Skip to main content

Advertisement

SpringerLink
Log in

Evidence of at least two evolutionary lineages in Melipona subnitida (Apidae, Meliponini) suggested by mtDNA variability and geometric morphometrics of forewings

  • Original Paper
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

Melipona subnitida, a tropical stingless bee, is an endemic species of the Brazilian northeast and exhibits great potential for honey and pollen production in addition to its role as one of the main pollinators of the Caatinga biome. To understand the genetic structure and better assist in the conservation of this species, we characterized the population variability of M. subnitida using geometric morphometrics of the forewing and cytochrome c oxidase I gene fragment sequencing. We collected workers from six localities in the northernmost distribution. Both methodologies indicated that the variability among the sampled populations is related both to the environment in which samples were collected and the geographical distance between the sampling sites, indicating that differentiation among the populations is due to the existence of at least evolutionary lineages. Molecular clock data suggest that this differentiation may have begun in the middle Pleistocene, approximately 396 kya. The conservation of all evolutionary lineages is important since they can present differential resistance to environmental changes, as resistance to drought and diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ab’Saber AN (1977) Espaços ocupados pela expansão dos climas secos da América do Sul, por ocasião dos períodos glaciais quaternários. Paleoclimas 3:1–19

    Google Scholar 

  • Almeida FC, Bonvicino CR, Cordeiro-Estrela P (2007) Phylogeny and temporal diversification of Calomys (Rodentia, Sigmodontinae): implications for the biogeography of an endemic genus of the open/dry biomes of South America. Mol Phylog Evol 42:449–466. doi:10.1016/j.ympev.2006.07.005

    Article  CAS  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 bees. Apidologie 37:259–274. doi:10.1051/apido:2006021

    Article  CAS  Google Scholar 

  • Assis AF (2010) Estudo populacional e molecular de Nannotrigona testaceicornis Cockerell (Hymenoptera, Apidae, Meliponini) através do DNA mitocondrial. Dissertation, University of São Paulo

  • Auler AS, Wang X, Edwards RL, Cheng H, Cristalli PS, Smart PL, Richards DA (2004) Quaternary ecological and geomorphic changes associated with rainfall events in presently semi-arid northeastern Brazil. J Quat Sci 19:693–701

    Article  Google Scholar 

  • Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific Phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Ann Rev Ecolog Syst 18:489–522

    Google Scholar 

  • Batalha-Filho H, Waldschmidt AM, Campos LAO, Tavares MG, Fernandes-Salomão TM (2010) Phylogeography and historical demography of the neotropical stingless bee Melipona quadrifasciata (Hymenoptera, Apidae): incongruence between morphology and mitochondrial DNA. Apidologie 41:534–547

    Article  CAS  Google Scholar 

  • Behling H, Arz HW, Patzold J, Wefer G (2000) Late Quaternary vegetational and climate dynamics in northeastern Brazil, inferences from marine core GeoB 3104-1. Quat Sci Rev 19:981–994

    Article  Google Scholar 

  • Bischoff I, Schröder S, Misof B (2009) Differentiation and range expansion of North American squash bee, peponapis pruinosa (Apidae: Apiformes) populations assessed by geometric wing morphometry. Ann Entomol Soc Am 102:60–69. doi:10.1603/008.102.0106

    Article  Google Scholar 

  • Breuker CJ, Patterson JS, Klingenberg CP (2006) A single basis for developmental buffering of Drosophila wing shape. PLoS ONE 1:e7

    Article  PubMed Central  PubMed  Google Scholar 

  • Breuker CJ, Brakefield PM, Gibbs M (2007) The association between wing morphology and dispersal is sex-specific in the glanville fritillary butterfly Melitaea cinxia (Lepidoptera: Nymphalidae). Eur J Entomol 104:445–452

    Article  Google Scholar 

  • Brito RM, Arias MC (2005) Mitochondrial DNA characterization of two Partamona species (Hymenoptera, Apidae, Meliponini) by PCR + RFLP and sequencing. Apidologie 36:431–438

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Bruening PH (1990) Abelha Jandaíra. Coleção Mossoroense, Mossoró

    Google Scholar 

  • Camargo JMF, Pedro SRM (2013). Meliponini Lepeletier, 1836. In Moure JS, Urban D, Melo GAR (Eds). Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region - online version. Available at http://www.moure.cria.org.br/catalogue. Accessed 27 Dec 2013

  • Carnaval AC, Bates JM (2007) Amphibian DNA shows marked genetic structure and tracks pleistocene climate change in Northeastern Brazil. Evol 61:2942–2957

    Article  CAS  Google Scholar 

  • Cortopassi-Laurino M, Imperatriz-Fonseca VL (2001) La cria de abejas sin aguijon mas comunes em el Nordeste Brasilero. II Seminario Mexicano Sobre Abejas Sin Aguijón - una visión sobre su biología y cultivo, Mérida, pp 40–43

    Google Scholar 

  • Costa C, Büchler R, Berg S et al (2012) Results of the Europe-wide genotype – environment interactions experiment. 8th COLOSS Conference/MC meeting. International meeting of the COLOSS network providing an update on losses and the factors involved, Halle, pp 24–25

    Google Scholar 

  • Cruz DO, Freitas BM, Silva LA, Silva EMS, Bomfim IGA (2004) Adaptação e comportamento de pastejo da abelha jandaíra (Melipona subnitida Ducke) em ambiente protegido. Acta Sci 26:293–298. doi:10.4025/actascianimsci.v26i3.1777

    Google Scholar 

  • Danforth BN, Sipes S, Fang J, Brady SG (2006) The history of early bee diversification based on five genes plus morphology. Proc Natl Acad Sci U S A 103:15118–15123

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192

    Article  CAS  PubMed  Google Scholar 

  • Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2011) Geneious v5.4. http://www.geneious.com

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

    Article  PubMed  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genet 131:479–491

    CAS  Google Scholar 

  • Francisco FDO, Arias MC (2009) Inferences of evolutionary and ecological events that influenced the population structure of Plebeia remota, a stingless bee from Brazil. Apidologie 41:216–224

    Article  Google Scholar 

  • Francisco FDO, 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). Insect Soc 55:231–237. doi:10.1007/s00040-008-0992-7

    Article  Google Scholar 

  • Franco FF, Manfrin MH (2013) Recent demographic history of cactophilic Drosophila species can be related to Quaternary palaeoclimatic changes in South America. J Biogeogr 40:142–154. doi:10.1111/j.1365-2699.2012.02777.x

    Article  Google Scholar 

  • Francoy TM, Imperatriz-Fonseca VL (2010) A Morfometria geométrica de asas e a identificação automática de espécies de abelhas. Oecologia Australis 14:317–321

    Article  Google Scholar 

  • Francoy TM, Grassi ML, Imperatriz-Fonseca VL, Jesús May-Itzá W, 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. doi:10.1007/s13592-011-0013-0

    Article  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. doi:10.1051/apido/2009012

    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

  • Hedrick PW (1999) Genetics of Populations, 2nd edn. Jones and Bartlett Publishers, Sudbury

    Google Scholar 

  • Kalinowski ST (2009) How well do evolutionary trees describe genetic relationships among populations? Hered 102:506–513. doi:10.1038/hdy.2008.136

    Article  CAS  Google Scholar 

  • Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proceedings. Proc R Soc B 274:303–313. doi:10.1098/rspb.2006.3721

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinform 25:1451–1452

    Article  CAS  Google Scholar 

  • Lopes MTR, Silva JO, Pereira FM, Camargo RCR, Vieira Neto JM, Ribeiro VQ (2007) Atividade de vôo de abelhas jandaíra (Melípona subnitida Ducke, 1910) instaladas em dois modelos de colméia. http://www.cpamn.embrapa.br/publicacoes/new/boletins/bpd_pdf/boletim_72.PDF. Accessed 20 June 2011

  • Marinho IV, Freitas MF,César F, Zanella V, Caldas AL (2002) Espécies vegetais da Caatinga utilizadas pelas abelhas indígenas sem ferrão como fonte de recursos e local de nidificação. http://www.prac.ufpb.br/anais/Icbeu_anais/anais/meioambiente/ferrao.pdf. Accessed 6 May 2011

  • Martins CF, Cortopassi-Laurino M, Koedam D, Imperatriz-Fonseca VL (2004) Espécies arbóreas utilizadas para nidificação por abelhas sem ferrão na Caatinga (Seridó, PB; João Câmara, RN). Biota Neotrop 4:1–8

    Article  Google Scholar 

  • Mata LJ, Campos M (2001) Latin America. In: McCarthy JJ, Canziani OF, Leary NA, Dokken DJ, White KS (eds) Climate change 2001: Impacts, adaptations and vulnerability. Cambridge University Press, Cambridge, pp 693–734

    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 

  • Miller MP (1997) Tools for population genetic analyses (TFPGA): A windows program for the anasylis of allozyme and molecular population genetic data. Computer software distributed by author

  • Moritz C, Dowling TE, Brown WM (1987) Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Ann Rev Ecol Syst 18:269–292

    Article  Google Scholar 

  • Murray TE, Fitzpatrick U, Brown MJF, Paxton RJ (2007) Cryptic species diversity in a widespread bumble bee complex revealed using mitochondrial DNA RFLPs. Conserv Genet 9:653–666

    Article  Google Scholar 

  • Nogueira-Neto P (1954) Notas bionômicas sobre Meliponineos III – Sôbre a enxameagem (Hym. Apoidea). Rio de Janeiro - Brasil, pp 419-452

  • Pennington RT, Prado DE, Pendry CA (2000) Neotropical seasonally dry forests and Quaternary vegetation changes. J Biogeogr 27:261–273

    Article  Google Scholar 

  • Polzin T (2003) On Steiner trees and minimum spanning trees in hypergraphs. Oper Res Lett 31:12–20

    Article  Google Scholar 

  • Rêgo M, Albuquerque P (2006) Redescoberta de Melipona subnitida Ducke (Hymenoptera: Apidae) nas Restingas do Parque Nacional dos Lençóis Maranhenses, Barreirinhas, MA. Neotrop Entomol 35:416–417

    Article  PubMed  Google Scholar 

  • Resende HC, Yotoko KSC, Delabie JHC, Costa MA, Campiolo S, Tavares MG, Campos LAO, Fernandes-Salomão TM (2010) Pliocene and Pleistocene events shaping the genetic diversity within the central corridor of the Brazilian Atlantic Forest. Biol J Linn Soc 101:949–960. doi:10.1111/j.1095-8312.2010.01534.x

    Article  Google Scholar 

  • Rohlf FJ (2008) tpsDig. Departament of Ecology and Evolution. State University of New York, New York

    Google Scholar 

  • Silva JF, Fariñas MR, Felfili JM, Klink CA (2006) Spatial heterogeneity, land use and conservation in the Cerrado region of Brazil. J Biogeogr 33:536–548

    Article  Google Scholar 

  • Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:651–701

    CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  Google Scholar 

  • Trovão DMBM, Souza BC, Carvalho ECD, Oliveira PTB, Ferreira LMR (2009) Espécies vegetais da caatinga associadas às comunidades de abelhas (Hymenoptera: Apoidea : Apiformis). Caatinga (Mossoró, Brasil) 22:136–143

    Google Scholar 

  • Turchetto-Zolet AC, Pinheiro F, Salgueiro F, Palma-Silva C (2013) Phylogeographical patterns shed light on evolutionary process in South America. Mol Ecol 22:1193–1213. doi:10.1111/mec.12164

    Article  CAS  PubMed  Google Scholar 

  • Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTech 10:506–513

    CAS  Google Scholar 

  • Wappler T, De Meulemeester T, Aytekin AM, Michez D, Engel MS (2012) Geometric morphometric analysis of a new Miocene bumble bee from the Randeck Maar of southwestern Germany (Hymenoptera: Apidae). Syst Entomol 37:784–792. doi:10.1111/j.1365-3113.2012.00642.x

    Article  Google Scholar 

  • Wüster W, Ferguson JE, Quijada-Mascareñas JA, Pook CE, Salomão MG, Thorpe RS (2005) Tracing an invasion: landbridges, refugia, and the phylogeography of the Neotropical rattlesnake (Serpentes: Viperidae: Crotalus durissus). Mol Ecol 14:1095–1108

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo à Pesquisa do Estado de São Paulo (2011/07857-9 to TMF), Programa de Pós-graduação em Diversidade Biológica e Conservação (CCTS, UFSCar) and Research Support Nucleus BioComp for financial support. Flávio de Oliveira Francisco, Maria Cristina Arias, and Rodrigo Pires Dallacqua are appreciated for their assistance with the molecular experiments. Vera Lucia Imperatriz Fonseca, Carlos Henrique Lobo, and Rafael Cabral Santos Borges are appreciated for sample collection.

Author information

Authors and Affiliations

  1. Departamento de Genética, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Av. Bandeirantes, 3900, 14049-900, Ribeirão Preto, SP, Brazil

    Vanessa Bonatti

  2. Departamento de Biologia, Faculdade de Filosofia Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Av. Bandeirantes, 3900, 14040-901, Ribeirão Preto, SP, Brazil

    Zilá Luz Paulino Simões

  3. Departamento de Biologia, Centro de Ciências e Tecnologias para a Sustentabilidade, Universidade Federal de São Carlos, Rod. João Leme dos Santos, Km 110, 18052-780, Sorocaba, SP, Brazil

    Fernando Faria Franco

  4. Escola de Artes, Ciências e Humanidades, Universidade de São Paulo, Rua Arlindo Béttio, 1000, 03828-000, São Paulo, SP, Brazil

    Tiago Mauricio Francoy

Authors
  1. Vanessa Bonatti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zilá Luz Paulino Simões
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fernando Faria Franco
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tiago Mauricio Francoy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tiago Mauricio Francoy.

Additional information

Communicated by: Sven Thatje

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 16.9 kb)

ESM 2

(DOCX 17.0 kb)

ESM 3

(DOCX 90.2 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bonatti, V., Simões, Z.L.P., Franco, F.F. et al. 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 (2014). https://doi.org/10.1007/s00114-013-1123-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-013-1123-5

Keywords

Search

Navigation