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Genetic Differentiation Among Geographic Groups of Three Honeybee

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Genetic Differentiation Among Geographic Groups of Three Honeybee Article Genetic differentiation among geographic groups of three honeybee species, Apis cerana, A. koschevnikovi and A. dorsata, in Borneo Hiroyuki Tanaka1*, Takeshi Suka2, David W. Roubik3 and Maryati Mohamed4 1 Center for Ecological Research, Kyoto University, Kamitanokami, Otsu, Shiga 520-2113, Japan 2 Nagano Nature Conservation Research Institute, 2054-120 Kitago, Nagano 381-0075, Japan 3 Smithsonian Tropical Research Institute, APDO 2072, Balboa, Panama 4 Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah, Locked Bag 2073, 88999 Kota Kinabalu, Sabah, Malaysia Abstract We sequenced the mitochondrial cytochrome oxidase 1 (COl) gene of three honeybee species of Borneo, Apis cerana, A. koschevnikovi and A. dorsata, and carried out phylogenetic analyses considering geographic genetic variation. We also compared the sequence divergence-geographic distance relationships among the three species. Estimated genetic differentiation was an order of magnitude larger in A. koschevnikovi than in A. cerana and A. dorsata. Migratory nesting behavior and cold tolerance of each honeybee, and the paleoclimate of the Southeast Asian tropics, are discussed as factors that produced these characteristics for mitochondrial genetic markers, and conservation priorities are recommended. Key words: Apis, Borneo, cytochrome oxidase 1, genetic differentiation, migratory nesting behavior, paleoclimate Introduction to understanding evolution of plant-pollinator interaction but also present essential knowledge to Of the nine species and/or candidate of species conservation planning of tropical forests (see Lee et recognized at present in honeybees, genus Apis (Engel, al., 2000; Rincon et al., 1999). We suggest that genetic 1999; Otis, 1996), five species inhabit Borneo; the dwarf variation within plant-pollinator assemblages clarifies honeybee (A. andreniformis), the giant honeybee (A. not only phylogenetic concepts associated with dorsata), the Asian honeybee (A. c era no), the Saban biological species, but may also indicate evolutionary honeybee (A. koschevnikovi) and the Bornean montane potential and adaptive diversity in mutualisms honeybee (A. nuluensis). The dwarf honeybees and the (Thompson, 1994). giant honeybees make a single-comb nest in the open Smith (1991) demonstrated that mitochondrial DNA (Ruttner, 1988), whereas the others are cavity-nesting (mtDNA) was a powerful tool to estimate genetic honeybees which construct multiple parallel combs in differentiation and geographic variations within species hollows (Ruttner, 1988; Tingek et al., 1988, 1996). of Apis. For A. mellifera, the western cavity-nesting Recent studies reveal that eusocial bees such as honeybee, intensive studies have been carried out to honeybees and stingless bees (Apini and Meliponini, clarify the phylogeny of subspecies or geographic races Apidae) are important as pollinators for many tropical by employing the C01-C02 region (the intergenic non- plant species (e.g., Momose et al., 1998). Hence, coding region between cytochrome oxidases 1 and 2) detailed geographic studies on phylogenetic (Cornuet and Garnery, 1991; Franck et al., 1998; relationships and genetic divergence among honeybees Garnery et al., 1992) and NADH dehydrogenase 2 in the Southeast Asian tropics will not only contribute (Arias and Sheppard, 1996) of mtDNA. Geographic * Present address: Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan relationships of A. cerana in its range (Deowanish et localities shown in Fig. 1. In Crocker Range Park, al., 1996; Smith and Hagen, 1996; Smith et al., 2000) Sabah, Malaysia, A. cerana and A. koschevnikovi were and population structure of this species in Thailand collected at Mahua camp and A. dorsata was caught at (Sihanuntavong et al., 1999) and in the Philippines (De Ulu Senagang in a field survey as a part of the La Rua et al., 2000) were also investigated by using the CROCKER XPDC '99 organized by The Sabah Parks, C01-C02 region. However, such a genetic study has Universiti Malaysia Sabah and Universiti Malaysia been rarely conducted for other Apis since Smith's Sarawak. Both Mahua and Ulu Senagang are located (1991) work, and never for more than one co-occurring on the eastern side of the mountain range. The species. Tanaka et al. (2001) suggested that specimens of A. dorsata were also collected in Bandar mitochondrial cytochrome oxidase 1 (COl) is useful Sri Aman, Sarawak, Malaysia. After the collection, bee for intra-specific genetic studies in Apis in the previous samples were fixed with 99.5 % ethanol until DNA work that examined the phylogenetic position of A. extraction. Samples examined in a previous study nuluensis of northern Borneo in genus Apis. (Tanaka et al., 2001) were also included in phylogenetic In the present study, we sequence the COl gene of analyses (see below). Those specimens comprise A. three honeybee species living in Borneo (A. cerana, A. cerana from Kinabalu Park (Sabah), Brunei, Taiwan, koschevnikovi and A. dorsata) and carry out Thailand, Russia, Japan, South Korea, A. nuluensis from phylogenetic analyses in order to examine genetic Mt. Kinabalu, A. koschevnikovi from Brunei, Lambir relationships among geographic groups of each species. (Sarawak), A. mellifera from Uzbekistan, and A. dorsata Then we compare the sequence divergence-geographic from Lambir (Table 1). distance relationships in Borneo among the three Extraction of total DNA was done according to the species. Finally, we discuss possible roles of different method of Hillis et al. (1996). A partial sequence of factors producing geographical genetic divergences the CO 1 was amplified by polymerase chain reaction among those species. (PCR). The primers used in amplification and the condition of PCR were described elsewhere (Tanaka et Materials and Methods al., 2001). Amplified fragments were purified by a QIAquick PCR purification kit (QIAGEN) and then Collection of bees and experimental procedures used in sequencing reaction with a Dye terminator cycle Bee samples of Borneo were collected from sequencing kit (Applied Biosystems). The DNA Fig. 1. Map showing the sampling sites of Apis specimens in Borneo. Table 1. List of Apis samples used in phylogenetic analyses in the present study sequencing was carried out with an auto-sequencer Results (Applied Biosystems 373 DNA sequencer). Voucher specimens are at the Center for Ecological Research, Phylogenetic analyses Kyoto University. Sequence data obtained here have been entered in Gen Bank (Table 1). The common CO 1 haplotypes were Phylogenetic analyses shared between A. cerana of Kinabalu 1 (sample No. 1 The honeybee sequences listed in Table 1 were collected at Kinabalu Park) and of Brunei and also aligned with an outgroup sequence of a stingless bee between A. cerana of Japan and of South Korea, (Trigona amalthea; Genbank accession No. AF214669, respectively. Therefore, a total of 20 different honeybee Tanaka et al., 2001) using CLUSTAL W (Thompson et sequences were analyzed. Of the 1041 nucleotide al., 1994). The 1041 base-pair sequences were analyzed positions, 277 characters were variable, which included by maximum parsimony (MP) and neighbor-joining 180 parsimony-informative characters. Figures 2 and (NJ) methods using PAUP*4.0 beta version (Swofford, 3 present phylogenetic relationships among Apis species 1999). In the MP analysis, a character-weighting and geographic groups of A. cerana, A. koschevnikovi method was performed with transversions weighted 5 and A. dorsata obtained by the weighted MP and NJ times as much as transitions, according to our previous analyses, respectively. The topologies of both study (Tanaka et al., 2001). The heuristic search option phylogenetic trees were nearly congruent with each with the simple sequence addition and TBR branch- other. The species relationships depicted in these trees swapping algorithm were selected. For the NJ analysis, coincided with the Apis phylogeny proposed by Engel evolutionary distance was measured by a general time- (1998) and Engel and Schultz (1997), also with that reversible model (Yang, 1994). To evaluate the reconstructed using morphological data (Alexander, confidence of internal branches, a bootstrap test was 1991 a, 1991b), except for including A. nuluensis (sister implemented with 1,000 replicates in both analyses. to A. cerana) and excluding dwarf honeybees (basal to To estimate the degree of genetic differentiation A. dorsata). among geographic groups of A. cerana, A. In the phylogenetic trees, A. cerana from Crocker koschevnikovi and A. dorsata, sequence di vergence was Range was placed in a cluster of Bornean group. Apis calculated using the Tamura and Nei (1993) distance, koschevnikovi from Crocker Range was connected to based on pairwise comparisons of COl haplotypes. the cluster consisting of Lambir and Brunei but diverged from each, as indicated by the deep branching pattern in the NJ tree (Fig. 3). For A. dorsata, two slightly Fig. 2. Phylogenetic relationships of Apis species and the Fig. 3. The neighbor-joining tree showing phylogenetic geographic groups of A. cerana, A. koschevnikovi and A. dorsata relationships of Apis species and the geographic groups of A. studied. The tree is strict consensus of 3 equally parsimonious cerana, A. koschevnikovi and A. dorsata studied. The trees obtained by weighted maximum parsimony analysis with evolutionary distance was measured by a general time-reversible transversions weighted five times as much as transitions. model (Yang, 1994). Numbers above the
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