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Genetic Characterization of Italian Honeybees, Apis Mellifera Ligustica, Based on Microsatellite DNA Polymorphisms*

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Genetic Characterization of Italian Honeybees, Apis Mellifera Ligustica, Based on Microsatellite DNA Polymorphisms* Apidologie 38 (2007) 207–217 207 c INRA/DIB-AGIB/ EDP Sciences, 2007 DOI: 10.1051/apido:2006073 Original article Genetic characterization of Italian honeybees, Apis mellifera ligustica, based on microsatellite DNA polymorphisms* Raffaele D’Oa,AlbertoMa, Marco La, Robin F.A Mb a Istituto Nazionale di Apicoltura, via di Saliceto, 80 40128 Bologna, Italia b Institut für Zoologie, Martin-Luther-Universität Halle-Wittenberg, Hoher Weg 4, 06099 Halle/Saale, Germany Received 7 June 2006 – Accepted 15 September 2006 Abstract – The genetic variability of Apis mellifera ligustica was screened throughout the Italian peninsula and Sardinia with eight polymorphic microsatellite loci. Samples of Apis mellifera mellifera, Apis mellifera carnica and from the Buckfast breeding line were genotyped for comparison. Low Fis and Fst values suggest the absence of genetic structure within and among A. m. ligustica populations, although the high number of alleles detected and heterozygosity. Phylogenetic and individual analyses confirmed that A. m. ligustica has come to resemble one large population, probably as a result of intensive beekeeping practices such as migratory beekeeping and large-scale commercial queen trading. Since the introgression of foreign alleles into both endemic natural and commercial A. m. ligustica populations, can be detected and monitored by microsatellite analysis, the results provide a reference data set for future local biodiversity conservation and other controlled breeding programs. Apis mellifera ligustica / microsatellite / genetic variability / conservation 1. INTRODUCTION markers (Estoup et al., 1995). The mitochon- drial C branch is composed of subspecies from The honeybee Apis mellifera L. has been both the “C” and “O” morphological lineages, ff intensively studied to assess both its phylo- suggesting that the di erentiation of these lin- genetic origin and taxonomy. Ruttner (1988) eages postdated the origin of the C mitochon- conducted the most extensive morphologi- drial branch. cal characterization, classifying 24 Apis mel- The Italian peninsula plays a pivotal role lifera subspecies into four major evolution- for honeybee biogeography in this scenario, as ary biogeographic branches. Ruttner’s now it did for many other taxa during the Pleis- classic hypothesis is supported by a set of tocene glacial period (Hewitt, 1996; Taberlet morphometric studies (Cornuet and Fresnaye, et al., 1998; Hewitt, 1999). A. m. ligustica 1989; Cornuet et al., 1988; Lebdigrissa et al., genetic variability has been studied in detail 1991). Three main evolutionary branches, ‘A’ using allozymes (Badino et al., 1982, 1983; (African subspecies), ‘C’ (northern Mediter- Manino and Marletto, 1984; Marletto et al., ranean subspecies, including the Italian hon- 1984) and other molecular markers (Franck, eybee, Apis mellifera ligustica Spinola) and 2004), which have shown hybridization with ‘M’ (western European subspecies) have been A. m. mellifera along the western Alpine arc defined using mitochondrial DNA (Garnery and the Ligurian coast. Moreover, the east- et al., 1992; Franck et al., 1998) and nuclear ern Alpine arc and particularly the Friuli re- gion were already known as a natural hy- Corresponding author: R. Dall’Olio, bridization zone with a subspecies from the [email protected] ‘C’ lineage, Apis mellifera carnica (Comparini * Manuscript editor: Walter S. Sheppard and Biasiolo, 1991; Nazzi, 1992; Meixner Article published by EDP Sciences and available at http://www.edpsciences.org/apido or http://dx.doi.org/10.1051/apido:2006073 208 R. Dall’Olio et al. et al., 1993). Recently, extensive studies have Table I. Locus-specific PCR conditions; tempera- also provided mitochondrial and microsatel- ture ramping speed between cycle steps was 5 ˚C/s. lite evidence of past contacts between hon- eybees from different evolutionary branches, Locus [MgCl2] Cycles Tm (˚C) thus confirming past hybridization within Ital- A113 1.0 mM 30 60 ian honeybees (Franck et al., 2000; Marino A7 1.2 mM 25 58 A88 1.2 mM 30 55 et al., 2002). A(B)24 1.2 mM 30 55 Italian beekeeping developed from an A107 1.2 mM 30 58 ancient rural tradition. Today the queen Ap43 1.2 mM 35 60 bee breeding system is based on selection A28 1.7 mM 30 54 within autochthonous populations. The en- A14 1.7 mM 30 58 demic subspecies has provided many advan- tages for beekeeping practice due to its large honey storing ability, docility and low swarm- of population bottlenecks caused by disease ing propensity. Because of these traits and (Lodesani et al., 1995) on the population struc- the subspecies’ adaptability to a wide range tures of A. m. ligustica. of climatic conditions, A. m. ligustica queens have been massively exported worldwide for more than 150 years (Bar-Cohen et al., 1978; 2. MATERIALS AND METHODS Sheppard, 1989; Woodward, 1993). In spite of this success, the importation of non-ligustica 2.1. Sampling queens into Italy has also increased, partic- ularly during the last ten years (source: Ital- Samples were collected from beekeepers (mainly hobbyist beekeepers who exclusively used ian Health Ministry, B.I.P. – Border Inspec- putative A. m. ligustica queens) or were kindly tion Post – data collection system). Besides provided by researchers. A single worker per reflecting the curiosity of beekeepers to work colony was trapped and immediately killed by with new stocks, this increase is likely to be immersion in absolute ethanol and then stored due to the lower production costs to be found at –20 ˚C until laboratory processing. A total elsewhere and the possibility of having queens of 379 colonies were sampled in different lo- right at the beginning of spring, if imported cations over a four-year period (2001–2004). from the southern hemisphere. It is currently A. m. ligustica samples were initially assigned unclear whether or how these imports affect lo- to seven distinct geographical groups (Fig. 1; cally existing populations in Italy. Given the exact sampling locations are available on the success and scale of the queen breeding in- web, www.inapicoltura.org/online/apidologie2006/ dustry, the conservation of Italian honeybees sample.htm). Three more groups were constituted is of major concern even for economic reasons with samples from A. m. mellifera, A. m. carnica alone. However, its conservation is also impor- and the Buckfast breeding line respectively. Taxa tant from a biodiversity perspective, where a cited in the text in normal case letters (e.g. Carnica) priority is laid on preserving the endemic races specifically refer to a geographical group. of honeybees in Europe. Here we present a nationwide data base 2.2. Molecular analyses which provides insight into the current genetic variability within A. m. ligustica. This data Total DNA was extracted from individual work- base will be an important tool for detecting in- ers’ anterior leg after rinsing twice with bi-distilled trogression of genes from other subspecies and water. DNA isolation was performed in a 96- ff for determining the e ects of a breeding pol- well microtitre plate, following the Chelex method icy based on controlled and co-ordinated rear- (Walsh et al., 1991) with slight modifications. ing programs with the intense rearing of thou- Eight polymorphic microsatellite loci were anal- sand of queens produced by selected mothers. ysed: A113, A28, A(B)24, A14, A107, A88, Ap43 We will also address the effects of professional and A7 (Solignac et al., 2003). The PCR reac- honeybee breeding and the potential impacts tion mixture contained 1X Taq buffer (Invitrogen), Genetic tools for A. m. ligustica conservation 209 Figure 1. Geographic distribution of the 379 sampled colonies. Italian samples were pooled in seven regions. The non- A. m. ligustica samples were treated as three additional taxonomic groups; name and sample size for each of the 10 groups are indicated. 400 nM of each primer, 1 mM of each dNTP, 0.25 U differentiation between groups was computed using of Taq DNA polymerase, 1 µL of DNA extract and unbiased estimates of Fst values provided by Fs- 2 PCR-water to a final volume 10 µL. MgCl2 con- tat and the (δµ) microsatellite distance (Goldstein centration and annealing temperature are reported et al., 1995). in Table I, while PCR cycle conditions were stan- Neighbor-joining analyses were performed to dard (Garnery et al., 1998); Invitrogen oligo primer establish relationships among groups using the pairs were used and the forward primer was la- “PHYLIP” software package (Felsenstein, 1993 belled with WellRED. PCRs were performed with ver.3.57), with the NJ-algorithm (Saitou and Nei, a T-Gradient 96 thermocycler (Biometra) and PCR 1987) and the two genetic distances of Cavalli- products were separated by capillary electrophore- Sforza and Edwards (1967) and Nei (1978). Boot- sis on a CEQ8000 Genetic Analysis System (Beck- strap values were computed over 2000 replications man Coulter, software ver. 8.0). Allele sizes were (Hedges, 1992) by resampling either loci or individ- scored with the CEQ DNA Size Standard Kit-400 uals within populations. (Beckman Coulter). “Structure” (Pritchard et al., 2000 ver.2.1) soft- ware was used to obtain individual ‘a posteriori’ 2.3. Statistical analyses confirmation of the taxonomic posting for each sample: a first analysis was conducted to infer the Unbiased estimates and standard deviations of most likely number of population (k), representa- gene diversity of microsatellite loci were computed tive of the whole dataset, without the use of any according to the method described by Nei (1978); ‘a priori’ information; a sub-dataset including only genotypic linkage disequilibrium (with Bonferroni A. m. mellifera, A. m. carnica and Emilia-Romagna correction), population parameters and microsatel- (to represent A. m. ligustica) bees was subsequently lite variation within and between groups were anal- investigated to detect the presence of hybrid traits ysed with “Fstat” software (Goudet, 1995). Exact in north-eastern Italian bees and assess the genetic tests for Hardy–Weinberg equilibrium and geno- composition of Buckfast samples.
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