA sequence data. Our data set includes 41 all the bees, this family includes the greatest number of OTUs representing 35 species of halictine bees from a eusocial species and shows the greatest intra- and diverse sample of outgroup genera and from the three interspecific variability in social behavior (Michener, widely recognized subgenera of Halictus (Halictus s.s., 1974). Within the halictid subfamily Halictinae there Seladonia, and Vestitohalictus). We analyzed 1513 total are seven genera and subgenera that include all or aligned nucleotide sites spanning three exons and two some eusocial species: Halictus (Halictus), Halictus introns. Equal-weights parsimony analysis of the over- (Seladonia), Lasioglossum (Evylaeus), Lasioglossum all data set yielded 144 equally parsimonious trees. (Dialictus), Augochlora, Augochlorella, and Pereirapis; Major conclusions supported in this analysis (and in and in most cases, even closely related species show all subsequent analyses) included the following: (1) widely differing levels of social organization (Michener, Thrincohalictus is the sister group to Halictus s.l., (2) 1990a; Packer, 1993; Wcislo, 1997; and Yanega, 1997 all Halictus s.l. is monophyletic, (3) Vestitohalictus ren- provide reviews of halictid social diversity). However, ders Seladonia paraphyletic but together Seladonia ؉ despite their importance, research on halictid sociality Vestitohalictus is monophyletic, (4) Michener’s Groups has been hindered by our poor understanding of phylo- 1 and 3 are monophyletic, and (5) Michener’s Group 1 genetic relationships at the generic and species levels. renders Group 2 paraphyletic. In order to resolve basal Phylogenetic analyses of social organisms have made relationships within Halictus we applied various important contributions to our understanding of social weighting schemes under parsimony (successive ap- evolution. Within social insects, phylogenetic ap- proximations character weighting and implied proaches have been used to analyze the origins of weights) and employed ML under 17 models of se- eusociality in the vespid wasps (Carpenter, 1989, 1991), quence evolution. Weighted parsimony yielded conflict- carinate Lasioglossum (subgenus Evylaeus) (Packer, ing results but, in general, supported the hypothesis 1991), Halictus (Richards, 1994), Augochlorini (Dan- -that Seladonia ؉ Vestitohalictus is sister to Michener’s forth and Eickwort, 1997), and corbiculate bees (for Group 3 and renders Halictus s.s. paraphyletic. ML merly the Apidae; cf. Roig-Alsina and Michener, 1993) analyses using the GTR model with site-specific rates (Michener, 1990b; Cameron, 1991, 1993; Prentice, 1991; -supported an alternative hypothesis: Seladonia ؉ Ves- Sheppard and McPheron, 1991; Chavarria and Carpen titohalictus is sister to Halictus s.s. We mapped social ter, 1994; Engel and Schultz, 1997). Recent phyloge- behavior onto trees obtained under ML and parsimony netic evidence from bees indicates that evolutionary in order to reconstruct the likely historical pattern of reversals from eusociality to solitary nesting may occur social evolution. Our results are unambiguous: the more frequently than independent origins of eusocial- ancestral state for the genus Halictus is eusociality. ity (Wcislo and Danforth, 1997). Reversal to solitary behavior has occurred at least four The genus Halictus was described by Latreille in times among the species included in our analysis. 1804 and includes over 300 species of small to large, ௠ 1999 Academic Press primarily eusocial bees. We chose to study this genus for several reasons. First, there is no previous phyloge- 605 1055-7903/99 $30.00 Copyright ௠ 1999 by Academic Press All rights of reproduction in any form reserved. 606 DANFORTH, SAUQUET, AND PACKER netic analysis of the higher-level relationships within closely related taxa introns might provide sufficient the genus (Richards (1994) included only two of the variation to resolve species-level relationships whereas three widely recognized subgenera, and Pesenko (1984) exons could provide resolution at deeper levels. Indeed, provided a morphological analysis of only one of the in initial analyses of EF-1␣ sequence variation among three subgenera). Like many genera of halictine bees, halictine genera this appears to be the case. morphological variation within Halictus is limited and Danforth and Ji (1998) showed that EF-1␣ occurs as traits are often continuously distributed. With few two paralogous copies (F1 and F2) in Hymenoptera, as discrete morphological characters for phylogeny recon- in Diptera (Hovemann et al., 1988). In our analysis, we struction, higher-level relationships remain obscure. sequenced most of the F2 copy, which is roughly 1600 Second, Halictus presents some interesting biogeo- bp in length and contains three introns (Danforth and graphic patterns that could be interpreted in light of a Ji, 1998). phylogeny. Halictus is found in all continents of the world except Australia (Moure and Hurd, 1987) but is most diverse and speciose in the Palearctic region MATERIALS AND METHODS (Michener, 1978b). Members of two of the three subgen- era apparently colonized the New World via the Bering Bees for this study were collected by the authors in land bridge during the Pleistocene (Michener, 1979). Europe and North America. Specimens used for sequenc- Finally, within this genus are solitary species (e.g., ing were primarily preserved in 95% EtOH but recently Halictus (Halictus) quadricinctus (Sakagami, 1974; collected pinned specimens and frozen specimens were Knerer, 1980)), socially polymorphic species (e.g., Halic- also used. Pinned specimens older than 3–5 years were tus (H.) rubicundus (Bonelli, 1967; Knerer, 1980; not suitable for DNA extractions but those collected Yanega, 1988, 1989, 1990, 1992, 1993)), and eusocial more recently provided good quality, high-molecular- species (e.g., Halictus (H.) farinosus (Eickwort, 1985)). weight DNA for PCR. Outgroup and ingroup taxa By mapping social behavior onto a well-resolved phylog- included in this study, locality data, specimen voucher eny for Halictus, we can infer the most likely scenario numbers, and GenBank accession numbers are listed for social evolution. in Table 1. Voucher specimens are housed in the Cornell For this study we chose a nuclear protein-coding University Insect Collection. gene, elongation factor-1␣ (EF-1␣). This gene encodes DNA extractions followed standard protocols de- an enzyme involved in the GTP-dependent binding of tailed in Danforth (1999). Two sets of PCR products charged tRNAs to the acceptor site of the ribosome were used to generate the data set (Table 2). Initially, during translation (Maroni, 1993). Recent work by primers were designed based on a comparison of pub- Jerome Regier and colleagues (Friedlander et al., 1992, lished Drosophila (Hovemann et al., 1988), Apis (Wall- 1994, 1997) has shown that EF-1␣ (as well as other dorf and Hovemann, 1990), and moth (Cho et al., 1995) nuclear protein-coding genes) can provide an extremely sequences. Primers that initially amplified at least good source of data for higher-level studies of insect some halictid species included For1-deg, For3, and phylogenetics. The advantages of nuclear protein- Cho10 (Table 2). Based on initial comparisons of the F1 coding genes include their slow rate of substitution, and F2 copies of EF-1␣ in halictid bees, we developed a unbiased nucleotide composition, and ease of sequence new, F2-specific, reverse primer (F2-Rev1). For the alignment (especially when introns are excluded). Pre- downstream (3Ј) end of EF-1␣ we used primers For3/ vious cladistic analyses of EF-1␣ sequence data have Cho10 (Table 2). These primers amplify both EF-1␣ found that this gene provides useful phylogenetic infor- copies; however, the presence of a roughly 200- to mation across a wide range of divergence times. Regier 250-bp intron in the F2 copy allows these PCR products and Shultz (1997) used EF-1␣ amino acid data to to be separated on low-melting-point agarose gels. Only reconstruct arthropod relationships, and McHugh (1997) the F2 copy was included in the present analysis. and Kojima (1998) found that EF-1␣ provided evidence PCR amplifications were carried out following stan- of polychaete paraphyly. Within insects, EF-1␣ has dard protocols (Palumbi, 1996), with the following cycle been shown to recover higher-level relationships in the conditions: 94°C, 1 min denaturation; 50–56°C, 1 min moth
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