Conservation Genetics

, Volume 18, Issue 3, pp 539–552 | Cite as

Phylogeography and historical demography of the orchid bee Euglossa iopoecila: signs of vicariant events associated to Quaternary climatic changes

  • Wilson Frantine-Silva
  • Douglas C. Giangarelli
  • Rafael E. S. Penha
  • Karen M. Suzuki
  • Enderlei Dec
  • Maria C. Gaglianone
  • Isabel Alves-dos-Santos
  • Silvia H. Sofia
Research Article

Abstract

The aim of this study was to investigate whether Pleistocene climatic instability influenced the phylogeographic structure and historical demography of an endemic Atlantic Forest (AF) orchid bee, Euglossa iopoecila Dressler, which shows two main patterns of integument colors over of its geographical distribution. We based our analysis on the concatenated sequence of four mtDNA segments belonging to genes 16S (357 bp), Cytb (651 bp) and COI (1206 bp), totaling 2234 bp. Samples of E. iopoecila populations were collected in 14 AF remnants along its geographic distribution. Median-Joining haplotype networks, SAMOVA and BAPS results indicated three lineages (southern, central and northern clusters) for E. iopoecila, with two important phylogeographic ruptures. We found higher genetic diversity among samples collected in the central region of the AF, which coincides with predicted areas of climatic stability, according to recent AF stability–extinction model. The demographic analysis suggests that only the southern cluster had undergone recent population expansion, which probably started after the last glacial maximum (LGM). Our data suggest that the differentiation observed in the three mitochondrial lineages of E. iopoecila is the result of past disconnections and multiple extinction/recolonization events involving climate fluctuations. In terms of conservation, we would emphasize the importance of considering: (1) the region of the central clade as the location of the highest genetic diversity of mtDNA of E. iopoecila populations; (2) the philopatric behavior of females that tends to restrict mtDNA gene flow in particular, with direct implications for the conservation of the total genetic diversity in euglossine populations.

Keywords

Euglossa iopoecila Euglossine Mitochondrial markers Genetic structure Orchid bee Bee conservation 

Supplementary material

10592_2016_905_MOESM1_ESM.jpg (277 kb)
Supplementary material 1 (JPEG 277 kb). Figure S1. a) Relationship between the genetic distances measured as FST/(1 − FST) and the logarithm of geographical distance (km); b) genetic distances (FST) and geographic distance (km) between pairs of Euglossa iopoecila samples surveyed across the Brazilian Atlantic Forest. Minimum distance was around 2 km (SP3-SP4) and maximum distance was 2341 km (SC- AL)
10592_2016_905_MOESM2_ESM.docx (14 kb)
Supplementary material 2 (DOCX 14 kb)
10592_2016_905_MOESM3_ESM.docx (22 kb)
Supplementary material 3 (DOCX 22 kb)
10592_2016_905_MOESM4_ESM.docx (57 kb)
Supplementary material 4 (DOCX 56 kb)
10592_2016_905_MOESM5_ESM.docx (17 kb)
Supplementary material 5 (DOCX 15 kb)

References

  1. Amaral FR, Albers PK, Edwards SV, Miyaki CY (2013) Multilocus tests of Pleistocene refugia and ancient divergence in a pair of Atlantic Forest antbirds (Myrmeciza). Mol Ecol 22:3996–4013CrossRefGoogle Scholar
  2. Augusto SC, Garófalo CA (2004) Nesting biology and social structure of Euglossa (Euglossa) townsendi Cockerell (Hymenoptera, Apidae, Euglossini). Insect Soc 51:400–409CrossRefGoogle Scholar
  3. Avise JC (2009) Phylogeography: retrospect and prospect. J Biogeogr 36:3–15CrossRefGoogle Scholar
  4. Batalha-Filho H, Miyaki CY (2016) Late Pleistocene divergence and postglacial expansion in the Brazilian Atlantic Forest: multilocus phylogeography of Rhopias gularis (Aves: Passeriformes). J Zool Syst Evol Res 54:137–147CrossRefGoogle Scholar
  5. Batalha-Filho H, Melo GAR, Waldschmidt AM, Campos LAO, Fernandes-Salomão TM (2009) Geographic distribution and spatial differentiation in the color pattern of abdominal stripes of the Neotropical stingless bee Melipona quadrifasciata (Hymenoptera: Apidae). Zoologia 26:213–219CrossRefGoogle Scholar
  6. 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 41:534–547CrossRefGoogle Scholar
  7. Boff S, Soro A, Paxton RJ, 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. Conserv Genet 15:1123–1135CrossRefGoogle Scholar
  8. Cabanne GS, Santos FR, Miyaki CY (2007) Phylogeography of Xiphorhynchus fuscus (Passeriformes, Dendrocolaptidae): vicariance and recent demographic expansion in southern Atlantic forest. Biol J Linn Soc 91:73–84CrossRefGoogle Scholar
  9. Cabanne GS, Trujillo-Arias N, Calderón L, D’Horta FM, Miyaki CY (2014) Phenotypic evolution of an Atlantic Forest passerine (Xiphorhynchus fuscus): biogeographic and systematic implications. Biol J Linn Soc 113:1047–1066CrossRefGoogle Scholar
  10. Cardoso DC, Cristiano MP, Tavares MG, Schubart CD, Heinze J (2015) Phylogeography of the sand dune ant Mycetophylax simplex along the Brazilian Atlantic Forest coast: remarkably low mtDNA diversity and shallow population structure. BMC Evol Biol 15:106CrossRefPubMedPubMedCentralGoogle Scholar
  11. Carnaval AC, Moritz C (2008) Historical climate modelling predicts patterns of current biodiversity in the Brazilian Atlantic Forest. J Biogeogr 35:1187–1201CrossRefGoogle Scholar
  12. Carnaval AC, Hickerson MJ, Haddad CFB, Rodrigues MT, Moritz C (2009) Stability predicts genetic diversity in the Brazilian Atlantic Forest hotspot. Science 323:785–789CrossRefPubMedGoogle Scholar
  13. Corander J, Tang J (2007) Bayesian analysis of population structure based on linked molecular information. Math Biosci 205:19–31CrossRefPubMedGoogle Scholar
  14. Corander J, Marttinen P, Sirén J, Tang J (2008) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinform 9:539–553CrossRefGoogle Scholar
  15. Dellicour S, Mardulyn P (2014) Spads 1.0: a toolbox to perform spatial analyses on DNA sequence data sets. Mol Ecol Resour 14:647–651CrossRefPubMedGoogle Scholar
  16. Dick CW, Roubik DW, Gruber KF, Bermingham E (2004) Long-distance gene flow and cross-Andean dispersal of lowland rainforest bees (Apidae: Euglossini) revealed by comparative mitochondrial DNA phylogeography. Mol Ecol 13:3775–3785CrossRefPubMedGoogle Scholar
  17. Dodson CH, Dressler RL, Hills HG, Adams RM, Williams NH (1969) Biologically active compounds in orchid fragrances. Science 164:1243–1249CrossRefPubMedGoogle Scholar
  18. Dressler RL (1982) Biology of orchid bees. Annu Rev Ecol Syst 13:373–394CrossRefGoogle Scholar
  19. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214. doi:10.1186/1471-2148-7-214 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581CrossRefPubMedGoogle Scholar
  21. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50Google Scholar
  22. Faria L Jr, Melo G (2007) Species of Euglossa (Glossura) in the Brazilian Atlantic Forest, with taxonomic notes on Euglossa stellfeldi Moure (Hymenoptera, Apidae, Euglossina). Rev Bras Entomol 51:275–284CrossRefGoogle Scholar
  23. Ferrari BR, Melo GAR (2014) Deceiving colors: recognition of color morphs as separate species in orchid bees is not supported by molecular evidence. Apidologie 45:641–652CrossRefGoogle Scholar
  24. Freiria GA, Ruim JB, de Souza RF, Sofia SH (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 43:392–402CrossRefGoogle Scholar
  25. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedPubMedCentralGoogle Scholar
  26. Galindo-Leal C, Câmara IG (2003) Atlantic Forest hotspot status: an overview. In: Galindo-Leal C, Câmara IG (eds) The Atlantic Forest of South America: biodiversity status, threats, and outlook. Center for Applied Biodiversity Science and Island Press, Washington, pp 3–11Google Scholar
  27. Giangarelli DC, Aguiar WM, Sofia SH (2015) Orchid bee (Hymenoptera: Apidae: Euglossini) assemblages from three different threatened phytophysiognomies of the subtropical Brazilian Atlantic Forest. Apidologie 46:71–83CrossRefGoogle Scholar
  28. Haffer J (1969) Speciation in Amazonian forest birds. Science 165:131–137CrossRefPubMedGoogle Scholar
  29. Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci USA 101:14812–14817CrossRefPubMedPubMedCentralGoogle Scholar
  30. Heled J, Drummond AJ (2008) Bayesian inference of population size history from multiple loci. BMC Evol Biol. doi:10.1186/1471-2148-8-289 PubMedPubMedCentralGoogle Scholar
  31. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  32. Ho SY, Shapiro B (2011) Skyline-plot methods for estimating demographic history from nucleotide sequences. Mol Ecol Resour 11:423–434CrossRefPubMedGoogle Scholar
  33. Knowles LL, Alvarado-Serrano DF (2010) Exploring the population genetic consequences of the colonization process with spatio-temporally explicit models: insights from coupled ecological, demographic and genetic models in montane grasshoppers. Mol Ecol 19:3727–3745CrossRefPubMedGoogle Scholar
  34. Laurance WF (2009) Conserving the hottest of the hotspots. Biol Conserv 142:1137CrossRefGoogle Scholar
  35. Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116CrossRefGoogle Scholar
  36. Leite YLR, Costa LP, Loss AC, Rocha RG, Batalha-Filho H, Bastos AC, Quaresma VS, Fagundes V, Paresque R, Passamani M, Pardini R (2016) Neotropical forest expansion during the last glacial period challenges refuge hypothesis. Proc Natl Acad Sci USA 113:1008–1013CrossRefPubMedPubMedCentralGoogle Scholar
  37. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  38. López-Uribe MM, Zamudio KR, Cardoso CF, Danforth BN (2014) Climate, physiological tolerance and sex-biased dispersal shape genetic structure of Neotropical orchid bees. Mol Ecol 23:1874–1890CrossRefPubMedGoogle Scholar
  39. Michener CD (2007) The bees of the world, 2nd edn. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  40. Moritz C (1994) Defining “evolutionarily significant units”. Trends Ecol Evol 9:373–375CrossRefPubMedGoogle Scholar
  41. Moure J, Melo GAR, Faria Jr L (2012) Catalogue of bees (Hymenoptera, Apoidea) in the Neotropical Region-online version. In: Euglossini Latrelli 1802. http://www.moure.cria.org.br/catalogue. Accessed 14 Apr 2016
  42. Myers N, Mittermeier R, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858CrossRefPubMedGoogle Scholar
  43. Nemésio A (2009) Orchid bees (Hymenoptera: Apidae) of the Brazilian Atlantic Forest. Zootaxa 2041:242Google Scholar
  44. Pearson RG, Dawson TP, Liu C (2004) Modelling species distributions in Britain: a hierarchical integration of climate and land-cover data. Ecography 27:285–298CrossRefGoogle Scholar
  45. Penha RES, Gaglianone MC, Almeida FS, Boff S, Sofia SH (2015) Mitochondrial DNA of Euglossa iopoecila (Apidae, Euglossini) reveals two distinct lineages for this orchid bee species endemic to the Atlantic Forest. Apidologie 46:346–358CrossRefGoogle Scholar
  46. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259CrossRefGoogle Scholar
  47. Pokorny T, Loose D, Dyker G, Quezada-Euán JJG, Eltz T (2015) Dispersal ability of male orchid bees and direct evidence for long-range flights. Apidologie 46:224–237CrossRefGoogle Scholar
  48. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256CrossRefPubMedGoogle Scholar
  49. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of akaike information criterion and bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808CrossRefPubMedGoogle Scholar
  50. Quantum GIS Development Team (2009) Quantum GIS geographic information system. Open Source Geospatial Foundation. http://qgis.osgeo.org
  51. Ramalho AV, Gaglianone MC, Oliveira ML (2009) Comunidades de abelhas Euglossina (Hymenoptera, Apidae) em fragmentos de Mata Atlântica no Sudeste do Brasil. Rev Bras Entomol 53:95–101CrossRefGoogle Scholar
  52. Ramírez S, Dressler RL, Ospina M (2002) Abejas euglosinas (Hymenoptera: Apidae) de la Región Neotropical: Listado de especies con notassobre su biología. Biota Colombiana 3:7–118Google Scholar
  53. Ramírez SR, Roubik DW, Skov C, Pierce NE (2010) Phylogeny, diversification patterns and historical biogeography of euglossine orchid bees (Hymenoptera: Apidae). Biol J Linn Soc 100:552–572CrossRefGoogle Scholar
  54. Ramírez-Soriano A, Ramos-Onsins SE, Rozas J, Calafell F, Navarro A (2008) Statistical power analysis of neutrality tests under demographic expansions, contractions and bottlenecks with recombination. Genetics 179:555–567CrossRefPubMedPubMedCentralGoogle Scholar
  55. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100CrossRefPubMedGoogle Scholar
  56. Raymond M, Rousset F (1995) GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249CrossRefGoogle Scholar
  57. Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153CrossRefGoogle Scholar
  58. Ribeiro RA, Lemos-Filho JP, Ramos ACS, Lovato MB (2011) Phylogeography of the endangered rosewood Dalbergia nigra (Fabaceae): insights into the evolutionary history and conservation of the Brazilian Atlantic Forest. Heredity 106:46–57CrossRefPubMedGoogle Scholar
  59. Rocha-Filho LC, Cerântola NCM, Garófalo CA, Imperatriz-Fonseca VL, Del Lama MA (2013) Genetic differentiation of the Euglossini (Hymenoptera, Apidae) populations on a mainland coastal plain and an island in southeastern Brazil. Genetica 74:65–74CrossRefGoogle Scholar
  60. Roubik D, Hanson P (2004) Orchid bees: biology and field guide. InBio Press, HerediaGoogle Scholar
  61. 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 87:651–701CrossRefGoogle Scholar
  62. SOS Mata Atlântica, Instituto Nacional de Pesquisas Espaciais (2015) Atlas dos Remanescentes florestais da Mata Atlântica, período de 2013-2014Google Scholar
  63. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentralGoogle Scholar
  64. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  65. Thomé MTC, Zamudio KR, Giovanelli JGR, Haddad CFB, Baldissera FA Jr, Alexandrino J (2010) Phylogeography of endemic toads and post-Pliocene persistence of the Brazilian Atlantic Forest. Mol Phylogenet Evol 55:1018–1031CrossRefPubMedGoogle Scholar
  66. Van Dike F (2008) Genetic diversity—understanding conservation at genetic levels. In: Van Dike F (ed) Conservation biology: foundations, concepts, applications. Springer, Dordrecht, pp 153–184CrossRefGoogle Scholar
  67. Zimmermann Y, Roubik DW, Quezada-Euan JJG, Paxton RJ, Eltz T (2009) Single mating in orchid bees (Euglossa, Apinae): implications for mate choice and social evolution. Insect Soc 56:241–249CrossRefGoogle Scholar
  68. Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17:2107–2121CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Wilson Frantine-Silva
    • 1
  • Douglas C. Giangarelli
    • 1
  • Rafael E. S. Penha
    • 2
  • Karen M. Suzuki
    • 1
  • Enderlei Dec
    • 3
  • Maria C. Gaglianone
    • 4
  • Isabel Alves-dos-Santos
    • 3
  • Silvia H. Sofia
    • 1
  1. 1.Departamento de Biologia Geral, Centro de Ciências BiológicasUniversidade Estadual de LondrinaLondrinaBrazil
  2. 2.Departamento de Genética, Evolução e Bioagentes, Instituto de BiologiaUniversidade Estadual de CampinasCampinasBrazil
  3. 3.Departamento de Ecologia, Instituto de BiociênciasUniversidade de São PauloSão PauloBrazil
  4. 4.Laboratório de Ciências Ambientais, Programa de Pós-Graduação em Ecologia e Recursos NaturaisUniversidade Estadual do Norte FluminenseCampos dos GoytacazesBrazil

Personalised recommendations