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A geometric morphometric and microsatellite analyses of Scaptotrigona mexicana and S. pectoralis (Apidae: Meliponini) sheds light on the biodiversity of Mesoamerican stingless bees

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Abstract

Geometric morphometrics and molecular methods are effective tools to study the variability of stingless bee populations and species that merit protection given their worldwide decline. Based on previous evidence of cryptic lineages within the Scaptotrigona genus, we tested the existence of multiple evolutionary lineages within the species S. mexicana and we investigated the status of S. pectoralis. By analyzing their population structure, we found differences between the Pacific and Atlantic populations of each of these species, although geometric morphometrics of the wing only confirmed these results in S. mexicana. There was a tendency towards enhanced genetic differentiation over larger distances in the Atlantic populations of both species but not in the Pacific populations. These results revealed a pattern of differentiation among evolutionary units and a specific distribution of genetic diversity within these Scaptotrigona species in Mesoamerica, suggesting the need for future taxonomic revisions, as well as activities aimed at management and conservation.

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References

  • Albores-González ML, García Guerra TG, Durán Olguín L, Aguliar Ayón A (2011) Experiencia de la Unión de Cooperativas Tosepan en el fomento a la cría de las abejas nativas Pitsilnejmej (Scaptotrigona mexicana) in Memorias del VII Seminario Mesaomerciano sobre abejas nativas, pp 95–99

  • Álvarez ME, Morrone JJ (2004) Propuesta de áreas para la conservación de aves de México, empleando herramientas panbiogeográficas e índices de complementariedad. Interciencia 29:112–120

    Google Scholar 

  • Anducho-Reyes MA, Cognato AI, Hayes JL, Zuniga G (2008) Phylogeography of the bark beetle Dendroctonus mexicanus Hopkins (Coleoptera: Curculionidae: Scolytinae). Mol Phylogenet Evol 49:930–940

    Article  CAS  PubMed  Google Scholar 

  • Arias MC, Brito RM, Francisco FO, Moretto G, Oliveira FF, Silvestre D, Sheppard WS (2006) Molecular markers as a tool for population and evolutionary studies of stingless bee. Apidologie 37:259–274

    Article  CAS  Google Scholar 

  • Ayala R (1999) Revisión de las abejas sin aguijón de México (Hymenoptera, Apoidea). Folia Entomol Mex 106:1–123

    Google Scholar 

  • Ayala R, González VH, Engels MS (2013) Mexican stingless bees (Hymenoptera: Apidae): diversity, distribution, and indigenous knowledge. In: Vit P, Pedro SRM, Roubik DW (eds) Pot-Honey: a legacy of stingless bees. Springer, New York, pp 135–152

    Chapter  Google Scholar 

  • Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol Ecol 11:155–165

    Article  PubMed  Google Scholar 

  • Barkan NP, Aytekin AM (2013) Systematical studies on the species of the subgenus Bombus (Thoracobombus) (Hymenoptera: Apidae, Bombus Latreille) in Turkey. Zootaxa 3737(2):167–183

    Article  CAS  PubMed  Google Scholar 

  • Bonatti V, Simões ZLP, Franco FF, Francoy TM (2014) Evidence of at least two evolutionary lineages in Melipona subnitida (Apidae, Meliponini) suggested by mtDNA variability and geometric morphometrics of forewings. Naturwissenschaften 101:17–24

    Article  CAS  PubMed  Google Scholar 

  • Bookstein FL (1991) Morphometric tools for landmark data. Cambridge University Press, Cambridge

    Google Scholar 

  • Borges AA, Campos LAO, Salomão TMF, Tavares MG (2010) Genetic variability in five populations of Partamona helleri (Hymenoptera: Apidae) from Minas Gerais State, Brazil. Genet Mol Biol 33:781–784

    Article  PubMed  PubMed Central  Google Scholar 

  • Bouga M, Alaux C, Bienkowska M, Büchler R, Carreck NL, Cauia E, Chlebo R, Dahle B, Dall’Olio R, De la Rúa P, Gregorc A, Ivanova E, Kence A, Kence M, Kezic N, Kiprijanovska H, Kozmus P, Kryger P, Le Conte Y, Lodesani M, Murilhas AM, Siceanu A, Soland G, Uzunov A, Wilde J (2011) A review of methods for discrimination of honey bee populations as applied to European beekeeping. J Apic Res 50(1):51–84

    Article  Google Scholar 

  • Brown JC, Albrecht C (2001) The effect of tropical deforestation on stingless bees of the genus Melipona (Insecta: Hymenoptera: Apidae: Meliponini) in central Rondonia, Brazil. J Biogeogr 28:623–624

    Article  Google Scholar 

  • Brown MJF, Paxton RJ (2009) The conservation of bees: a global perspective. Apidologie 40:410–416

    Article  Google Scholar 

  • Byatt MA, Chapman NC, Latty T, Oldroyd BP (2016) The genetic consequences of the anthropogenic movement of social bees. Insectes Soc 63(1):15–24

    Article  Google Scholar 

  • Camargo JMF, Pedro SRM (2013) Meliponini Lepeletier, 1836. In: Moure JS, Urban D, Melo GAR. (Orgs). Catalogue of bees (Hymenoptera, Apoidea) in the Neotropical Region-online version; [cited 2012 Sep 29]. http://www.moure.cria.org.br/catalogue. Accessed 23 Sept 2015

  • da Silva FL, Sella MLG, Francoy TM, Costa AHR (2015) Evaluating classification and feature selection techniques for honeybee subspecies identification using wing images. Comput Electron Agric 114:68–77

    Article  Google Scholar 

  • Dorn PL, Calderon C, Melgar S, Moguel B, Solorzano E, Dumonteil E, Rodas A, De la Rúa N, Garnica R, Monroy C (2009) Two distinct Triatoma dimidiata (Latreille, 1811) taxa are found in sympatry in Guatemala and Mexico. PLoS Negl Trop Dis 3:e393

    Article  PubMed  PubMed Central  Google Scholar 

  • Duarte OMP, Gaiotto FA, Costa MA (2014) Genetic differentiation in the stingless bee, Scaptotrigona xanthotricha Moure, 1950 (Apidae, Meliponini): a species with wide geographic distribution in the Atlantic rainforest. J Hered 105(4):477–484

    Article  Google Scholar 

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conser Genet Res 4(2):359–361

    Article  Google Scholar 

  • Engels W, Imperatriz-Fonseca VL (1990) Caste development, reproductive strategies and control of fertility in honey-bees and stingless bees. In: Engels W (ed) Social insects: an evolutionary approach to castes and reproduction. Springer, Berlin, pp 166–230

    Chapter  Google Scholar 

  • Estoup A, Scholl A, Pouvreau A, Solignac M (1995) Monoandry and polyandry in bumble bees (Hymenoptera: Bombinae) as evidenced by highly variable microsatellites. Mol Ecol 4:89–93

    Article  CAS  PubMed  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10(3):564–567

    Article  Google Scholar 

  • Fernandes CRM, Martins CF, Ferreira KM, Del Lama MA (2012) Gene variation, population differentiation and sociogenetic structure of nests of Partamona seridoensis (Hymenoptera: Apidae, Meliponini). Biochem Genet 50:325–335

    Article  CAS  PubMed  Google Scholar 

  • Ferreira VS, Aguiar CML, Costa MA, Silva JG (2011) Morphometric analysis of populations of Centris aenea Lepeletier (Hymenoptera: Apidae) from Northeastern Brazil. Neotrop Entomol 40:97–102

    Article  CAS  PubMed  Google Scholar 

  • Foley JA, DeFries R, Asner GP, Barford C, Bonan G, Carpenter SR, Chapin FS, Coe MT, Daily GC, Gibbs HK, Helkowski JH, Holloway T, Howard EA, Kucharik CJ, Monfreda C, Patz JA, Prentice IC, Ramankutty N, Snyder PK (2005) Global consequences of land use. Science 309:570–574

    Article  CAS  PubMed  Google Scholar 

  • Francisco FO, Brito RM, Arias MC (2006) Allele number of heterozigosity for microsatellite loci in different stingless bee species (Hymenoptera: Apidae: Meliponini). Neotrop Entomol 35:638–643

    Article  CAS  Google Scholar 

  • Francisco FO, Nunes-Silva P, Francoy TM, Wittmann D, Imperatriz-Fonseca VL, Arias MC, Morgan ED (2008) Morphometrical, biochemical and molecular tools for assessing biodiversity. An example in Plebeia remota (Holmberg, 1903) (Apidae, Meliponini). Insectes Soc 55(3):231–237

    Article  Google Scholar 

  • Francoy TM, Grassi ML, Imperatriz-Fonseca VL, May-Itzá WdJ, Quezada-Euán JJG (2011) Geometric morphometrics of the wing as a tool for assigning genetic lineages and geographic origin to Melipona beecheii (Hymenoptera: Meliponini). Apidologie 42:499–507

    Article  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Freitas BM, Imperatriz-Fonseca VL, Medina LM, Kleinert AMP, Galetto L, Nates-Parra G, Quezada-Euán JJG (2009) Diversity, threats and conservation of native bees in the Neotropics. Apidologie 40:332–346

    Article  Google Scholar 

  • Gonçalves PHP (2010) Análise da variabilidade genética de uma pequena população de Frieseomelitta varia (Hymenoptera, Apidae, Meliponini) por meio de análise do DNA mitocondrial, microssatélites e morfometria geométrica das asas. Dissertation, University of São Paulo

  • González-Acereto JA (2012) La importancia de la meliponicultura en México, con énfasis en la Península de Yucatán. Bioagrociencias 5(1):34–41

    Google Scholar 

  • González-Acereto JA, Quezada-Euá JJG, Medina-Medina LA (2006) New perspectives for stingless beekeeping in the Yucatan: results of an integral program to rescue and promote the activity. J Apicult Res 45(3):234–239

    Article  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9

    Google Scholar 

  • Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638

    Article  CAS  PubMed  Google Scholar 

  • Hurtado-Burillo M, Ruiz C, May-Itzá WdJ, Quezada-Eúan JJG, De la Rúa P (2013) Barcoding stingless bees: genetic diversity of the economically important genus Scaptotrigona in Mesoamerica. Apidologie 44:1–10

    Article  Google Scholar 

  • Ish-Am G, Barrientos-Priego F, Castañeda-Vildozola A, Gazit S (1999) Avocado (Persea americana Mill) pollinators in its region of origin. Rev Chapingo Ser Hortic 5:137–143

    Google Scholar 

  • Jaffé R, Pope N, Giannini TC, Acosta AL, Alves DA, Arias MC, Francisco FO, González A, Imperatriz-Fonseca VL, Jha S, De la Rúa P, Tavares MG, Carvalheiro LG (2016) Gene flow in stingless bees is determined by geographic distance and beekeeping practices. Mol Ecol (in press)

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  CAS  PubMed  Google Scholar 

  • Kalinowski ST (2005) HP-Rare: a computer program for performing rarefaction on measures of allelic diversity. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  • Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11:353–357

    Article  PubMed  Google Scholar 

  • Kraus FB, Weinhold S, Moritz RFA (2008) Genetic structure of drone congregations of the stingless bee Scaptotrigona mexicana. Insectes Soc 55:22–27

    Article  Google Scholar 

  • Leberg PL (2002) Estimating allelic richness: effects of sample size and bottlenecks. Mol Ecol 11:2445–2449

    Article  CAS  PubMed  Google Scholar 

  • Lima Junior CA, Carvalho CAL, Nunes LA, Francoy TM (2012) Population divergence of Melipona scutellaris Latreille (Hymenoptera: Meliponina) in two Restricted Areas in Bahia, Brazil. Sociobiology 59:107–122

    Article  Google Scholar 

  • Luikart G, England PR (1999) Statistical analysis of microsatellite DNA data. Trends Ecol Evol 14:253–255

    Article  PubMed  Google Scholar 

  • Mann HB, Whitney DR (1947) On a test of whether one of two random variables is stochastically larger than the other. Ann Math Stat 18(1):50–60

    Article  Google Scholar 

  • Manzo C (2009) Informe Final de Actividades de la Huasteca. Módulo de Abejas sin Aguijón (Scaptotrigona mexicana) Municipio de Cocoxtlán S.L.P

  • May-Itzá WdJ, Quezada-Eúan JJG, Medina-Medina LA, Enriquez E, De la Rúa P (2010) Morphometric and genetic differentiation in isolated populations of the endangered Mesoamerican stingless bee Melipona yucatanica (Hymenoptera: Apoidea) suggest the existence of a two species complex. Conserv Genet 11:2079–2084

    Article  Google Scholar 

  • May-Itzá WdJ, Quezada-Eúan JJG, Ayala R, De la Rúa P (2012) Morphometric and genetic analyses differentiate Mesoamerican populations of the endangered stingless bee Melipona beecheii (Hymenoptera: Meliponidae) and support their conservation as two separate units. J Insect Conserv 16(5):723–731

    Article  Google Scholar 

  • Mendes MFM, Francoy TM, Nunes-Silva P, Menezes C, Imperatriz-Fonseca VL (2007) Intra-populational variability of Nannotrigona testaceicornis Lepeletier, 1836 (Hymenoptera, Meliponini) using relative warp analysis. Biosci J 23:147–152

    Google Scholar 

  • Michener CD (2007) The bees of the world, 2nd edn. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Morandin LA, Winston ML (2006) Pollinators provide economic incentive to preserve natural land in agroecosystems. Agric Ecosyst Environ 116:289–292

    Article  Google Scholar 

  • Mueller MY, Moritz RFA, Kraus FB (2012) Outbreeding and lack of temporal genetic structure in a drone congregation of the Neotropical stingless bee Scaptotrigona mexicana. Ecol Evol 2:1304–1311

    Article  PubMed  PubMed Central  Google Scholar 

  • Nunes LA, Passos GB, Carvalho CAL, Araújo ED (2013) Spatial variation of size and shape of the wing in Melipona quadrifasciata anthidioides Lepeletier, 1836 (Hymenoptera; Meliponini) assessed by geometric morphometrics. Braz J Biol 73:887–893

    Article  CAS  PubMed  Google Scholar 

  • Oleksa A, Tofilski A (2015) Wing geometric morphometrics and microsatellite analysis provide similar discrimination of honey bee subspecies. Apidologie 46(1):49–60

    Article  Google Scholar 

  • Paxton RJ, Weibschuh N, Quezada-Euán JJG (1999) Characterization of dinucleotide microsatellite loci for stingless bees. Mol Ecol 8:685–702

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) GENEALEX 6: genetic analysis in Excel, Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peters JM, Queller DC, Imperatriz-Fonseca VL, Strassmann JE (1998) Microsatellite loci for stingless bees. Mol Ecol 7:783–792

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Quezada-Euán JJG, May-Itzá WdJ, Rincón M, De la Rúa P, Paxton RJ (2012) Genetic and phenotypic differentiation in endemic Scaptotrigona hellwegeri (Apidae: Meliponini): implications for the conservation of stingless bee populations in contrasting environments. Insect Conserv Divers 5(6):433–443

    Article  Google Scholar 

  • Raymond M, Rousset F (1995a) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Raymond M, Rousset F (1995b) An exact test for population differentiation. Evolution 49:1283–1286

    Article  Google Scholar 

  • Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103

    Article  CAS  PubMed  Google Scholar 

  • Rice W (1989) Analysing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Rohlf FJ (2013) TPSdig v. 2.17. NY State University at Stony Brook, Stony Brook

    Google Scholar 

  • Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Russell KN, Ikerd H, Droege S (2005) The potential conservation value of unmowed powerline strips for native bees. Biol Conserv 124:133–148

    Article  Google Scholar 

  • Santiago LR, Francisco FO, Jaffé R, Arias MC (2016) Genetic variability in captive populations of the stingless bee Tetragonisca angustula. Genetica 144:397–405

    Article  PubMed  Google Scholar 

  • Schlick-Steiner BC, Steiner FM, Seifert B, Stauffer C, Christian E, Crozier RH (2010) Integrative taxonomy: a multisource approach to exploring biodiversity. Annu Rev Entomol 55:421–438

    Article  CAS  PubMed  Google Scholar 

  • Slaa EJ, Sánchez LA, Malagodi-Braga KS, Hofstede FE (2006) Stingless bees in applied pollination: practice and perspectives. Apidologie 37:293–315

    Article  Google Scholar 

  • Stout JC, Morales CL (2009) Ecological impacts of invasive alien species on bees. Apidologie 40:388–409

    Article  Google Scholar 

  • Tavares MG, Dias LAD, Borges AA, Lopes DM, Busse AHP, Costa RG, Salomão TMF, Campos LAO (2007) Genetic divergence between populations of the stingless bee uruçu amarela (Melipona rufiventris group, Hymenoptera, Meliponini): is there a new Melipona species in the Brazilian state of Minas Gerais? Gen Mol Biol 30:667–675

    Article  CAS  Google Scholar 

  • Valdovinos-Núñez GR, Quezada-Euán JJG, Ancona-Xiu P, Moo-Valle H, Carmona A, Ruiz Sánchez E (2009) Comparative toxicity of pesticides to stingless bees (Hymenoptera: Apidae: Meliponini). J Econ Entomol 102:1737–1742

    Article  PubMed  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Venturieri GC (2009) The impact of forest exploitation on Amazonian stingless bees (Apidae, Meliponini). Genet Mol Res 8:684–689

    Article  CAS  PubMed  Google Scholar 

  • Yáñez-Ordóñez O, Trujano Ortega A, Llorente Bousquets J (2008) Patrones de distribución de las especies de la tribu Meliponini (Hymenoptera: Apoidea: Apidae) en México. Interciencia 33(1):41–45

    Google Scholar 

  • Zayed A (2009) Bee genetics and conservation. Apidologie 40:237–262

    Article  Google Scholar 

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Acknowledgments

We appreciate the stingless beekeepers and Dr. Remy Vandame that provided samples. We also thank the editor and three anonymous reviewers for their comments which helped improve the manuscript and BiomedRed for English editing. This research has been funded by the Regional Government of Murcia (Fundación Séneca; Grant Number 19908/GERM/2015) and Conacyt (“CONSERVACION DE LAS ABEJAS SIN AGUIJON DE MEXICO” Grant Number 103341). Dr. De la Rúa is presently member and receives support from COST Action FA1307, Sustainable pollination in Europe: joint research on bees and other pollinators, SUPER-B (http://www.cost.eu/COST_Actions/fa/Actions/FA1307).

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    1. Departamento de Zoología y Antropología Física, Facultad de Veterinaria, Universidad de Murcia, 30100, Murcia, Spain

      Miguel Hurtado-Burillo, Laura Jara, Carlos Ruiz & Pilar De la Rúa

    2. Departamento de Apicultura, Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Yucatán, Apdo. 4-116 Itzimná, 97100, Mérida, Yucatán, Mexico

      William de Jesús May-Itzá & José Javier G. Quezada-Euán

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    1. Miguel Hurtado-Burillo
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    Correspondence to Pilar De la Rúa.

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    Miguel Hurtado-Burillo and Laura Jara have contributed equally to this work.

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    Hurtado-Burillo, M., Jara, L., May-Itzá, W. et al. A geometric morphometric and microsatellite analyses of Scaptotrigona mexicana and S. pectoralis (Apidae: Meliponini) sheds light on the biodiversity of Mesoamerican stingless bees. J Insect Conserv 20, 753–763 (2016). https://doi.org/10.1007/s10841-016-9899-1

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