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Assessment of genetic diversity and population structure of Eulaema nigrita (Hymenoptera: Apidae: Euglossini) as a factor of habitat type in Brazilian Atlantic forest fragments

Published online by Cambridge University Press:  26 May 2021

Claudinéia Pereira Costa Open the ORCID record for Claudinéia Pereira Costa [Opens in a new window] ,
Clycie Aparecida da Silva Machado  and
Tiago Mauricio Francoy Open the ORCID record for Tiago Mauricio Francoy [Opens in a new window]
Claudinéia Pereira Costa
Affiliation:
Departamento de Genética, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, São Paulo, 14049-900, Brazil Department of Entomology, University of California, Riverside, California, 92521, United States of America
Clycie Aparecida da Silva Machado
Affiliation:
Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, São Paulo, 14049-900, Brazil
Tiago Mauricio Francoy*
Affiliation:
Escola de Artes, Ciências e Humanidades, Universidade de São Paulo, São Paulo, São Paulo, 03828-000, Brazil
*
*Corresponding author. Email: tfrancoy@usp.br
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Abstract

In many organisms, habitat affects ecological and genetic diversity and, for certain species, it is expected that a large population should have higher genetic diversity than a smaller population. We analysed the genetics of males of the orchid bee, Eulaema nigrita (Hymenoptera: Apidae) and examined the links between local abundance and habitat with genetic diversity. We also investigated the impact of landscape features on genetic population structure, through microsatellite and mitochondrial DNA analysis, among populations found across 700 km of Brazilian Atlantic forest fragments. We found that genetic variation was not a function of local abundance, but it correlated significantly with habitat. There was significant but low genetic differentiation among populations. We found a single mitochondrial DNA haplotype in all sequenced specimens, which may be widespread throughout the Atlantic forest. Our results reinforce the idea that orchid bees can fly long distances. High-dispersal capacity, together with insufficient time in eventual isolation, can directly contribute to the high degree of similarity among populations for this species, despite their wide geographical distribution.

Type
Research Papers
Information
The Canadian Entomologist , Volume 153 , Issue 4 , August 2021 , pp. 446 - 460
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© The Author(s), 2021. Published by Cambridge University Press on behalf of the Entomological Society of Canada

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Footnotes

Subject editor: Leah Flaherty

References

Ackerman, J.D. 1983. Diversity and seasonality of male euglossine bees (Hymenoptera: Apidae) in central Panama. Ecology, 64: 274–283. https://doi.org/10.2307/1937075.CrossRefGoogle Scholar
Alvarenga, P.E.F., Freitas, R.F., and Augusto, S.C. 2007. Diversidade de Euglossini (Hymenoptera: Apidae) em áreas de Cerrado do Triângulo Mineiro, MG. Bioscience Journal, 23: 30–37. http://www.seer.ufu.br/index.php/biosciencejournal/article/view/6802.Google Scholar
Avise, J.C. and Hamrick, J.L. 1996. Conservation genetics: case studies from nature. Springer U.S., New York, New York, United States of America.CrossRefGoogle Scholar
Barton, K. 2020. MuMIn: Multi-model inference. R package, version 1.43.17. Available from http://CRAN.R-project.org/package=MuMIn.Google Scholar
Bates, D., Maechler, M., Bolker, B., and Walker, S. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67: 1–48. https://arxiv.org/abs/1406.5823.CrossRefGoogle Scholar
Boff, S., Soro, A., Paxton, R.J., and Alves-dos-Santos, I. 2014. Island isolation reduces genetic diversity and connectivity but does not significantly elevate diploid male production in a neotropical orchid bee. Conservation Genetics, 15: 1123–1135. https://doi.org/10.1007/s10592-014-0605-0.CrossRefGoogle Scholar
Calaboni, A., Tambosi, L.R., Igari, A.T., Farinaci, J.S., Metzger, J.P., and Uriarte, M. 2018. The forest transition in São Paulo, Brazil: historical patterns and potential drivers. Ecology and Society, 23: 7. https://doi.org/10.5751/ES-10270–230407.CrossRefGoogle Scholar
Cohen, J. 1988. Statistical power analysis for the behavioral sciences. Second edition. Laurence Erlbaum Associates, Hillsdale, New Jersey, United States of America.Google Scholar
Costa, C.P., Machado, C.A.S., Santiago, W.M.S., Dallacqua, R.P., Garófalo, C.A., and Francoy, T.M. 2020. Biome variation, not distance between populations, explains morphological variability in the orchid bee Eulaema nigrita (Hymenoptera, Apidae, Euglossini). Apidologie, 51: 984–996. https://doi.org/10.1007/s13592-020-00776-z.CrossRefGoogle Scholar
Crozier, Y.C., Koulianos, S., and Crozier, R.H. 1991. An improved test for Africanized honeybee mitochondrial DNA. Experientia, 47: 968–969.CrossRefGoogle ScholarPubMed
Davis, E.S., Murray, T.E., Fitzpatrick, U., Brown, M.J., and Paxton, R.J. 2010. Landscape effects on extremely fragmented populations of a rare solitary bee, Colletes floralis . Molecular Ecology, 19: 4922–4935. https://doi.org/10.1111/j.1365-294X.2010.04868.x.CrossRefGoogle ScholarPubMed
Dick, C.W., Roubik, D.W., Gruber, K.F., and Bermingham, E. 2004. Long-distance gene flow and cross-Andean dispersal of lowland rainforest bees (Apidae: Euglossini) revealed by comparative mitochondrial DNA phylogeography. Molecular Ecology, 13: 3775–3785. https://doi.org/10.1111/j.1365–294X.2004.02374.x.CrossRefGoogle ScholarPubMed
Dressler, R.L. 1982. Biology of the orchid bees (Euglossini). Annual Review of Ecology and Systematics, 13: 373–394. https://doi.org/10.1146/annurev.es.13.110182.002105.CrossRefGoogle Scholar
Earl, D.A. and von Holdt, B.M. 2012. Structure Harvester: a website and program for visualising Structure output and implementing the Evanno method. Conservation Genetics Resources, 4: 359–361. https://doi.org/10.1007/s12686-011-9548-7.CrossRefGoogle Scholar
Ellis, J.S., Knight, M.E., Darvill, B., and Goulson, D. 2006. Extremely low effective population sizes, genetic structuring and reduced genetic diversity in a threatened bumblebee species, Bombus sylvarum (Hymenoptera: Apidae). Molecular Ecology, 15: 4375–4386. https://doi.org/10.1111/j.1365–294X.2006.03121.x.CrossRefGoogle Scholar
Fahrig, L. 2003. Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics, 34: 487–515. https://doi.org/10.1146/annurev.ecolsys.34.011802.132419.CrossRefGoogle Scholar
Frankham, R. 2005. Genetics and extinction. Biological Conservation, 126: 131–140. https://doi.org/10.1016/j.biocon.2005.05.002.CrossRefGoogle Scholar
Freiria, G.A., Ruim, J.B., de Souza, R.F., and Sofia, S.H. 2012. Population structure and genetic diversity of the orchid bee Eufriesea violacea (Hymenoptera, Apidae, Euglossini) from Atlantic forest remnants in southern and southeastern Brazil. Apidologie, 43: 392–402. https://doi.org/10.1007/s13592-011-0104-y.CrossRefGoogle Scholar
Grassi-Sella, M.L., Garófalo, C.A., and Francoy, T.M. 2018. Morphological similarity of widely separated populations of two Euglossini (Hymenoptera: Apidae) species based on geometric morphometrics of wings. Apidologie, 49: 151–161.CrossRefGoogle Scholar
Habel, J.C., Husemann, M., Finger, A., Danley, P.D., and Zachos, F.E. 2014. The relevance of time series in molecular ecology and conservation biology. Biological Reviews, 89: 484–492. https://doi.org/10.1111/brv.12068.CrossRefGoogle ScholarPubMed
Hothorn, T., Bretz, F., and Westfall, P. 2008. Simultaneous inference in general parametric models. Biometrical Journal, 50: 346–363. https://doi.org/10.1002/bimj.200810425.CrossRefGoogle ScholarPubMed
Janzen, D.H. 1971. Euglossine bees as long-distance pollinators of tropical plants. Science, 171: 203–205.CrossRefGoogle ScholarPubMed
Janzen, D.H. 1981. Bee arrival at two Costa Rican female Catasetum orchid inflorescences, and a hypothesis on euglossine population structure. Oikos, 36: 177–183. https://doi.org/10.1126/science.171.3967.203.CrossRefGoogle Scholar
Jha, S. 2015. Contemporary human-altered landscapes and oceanic barriers reduce bumblebee gene flow. Molecular Ecology, 24: 993–1006. https://doi.org/10.1111/mec.13090.CrossRefGoogle Scholar
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., et al. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28: 1647–1649. https://doi.org/10.1093/bioinformatics/bts199.CrossRefGoogle ScholarPubMed
Keenan, K., McGinnity, P., Cross, T.F., Crozier, W.W., and Prodöhl, P.A. 2013. diveRsity: an R package for the estimation of population genetics parameters and their associated errors. Methods in Ecology and Evolution, 4: 782–788.CrossRefGoogle Scholar
Koch, J.B., Looney, C., Sheppard, S., and Strange, J.P. 2017. Patterns of population genetic diversity and structure across bumblebee communities in the Pacific Northwest. Conservation Genetics, 18: 507–520. https://doi.org/10.1007/s10592-017-0944-8.CrossRefGoogle Scholar
Kokko, H. and López-Sepulcre, A. 2006. From individual dispersal to species ranges: perspectives for a changing world. Science, 313: 789–791. https://doi.org/10.1126/science.1128566.CrossRefGoogle ScholarPubMed
Lewis, S.L., Edwards, D.P., and Galbraith, D. 2015. Increasing human dominance of tropical forests. Science, 349: 827–832. https://doi.org/10.1126/science.aaa9932.CrossRefGoogle ScholarPubMed
López-Uribe, M.M. and Del Lama, M.A. 2007. Molecular identification of species of the genus Euglossa Latreille (Hymenoptera: Apidae, Euglossini). Neotropical Entomology, 36: 712–720. https://doi.org/10.1590/S1519-566X2007000500012.CrossRefGoogle Scholar
López-Uribe, M.M., Soro, A., and Jha, S. 2017. Conservation genetics of bees: advances in the application of molecular tools to guide bee pollinator conservation. Conservation Genetics, 18: 501–506. https://doi.org/10.1007/s10592-017-0975-1.CrossRefGoogle Scholar
Lozier, J.D., Strange, J.P., and Koch, J.B. 2013. Landscape heterogeneity predicts gene flow in a widespread polymorphic bumble bee, Bombus bifarius (Hymenoptera: Apidae). Conservation Genetics, 14: 1099–1110. https://doi.org/10.1007/s10592-013-0498-3.CrossRefGoogle Scholar
Machado, C.A.S., Costa, C.P., and Francoy, T.M. 2018. Different physiognomies and the structure of Euglossini bee (Hymenoptera: Apidae) communities. Sociobiology, 65: 471–481. http://dx.doi.org/10.13102/sociobiology.v65i3.2718.CrossRefGoogle Scholar
Maebe, K., Karise, R., Meeus, I., Mänd, M., and Smagghe, G. 2019a. Level of genetic diversity in European bumblebees is not determined by local species abundance. Frontiers in Genetics, 10: 1262. https://doi.org/10.3389/fgene.2019.01262.CrossRefGoogle Scholar
Maebe, K., Karise, R., Meeus, I., Mänd, M., and Smagghe, G. 2019b. Pattern of population structuring between Belgian and Estonian bumblebees. Scientific Reports, 9: 9651. https://doi.org/10.1038/s41598-019-46188-7.CrossRefGoogle ScholarPubMed
Maebe, K., Meeus, I., Vray, S., Claeys, T., Dekoninck, W., Boevé, J.L., et al. 2016. A century of temporal stability of genetic diversity in wild bumblebees. Scientific Reports, 6: 38289. https://doi.org/10.1038/srep38289.CrossRefGoogle ScholarPubMed
Meirmans, P.G. and Hedrick, P.W. 2011 Assessing population structure: FST and related measures. Molecular Ecology Resources, 11: 5–18. https://doi.org/10.1111/j.1755-0998.2010.02927.x.CrossRefGoogle Scholar
Morato, E.F. 1998. Estudos sobre comunidades de abelhas Euglossini. Anais do Encontro sobre Abelhas, 3: 135–143.Google Scholar
Morellato, L.P.C. and Haddad, C.F.B. 2000. Introduction: the Brazilian Atlantic forest. Biotropica, 32: 786–792. http://www.jstor.org/stable/2663917.CrossRefGoogle Scholar
Moure, J.S., Melo, G.A.R., and Faria, L.R.R. Jr. 2008. Euglossini Latreille, 1802 [online]. In Catalogue of bees (Hymenoptera, Apoidea) in the Neotropical region. Edited by J.S. Moure, D. Urban, and G.A.R. Melo. Available from http://www.moure.cria.org.br/catalogue [accessed 1 January 2016].Google Scholar
Nakagawa, S. and Schielzeth, H. 2013. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods in Ecology and Evolution, 4: 133–142. https://doi.org/10.1111/j.2041-210x.2012.00261.x.CrossRefGoogle Scholar
Nei, M. 1977. F-statistics and analysis of gene diversity in subdivided populations. Annals of Human Genetics, 41: 225–233.CrossRefGoogle ScholarPubMed
Peakall, R. and Smouse, P.E. 2006. GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6: 288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x.CrossRefGoogle Scholar
Peakall, R. and Smouse, P.E. 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics, 28: 2537–2539. https://doi.org/10.1093/bioinformatics/bts460.CrossRefGoogle ScholarPubMed
Penha, R.E.S., Gaglianone, M.C., Almeida, F.S., Boff, S.V., and Sofia, S.H. 2015. Mitochondrial DNA of Euglossa iopoecila (Apidae, Euglossini) reveals two distinct lineages for this orchid bee species endemic to the Atlantic forest. Apidologie, 46: 346–358. http://dx.doi.org/10.1007/s13592-014-0329-7.CrossRefGoogle Scholar
Peruquetti, R.C., Campos, L.A.O., Coelho, C.D.P., Abrantes, C.V.M., and Lisboa, L.C.O. 1999. Abelhas Euglossini (Apidae) de áreas de Mata Atlântica: abundância, riqueza e aspectos biológicos. Revista Brasileira de Zoologia, 16: 101–118. https://doi.org/10.1590/S0101-81751999000600012.CrossRefGoogle Scholar
Pinto, N.S., Silva, D.P., Rodrigues, J.G., and De Marco, P. 2015. The size but not the symmetry of the wings of Eulaema nigrita Lepeletier (Apidae: Euglossini) is affected by human-disturbed landscapes in the Brazilian Cerrado savanna. Neotropical Entomology, 44: 439–447. https://doi.org/10.1007/s13744–015–0316–3.CrossRefGoogle Scholar
Pokorny, T., Loose, D., Dyker, G., Quezada-Euán, J.J., and Eltz, T. 2015. Dispersal ability of male orchid bees and direct evidence for long-range flights. Apidologie, 46: 224–237. https://doi.org/10.1007/s13592-014-0317-y.CrossRefGoogle Scholar
Pritchard, J.K., Stephens, M., and Donnelly, P. 2000. Inference of population structure using multilocus genotype data. Genetics, 155: 945–959.CrossRefGoogle ScholarPubMed
R Core Team. 2019. R: a language and environment for statistical computing [online]. R Foundation for Statistical Computing, Vienna, Austria. Available from https://www.R-project.org/ Google Scholar
Raw, A. 1989. The dispersal of euglossine bees between isolated patches of eastern Brazilian wet forest (Hymenoptera: Apidae). Revista Brasileira de Entomologia, 33: 103–107.Google Scholar
Raymond, M. and Rousset, F. 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity, 86: 248–249. https://doi.org/10.1093/oxfordjournals.jhered.a111573.CrossRefGoogle Scholar
Rebêlo, J.M.M. and Garófalo, C.A. 1991. Diversidade e sazonalidade de machos de Euglossini (Hymenoptera, Apidae) e preferência por iscas-odores em um fragmento de floresta no sudeste do Brasil. Revista Brasileira de Entomologia, 51: 787–799.Google Scholar
Rebêlo, J.M.M. and Garófalo, C.A. 1997. Comunidades de machos de Euglossini (Hymenoptera: Apidae) em matas semidecíduas do nordeste do Estado de São Paulo. Anais da Sociedade Entomologica do Brasil, 26: 243–255. https://doi.org/10.1590/S0301-80591997000200005.CrossRefGoogle Scholar
Rissler, L.J. 2016. Union of phylogeography and landscape genetics. Proceedings of the National Academy of Sciences, 113: 8079–8086. https://doi.org/10.1073/pnas.1601073113.CrossRefGoogle ScholarPubMed
Rocha-Filho, L.C., Cerântola, N.C.M., Garófalo, C.A., Imperatriz Fonseca, V.L., and Del Lama, M.A. 2013. Genetic differentiation of the Euglossini (Hymenoptera, Apidae) populations on a mainland coastal plain and an island in southeastern Brazil. Genetica, 141: 65–74. https://doi.org/10.1007/s10709–013–9706–9.CrossRefGoogle Scholar
Rocha-Filho, L.C. and Garófalo, C.A. 2013. Community ecology of euglossine bees in the coastal Atlantic forest of São Paulo State, Brazil. Journal of Insect Science, 13: 1–19. https://doi.org/10.1673/031.013.2301.CrossRefGoogle ScholarPubMed
Rocha-Filho, L.C. and Garófalo, C.A. 2014. Phenological patterns and preferences for aromatic compounds by male Euglossine bees (Hymenoptera, Apidae) in two coastal ecosystems of the Brazilian Atlantic forest. Neotropical Entomology, 43: 9–20. https://doi.org/10.1007/s13744–013–0173-x.CrossRefGoogle ScholarPubMed
Rocha-Filho, L.C., Krug, C., Silva, C.I., and Garófalo, C.A. 2012. Floral resources used by Euglossini bees (Hymenoptera: Apidae) in coastal ecosystems of the Atlantic forest. Psyche, 2012: 934951. https://doi.org/10.1155/2012/934951.Google Scholar
Rousset, F. 2008. Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources, 8: 103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x.CrossRefGoogle Scholar
Russildi, G., Arroyo-Rodríguez, V., Hernández-Ordóñez, O., Pineda, E., and Reynoso, V.H. 2016. Species- and community-level responses to habitat spatial changes in fragmented rainforests: assessing compensatory dynamics in amphibians and reptiles. Biodiversity and Conservation, 25: 375–392. https://doi.org/10.1007/s10531–016–1056–3.CrossRefGoogle Scholar
Ryman, N. and Palm, S. 2006. POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Molecular Ecology Notes, 6: 600–602. https://doi.org/10.1111/j.1471-8286.2006.01378.x.CrossRefGoogle Scholar
Schuelke, M. 2000. An economic method for the fluorescent labelling of PCR fragments. Nature Biotechnology, 18: 233–234. https://doi.org/10.1038/72708.CrossRefGoogle Scholar
Silva, D.P. and De Marco, P. Jr. 2014. No evidence of habitat loss affecting the orchid bees Eulaema nigrita Lepeletier and Eufriesea auriceps Friese (Apidae: Euglossini) in the Brazilian Cerrado savanna. Neotropical Entomology, 43: 509–518. https://doi.org/10.1007/s13744-014-0244-7.CrossRefGoogle ScholarPubMed
Silva, M.C., Lomônaco, C., Augusto, S.C., and Kerr, W.E. 2009. Climatic and anthropic influence on size and fluctuating asymmetry of Euglossine bees (Hymenoptera, Apidae) in a semideciduous seasonal forest reserve. Genetics and Molecular Research, 8: 730–737.CrossRefGoogle Scholar
Sofia, S.H., Paula, F.M., Santos, A.M., Almeida, F.S., and Sodré, L.M.K. 2005. Genetic structure analyses of Eufriesea violacea (Hymenoptera, Apidae) populations from southern Brazilian Atlantic rainforest remnants. Genetics and Molecular Biology, 28: 479–484. http://dx.doi.org/10.1590/S1415-47572005000300026.CrossRefGoogle Scholar
Soro, A., Field, J., Bridge, C., Cardinal, S.C., and Paxton, R.J. 2010. Genetic differentiation across the social transition in a socially polymorphic sweat bee, Halictus rubicundus . Molecular Ecology, 19: 3351–3363. https://doi.org/10.1111/j.1365-294X.2010.04753.x.CrossRefGoogle Scholar
Soro, A., Quezada-Euan, J.J.G., Theodorou, P., Moritz, R.F.A., and Paxton, R.J. 2017. The population genetics of two orchid bees suggests high dispersal, low diploid male production and only an effect of island isolation in lowering genetic diversity. Conservation Genetics, 18: 607–619. https://doi.org/10.1007/s10592-016-0912-8.CrossRefGoogle Scholar
Souza, R.O., Cervini, M., Del Lama, M.A., and Paxton, R.J. 2007. Microsatellite loci for euglossine bees (Hymenoptera: Apidae). Molecular Ecology Notes, 6: 1352–1356. https://doi.org/10.1111/j.1471–8286.2007.01878.x.CrossRefGoogle Scholar
Souza, R.O., Del Lama, M.A., Cervini, M., Mortari, N., Eltz, T., Zimmermann, Y., et al. 2010. Conservation genetics of neotropical pollinators revisited: microsatellite analysis suggests that diploid males are rare in orchid bees. Evolution, 64: 3318–3326. https://doi.org/10.1111/j.1558-5646.2010.01052.x.CrossRefGoogle ScholarPubMed
Suni, S.S., Bronstein, J.L., and Brosi, B.J. 2014. Spatio-temporal genetic structure of a tropical bee species suggests high dispersal over a fragmented landscape. Biotropica, 46: 202–2019. https://doi.org/10.1111/btp.12084.CrossRefGoogle Scholar
Toledo, J.A.M., Junqueira, C.N., Augusto, S.C., and Brito, R.M. 2017. Accessing the genetic content of Xylocopa frontalis bees (Apidae, Xylocopini) for sustainable management in pollination services of passion fruit. Apidologie, 48: 795–805. https://doi.org/10.1007/s13592-017-0524-4.CrossRefGoogle Scholar
Tonhasca, A., Albuquerque, G.S., and Blackmer, J.L. 2003. Dispersal of euglossine bees between fragments of the Brazilian Atlantic forest. Journal of Tropical Ecology, 19: 99–102. https://doi.org/10.1017/S0266467403003122.CrossRefGoogle Scholar
Tonhasca, A., Blackmer, J.L., and Albuquerque, G.S. 2002. Abundance and diversity of euglossine bees in the fragmented landscape of the Brazilian Atlantic forest. Biotropica, 34: 416–422. https://doi.org/10.1111/j.1744-7429.2002.tb00555.x.CrossRefGoogle Scholar
Uehara-Prado, M. and Garófalo, C.A. 2006. Small-scale elevational variation in the abundance of Eufriesea violacea (Blanchard) (Hymenoptera: Apidae). Neotropical Entomology, 35: 446–451. https://doi.org/10.1590/S1519-566X2006000400004.CrossRefGoogle Scholar
Walsh, P.S., Metzger, D.A., and Higuchi, R. 1991. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques, 10: 506–513.Google ScholarPubMed
Wright, S. 1978. Evolution and the genetics of populations. Volume 4. Variability within and among natural populations. University of Chicago Press, Chicago, Illinois, United States of America.Google Scholar
Zayed, A. 2009. Bee genetics and conservation. Apidologie, 40: 237–262.CrossRefGoogle Scholar
Zayed, A. and Packer, L. 2007. The population genetics of a solitary oligolectic sweat bee, Lasioglossum (Sphecodogastra) oenotherae (Hymenoptera: Halictidae). Heredity, 99: 397–405. https://doi.org/10.1038/sj.hdy.6801013.CrossRefGoogle Scholar
Zimmermann, Y., Schorkopf, D.L.P., Moritz, R.F.A., Pemberton, R.W., Quezada-Euan, J.J.G., and Eltz, T. 2011. Population genetic structure of orchid bees (Euglossini) in anthropogenically altered landscapes. Conservation Genetics, 12: 1183–1194. https://doi.org/10.1007/s10592-011-0221-1.CrossRefGoogle Scholar
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