Genetic structure of the gentle Africanized honey bee population (gAHB) in Puerto Rico

BMC Genetics

Volumn 14, Issue , 2013, Pages

  Galindo Cardona, Alberto ^a   Acevedo Gonzalez, Jenny P ^a   Rivera Marchand, Bert ^b   Giray, Tugrul ^a  

^a UNIVERSITY OF PUERTO RICO   (Puerto Rico)

^b Interamerican University   (Puerto Rico)

Author keywords

Africanized; Apis mellifera; European bees; Honeybee population; Hybridization

Indexed keywords

ARTICLE; DEFENSIVENESS; DNA HYBRIDIZATION; GENE FREQUENCY; GENETIC ASSOCIATION; GENETIC LINKAGE; GENETIC RESISTANCE; GENETIC VARIABILITY; HONEYBEE; INSECT GENETICS; MICROSATELLITE MARKER; NONHUMAN; ORGANISM COLONY; POLYMORPHIC LOCUS; POPULATION GENETIC STRUCTURE; POPULATION GENETICS; PUERTO RICO; QUANTITATIVE TRAIT LOCUS; VARROA;

ANIMALS; BASE SEQUENCE; BEES; DNA; DNA PRIMERS; GENETICS, POPULATION; MICROSATELLITE REPEATS; POLYMERASE CHAIN REACTION; PUERTO RICO;

APIS MELLIFERA; APOIDEA; VARROA;

EID: 84881082447     PISSN: None     EISSN: 14712156     Source Type: Journal    
DOI: 10.1186/1471-2156-14-65     Document Type: Article

References (58)

1. Ruttner F, Tassencourt L, Louveaux J. Biometrical-statistical analysis of the geographic variability of Apis mellifera L. Apidologie 1978, 9:363-381.
2. Ruttner F. Biogeography and taxonomy of honey bees 1988, Berlin: Springer.
3. Whitfield CW, Behura SK, Berlocher SH, Clark AG, Johnston JS, Sheppard WS, Smith DR, Suarez AV, Weaver D, Tsutsui ND. Thrice out of Africa: ancient and recent expansions of the honey bee, Apis mellifera. Science 2006, 314:642-646. 10.1126/science.1132772, 17068261.
4. Morse RA, Burgett DM, Ambrose JP, Conner WE, Fell RD. Early introductions of African bees into Europe and the New World. Bee World 1973, 54:57-60.
5. Sheppard WS, Rinderer TE, Mazzolli JA, Stelzer JA, Shimanuki H. Gene flow between African- and European-derived honey bee populations in Argentina. Nature 1991, 349:782-784.
6. Sheppard WS, Soares AEE, DeJong D, Shimanuki H. Hybrid status of honey bee populations near the historic origin of Africanization in Brazil. Apidologie 1991, 22:643-652.
7. Michener CD. The Brazilian bee problem. Ann Rev Entomol 1975, 20:399-416.
8. Taylor OR. African Bees: potential impact in the United States. Bull Entomol Soc Am 1985, 31:14-24.
9. Rinderer TE. Africanized bees: the Africanization process and potential range in the United States. Bull Entomol Soc Am 1986, 32:222-227.
10. Hall HG, Muralidharan K. Evidence from mitochondrial DNA that African honey bees spread as continuous maternal lineages. Nature 1989, 339:211-213. 10.1038/339211a0, 2566122.
11. Smith DR, Taylor OR, Brown WM. Neotropical Africanized honey bees have African mitochondrial DNA. Nature 1989, 339:213-215. 10.1038/339213a0, 2566123.
12. Hall HG. Parental analysis of introgressive hybridization between African and European honeybees using nuclear DNA RFLPs. Genetics 1990, 125:611-621. 1204087, 1974226.
13. Rinderer TE, Stelzer JA, Oldroyd BP, Buco SM, Rubink WL. Hybridization between European and Africanized Honey bees in the neotropical Yucatan peninsula. Science 1991, 253:309-311. 10.1126/science.253.5017.309, 17794698.
14. Rivera-Marchand B. Africanized Honey Bees in Puerto Rico 2007, Biology Department, Rio Piedras Station: University of Puerto Rico, PhD thesis.
15. Rivera-Marchand B, Giray T, Guzman-Novoa E. The cost of defense in social insects: insights from the honey bee. Entomol Expt Appl 2008, 129:1-10.
16. Rivera-Marchand B, Oskay D, Giray T. Gentle Africanized bees on an oceanic island. Evol Appl 2012,
17. Cox B. Ahb In Puerto-Rico. Am Bee J 1994, 134:668-668.
18. Galindo-Cardona A. Male behavior and hybridization of Africanized and European bees 2010, Biology Department, Rio Piedras Station: University of Puerto Rico, PhD thesis.
19. Quezada-Euan JJG, May-Itza WD. Partial seasonal isolation of African and European-derived Apis mellifera (Hymenoptera: Apidae) drones at congregation areas from subtropical Mexico. Ann Entomol Soc Am 2001, 94:540-544.
20. Perez-Castro EE, May-Itza WD, Quezada-Euan JJG. Thirty years after: a survey on the distribution and expansion of Africanized honey bees (Apis mellifera) in Peru. J Apic Res 2002, 41:69-73.
21. Pinto MA, Rubink WL, Patton JC, Coulson RN, Johnston JS. Africanization in the United States: Replacement of Feral European Honey Bees (Apis mellifera L.) by an African Hybrid Swarm. Genetics 2005, 170:1653-1665. 10.1534/genetics.104.035030, 1449774, 15937139.
22. Kraus FB, Franck P, Vandame R. Asymmetric introgression of African genes in honeybee populations (Apis mellifera L.) in Central Mexico. Heredity 2007, 99:233-240. 10.1038/sj.hdy.6800988, 17473860.
23. Rinderer TE, Rubink BS, Daly WL, Stelzer HV, Riggio JA, Baptista RM. Morphometric identification of Africanized and European honey bees using large reference populations. Apidologie 1993, 24:569-585.
24. Nielsen DI, Ebert PR, Page RE, Hunt GJ, Guzman-Novoa E. Improved polymerase chain reaction-based mitochondrial genotype assay for identification of the Africanized honey bee (Hymenoptera: Apidae). Ann Entomol Soc Am 2000, 93:1-6.
25. Suazo A, Hall HG. Nuclear DNA PCR-RFLPs that distinguish African and European honey bee groups of subspecies. I: Comparison of long PCR and standard PCR to screen for polymorphisms. Biochem Genet 2002, 40:225-239. 10.1023/A:1019830800282, 12296626.
26. Solignac M, Vautrin D, Baudry E, Mougel F, Loiseau A, Cornuet J-M. A microsatellite-based linkage map of the honeybee, Apis mellifera L. Genetics 2004, 167:253-262. 10.1534/genetics.167.1.253, 1470837, 15166152.
27. Gould WA, Alarcon C, Fevold B, Jimenez ME, Martinuzzi S, Potts G, Quiñones M, Solorzano M, Ventosa E. The Puerto Rico Gap Analysis Project. Volume 1: Land cover, vertebrate species distributions, and land stewardship 2008, U.S. Department of Agriculture, Forest Service, International Institute of Tropical Forestry. U.S.A.: Gen, Tech. Rep. IITF-GTR-39. Rio Piedras, PR.
28. Holdridge LR. Life zone ecology 1967, San Jose, Costa Rica Tropical: Science Center.
29. Ewel JJ, Whitmore JL. The ecological life zones of Puerto Rico and the U.S. Virgin Islands 1973, Institute of Tropical Forestry, Rio Piedras, PR: USDA Forest Service Research Paper No. ITF-18.
30. Zayed A, Whitfield CW. A genome-wide signature of positive selection in ancient and recent invasive expansions of the honey bee Apis mellifera. PNAS 2008, 105:3421-3426. 10.1073/pnas.0800107105, 2265178, 18299560.
31. Hohenlohe PA, Bassham S, Etter PD, Stiffler N, Johnson EA, Cresko WA. Population Genomics of Parallel Adaptation in Threespine Stickleback using Sequenced RAD Tags. PLoS Genet 2010, 6(2):e1000862. 10.1371/journal.pgen.1000862, 2829049, 20195501.
32. Daly C, Helmer EH, Quinones M. Mapping the climate of Puerto Rico, Vieques and Culebra. Int J Climatol 2003, 23:1359-1381.
33. Hale ML, Burg TM, Steeves TE. Sampling for microsatellite-based population genetic studies: 25 to 30 individuals per population is enough to accurately estimate allele frequencies. PLoS ONE 2012, 7(9):e45170. 10.1371/journal.pone.0045170, 3440332, 22984627.
34. Bauzá J. Para evitar la introducción a la isla de Vieques de las enfermedades y plagas peligrosas de las abejas (Apis mellifera) 1988, Departamento de Agricultura de Puerto Rico Cuarentena doméstica No.5.
35. Estoup A, Solignac M, Cornuet JM. Precise assessment of the number of patrilines and of genetic relatedness in honeybee colonies. Proc R Soc Lond B Biol Sci 1994, 258:1-7.
36. Estoup A, Garnery L, Solignac M, Cornuet JM. Microsatellite variation in Honey Bee (Apis mellifera L.) populations: hierarchical genetic structure and test of the infinite allele and stepwise mutation models. Genetics 1995, 140:679-695. 1206644, 7498746.
37. Rowe DJ, Rinderer TE, Stelzer JA, Oldroyd BP, Crozier RH. Seven polymorphic microsatellite loci in honeybees (Apis mellifera). Insectes Soc 1997, 44:85-93.
38. Schuelke M. An economic method for the fluorescent labeling of PCR fragments. Nat Biotech 2000, 18:233-234.
39. Raymond M, Rousset F. Population genetics software for exact test and ecumenism. J Hered 1995, 86:248-250.
40. Goudet J. FSTAT, a program to estimate and test gene diversities and fixation indices 2001, version 2.9.3) [http://www2.unil.ch/popgen/softwares/fstat.htm.
41. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959. 1461096, 10835412.
42. Falush D, Stephens M, Pritchard JK. Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 2003, 164:1567-1587. 1462648, 12930761.
43. Weir BS, Cockerham CC. Estimating F-statistics for the analysis of population structure. Evolution 1984, 38:1358-1370.
44. Belkhir KP, Borsa P, Chikhi L, Raufaste N, Bonhomme F. Genetix 4.04, logiciel sous windows TM pour la genetic des populations 2002, Laboratoire Génome, Populations, Interactions, Montpellier: Université de Montpellier, France.
45. Felsenstein J. PHYLIP, phylogeny inference package, Version 3.57 1993, Seattle: University of Washington.
46. Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A. GENECLASS2: A Software for Genetic Assignment and First-Generation Migrant Detection. J Hered 2004, 95(6):536-539. 10.1093/jhered/esh074, 15475402.
47. Galindo-Cardona A, Monmany AC, Moreno-Jackson R, Rivera-Rivera C, Huertas-Dones C, Caicedo-Quiroga L, Giray T. Landscape analyses of drone congregation areas of the honey bee Apis mellifera. J Insect Sci 2012, 12:104. 3605025, 23437991.
48. Barton NH, Hewitt GM. Adaptation, speciation and hybrid zones. Nature 1989, 341:497-503. 10.1038/341497a0, 2677747.
49. Arnold ML. Natural hybridization as an evolutionary process. Annu Rev Ecol Syst 1992, 23:237-261.
50. Arnold ML. Natural hybridization and evolution 1997, New York: Oxford University Press.
51. Rhymer JM, Simberloff D. Extinction by Hybridization and Introgression. Annu Rev Ecol Syst 1996, 27:83.
52. Mallet J. Hybridization as an invasion of the genome. Trends Ecol Evol 2005, 20:229. 10.1016/j.tree.2005.02.010, 16701374.
53. Hunt GJ, Amdam GV, Schlipalius D, Emore C, Sardesai N, Williams CE, Rueppell O, Guzmán-Novoa E, Arechavaleta-Velasco M, Chandra S, Fondrk MK, Beye M, Page RE. Behavioral genomics of honeybee foraging and nest defense. Naturwissenschaften 2007, 94:247-267. 10.1007/s00114-006-0183-1, 1829419, 17171388.
54. Navajas M, Migeon A, Alaux C, Martin-Magniette ML, Robinson GE, Evans JD, Cros-Arteil C, Crauser D, Le Cont Y. Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection. BMC Genomics 2008, 9:301. 10.1186/1471-2164-9-301, 2447852, 18578863.
55. Anderson DL, Trueman JWH. Varroa jacobsoni (Acari: Varroidae) is more than one species. Exp Appl Acarol 2000, 24:165-189. 10.1023/A:1006456720416, 11108385.
56. Beye M, Gattermeier I, Hasselmann M, Gempe T, Schioett M, Baines JF, Schlipalius D, Mougel F, Emore C, Rueppell O, Sirviö A, Guzmán-Novoa E, Hunt G, Solignac M, Page RE. Exceptionally high levels of recombination across the honey bee genome. Genome Res 2006, 16:1339-1344. 10.1101/gr.5680406, 1626635, 17065604.
57. Tsuruda JM, Harris JW, Bourgeois L, Danka RG, Hunt GJ. High-Resolution Linkage Analyses to Identify Genes That Influence Varroa Sensitive Hygiene Behavior in Honey Bees. PLoS ONE 2012, 7(11):e48276. 10.1371/journal.pone.0048276, 3487727, 23133626.
58. Endler JA. Natural selection in the wild 1986, New Jersey: Princeton University Press.