Abstract
The orchid bees includes many species whose integument color is predominantly metallic, in particular those from the genus Euglossa. In the Atlantic Forest, some species exhibit color variation that seems to be linked with their distribution, with warmer colors (green, with coppery and reddish tones) in lower latitudes and cooler colors (blue, with purple shades) in higher latitudes. Contrasting taxonomic interpretations of this color variation lead to the recognition of distinct species for the different color morphs. In all three case studies investigated in this work (Euglossa iopoecila, Euglossa stellfeldi, and Euglossa townsendi), the different forms were sampled throughout their distribution. Thirty samples from 16 different localities were used, which had their DNA extracted, amplified, and sequenced for fragments of the genes cytochrome b (cytb) and cytochrome C oxidase subunit 1 (CO1). A concatenated data matrix, totaling 1,089 bp, was submitted for Bayesian and maximum likelihood analyses. The resulting phylogenetic trees, together with the estimated genetic distances between samples, led to the conclusion that the different color morphs in all the three case studies do not represent separate species, but only integumental color variations of their respective species.
Similar content being viewed by others
References
Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402
Cameron, S.A., Mardulyn, P. (2001) Multiple molecular data sets suggest independent origins of highly eusocial behavior in bees (Hymenoptera: Apinae). Syst. Biol. 50(2), 194–214
Cha, S.Y., Yoon, H.J., Lee, E.M., Yoon, M.H., Hwang, J.S., Jin, B.R., Han, Y.S., Kim, I. (2007) The complete nucleotide sequence and gene organization of the mitochondrial genome of the bumblebee, Bombus ignitus (Hymenoptera: Apidae). Gene 392(1–2), 206–220
Crozier, R.H., Crozier, Y.C. (1993) The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Genetics 133, 97–117
Darveau, C.A., Hochachka, P.W., Welch Jr., K.C., Roubik, D.W., Suarez, R.K. (2005) Allometric scaling of flight energetics in Panamanian orchid bees: a comparative phylogenetic approach. J. Exp. Biol. 208(PT 18), 3581–3591
Dick, C.W., Roubik, D.W., Gruber, K.F., 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, 3775–3785
Dodson, C.H., Dressler, R.L., Hills, H.G., Adams, R.M., Williams, N.H. (1969) Biologically active compounds in orchid fragrances. Science 164, 1243–1249
Dressler, R.L. (1982a) New species of Euglossa II. (Hymenoptera: Apidae). Rev. Biol. Trop. 30, 121–129
Dressler, R.L. (1982b) New species of Euglossa. IV. The cordata and purpurea species groups (Hymenoptera: Apidae). Rev. Biol. Trop. 30(2), 141–150
Eltz, T., Fritzsch, F., Pech, J.R., Zimmermann, Y., Ramírez, S.R., Quezada-Euan, J.J.G., Bembé, B. (2011) Characterization of the orchid bee Euglossa viridissima (Apidae: Euglossini) and a novel cryptic sibling species, by morphological, chemical, and genetic characters. Zool. J. Linn. Soc. 163, 1064 –1076
Faria, L.R.R., Melo, G.A.R. (2007) Species of Euglossa (Glossura) in the Brazilian Atlantic forest, with taxonomic notes on Euglossa stellfeldi Moure (Hymenoptera: Apidae: Euglossina). Rev. Bras. Entomol. 51, 275–284
Folmer, O., Black, M., Hoeh, W., Lutz, R., Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotech. 3, 294–297
Hebert, P.D.N., Cywinska, A., Ball, S.L., deWaard, J.R. (2003) Biological identifications through DNA barcodes. Proc. R. Soc. Lond. B. 270, 313–321
Hong, M.Y., Cha, S.Y., Kim, D.Y., Yoon, H.J., Kim, S.R., Hwang, J.S., Kim, K.-G., Han, Y.S., Kim, I. (2008) Presence of several tRNA-like sequences in the mitochondrial genome of the bumblebee, Bombus hypocrita sapporoensis (Hymenoptera: Apidae). Genes Genom. 30(4), 307–318
Katoh, K., Misawa, K., Kuma, K., Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066
Koulianos, S., Schmid-Hempel, R., Roubik, D.W., Schmid-Hempel, P. (1999) Phylogenetic relationships within the corbiculate Apinae (Hymenoptera) and the evolution of eusociality. J. Evol. Biol. 12(2), 380–384
Meier, R., Zhang, G., Ali, F. (2008) The use of mean instead of smallest interspecific distances exaggerates the size of the “barcoding gap” and leads to misidentification. Syst. Biol. 57(5), 809–813
Meyer, C.P., Paulay, G. (2005) DNA barcoding: Error rates based on comprehensive sampling. PLoS Biol. 3, 2229–2238
Miller, M.A., Pfeiffer, W., and Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees, in: Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, pp. 1–8.
Nemésio, A. (2006) Euglossa anodorhynchi sp. n. (Hymenoptera: Apidae), a new orchid bee from southern Brazil. Syst. Entomol. 35(2), 206–209
Nemésio, A. (2009) Orchid bees (Hymenoptera: Apidae) of the Brazilian Atlantic Forest. Zootaxa 2041, 1–242
Ramirez, S.R., Roubik, D.W., Skov, C., Pierce, N.E. (2010) Phylogeny, diversification patterns and historical biogeography of euglossine orchid bees (Hymenoptera: Apidae). Biol. J. Linn. Soc. Lond. 100(3), 552–572
Rebêlo, J.M.M., Moure, J.S. (1996) As espécies de Euglossa Latreille do nordeste de São Paulo (Apidae, Euglossinae). Rev. Bras. Zool. 12, 445–466
Ronquist, F., Huelsenbeck, J.P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A., Huelsenbeck, J.P. (2012) MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space. Syst. Biol. 61(3), 539–542
Silvestre, D., Dowton, M., Arias, M.C. (2008) The mitochondrial genome of the stingless bee Melipona bicolor (Hymenoptera, Apidae, Meliponini): Sequence, gene organization and a unique tRNA translocation event conserved across the tribe Meliponini. Genet. Mol. Biol. 31, 451–460
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 PCR primers. Ann. Entomol. Soc. Am. 87, 651–701
Stamatakis, A., Hoover, P., Rougemont, J. (2008) A Rapid Bootstrap Algorithm for the RAxML Web-Servers. Syst. Biol. 75(5), 758–771
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
Tan, H.W., Liu, G.H., Dong, X., Lin, R.Q., Song, H.Q., Huang, S.Y., Yuan, Z.G., Zhao, G.H., Zhu, X.Q. (2011) The complete mitochondrial genome of the Asiatic cavity-nesting honeybee Apis cerana (Hymenoptera: Apidae). PLoS ONE 6(8), E23008
Acknowledgments
We would like to thank Thomas Eltz for providing the specimens of E. townsendi from Mexico, Marcos Barbeitos for his help with the maximum likelihood analysis, and Kevin A. Williams for his suggestions to an earlier version of the manuscript. GARM thanks Vitor Becker for granting access and for helping during the collection trip to RPPN Serra Bonita and Marco A. Costa for his help during collection trips to Bahia. ICMBio is thanked for the collecting permits and CNPq for financial support (grant 304053/2012-0).
Author information
Authors and Affiliations
Corresponding author
Additional information
Manuscript editor: Marina Meixner
Couleurs trompeuses: la reconnaissance de morphes différant par la couleur comme des espèces séparées chez les abeilles à orchidées n’a pas de fondement moléculaire
Forêt atlantique / Brésil / Euglossini / ADN mitochondrial / taxonomie moléculaire
Trügerische Farben: die Anerkennung von Prachtbienen-Farbmorphen als getrennte Arten wird durch molekulare Daten nicht unterstützt
Atlantischer Wald / Euglossini / mitochondriale DNA / molekulare Taxonomie
Rights and permissions
About this article
Cite this article
Ferrari, B.R., Melo, G.A.R. Deceiving colors: recognition of color morphs as separate species in orchid bees is not supported by molecular evidence. Apidologie 45, 641–652 (2014). https://doi.org/10.1007/s13592-014-0280-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13592-014-0280-7