Two Colors, One Species: The Case of Melissodes nigroaenea (Apidae: Eucerini), an Important Pollinator of Cotton Fields in Brazil

Carolina Grando, Nolan David Amon, Steven J Clough, Na Guo, Wei Wei, Patricia Azevedo, Margarita Maria López-Uribe, Maria Imaculada Zucchi

Abstract


Accurate taxonomic delimitation in ecological research is absolutely critical as studies that seek to evaluate levels of biodiversity and qualify human effects on the environment are rapidly undertaken. Coloration is a widely used morphological character for species identification through dichotomous keys. However, taxonomic identification based upon coloration is often unreliable because this character can exhibit high degree of intraspecific variation. In this study, we use a DNA barcoding approach to investigate the interpretation of two color morphs (yellow or dark) in the eucerine bee Melissodes nigroaenea. Our hypothesis is that if significant genetic divergence exists between each morphotype of M. nigroaenea, coloration reflects two distinct evolutionary lineages within this species, which may require taxonomic revision. Our alternative hypothesis is that, if genetic divergence is low between each morphotype of M. nigroaenea, we can attribute this variation to color polymorphism. Our Bayesian phylogenetic reconstruction revealed that both yellow and black individuals clustered together in a highly supported phylogenetic group. Additionally, pairwise genetic distances between M. nigroaenea color morphotypes were lower than 3%. These results indicate that both mesosome color morphs correspond to intraspecific variability within the same evolutionary unit. Together, our results indicate that mesosome coloration is not a reliable character for taxonomic differentiation of these Melissodes species, and that the incorporation of DNA barcoding approaches to taxonomic classification can help resolve some of the problems that originate while relying on purely morphological taxonomy.

Keywords


Cytochrome oxidase I, Bayesian phylogeny, bees, barcoding gap.

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References


Arribas, P., Abellán, P., Velasco, J., Bilton, D.T., Millán, A. & Sánchez-Fernández, D. (2012). Evaluating drivers of vulnerability to climate change: a guide for insect conservation strategies. Global Change Biology 18: 2135–2146. doi: 10.1111/j.1365-2486.2012.02691.x

Ascher, J.S. & Pickering, J. 2017. Discover Live bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila). http://www.discoverlife.org/mp/20q?search=Apoidea (accessed date: 18 April 2018)

Abrapa (2017). A cadeia do algodão brasileiro: safra 2016/2017. Associação Brasileira dos Produtores de Algodão, 248 p

Austen, G.E., Bindemann, M., Griffiths, R.A. & Roberts, D.L. (2016). Species identification by experts and non-experts: comparing images from field guides. Scientific Reports 6, p. 33634. doi: 10.1038/srep33634

Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K.K. & Das, I. (2007). Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution 22: 148–155. doi: 10.1016/j.tree.2006.11.004

Boyce, T.M., Zwick, M.E. & Aquadro, C.F. (1989). Mitochondrial DNA in the bark weevils: size, structure and heteroplasmy. Genetics 123: 825–836.

Čandek, K. & Kuntner, M. (2015). DNA barcoding gap: reliable species identification over morphological and geographical scales. Molecular Ecology Resources 15: 268–277. doi: 10.1111/1755-0998.12304

Cardoso, C.F., Silveira, F.A., Oliveira, G.M., Cavéchia, L.A., Almeida, J.P.S., Nakasu, E.Y.T., Sujii, E.R., Fontes, E.M.G., Pires, C.S.S. (2007). Principais polinizadores de Gossypium hirsutum latifolium cv. Delta Opal (Malvaceae), em uma localidade do Distrito Federal, Brasil. Boletim de Pesquisa e Desenvolvimento 212. Brasília: Embrapa Recursos Genéticos e Biotecnologia.

Carolan, J.C., Murray, T.E., Fitzpatrick, Ú., Crossley, J., Schmidt, H., Cederberg, B., McNally, L., Paxton, R.J., Williams, P.H. & Brown, M.J.F. (2012). Colour patterns do not diagnose species: quantitative evaluation of a DNA barcoded cryptic bumblebee complex. Plos One 7(1), p. e29251. doi: 10.1371/journal.pone.0029251

Colla S, Richardson L. & Williams P. 2011. Bumble bees of the eastern United States. https://www.fs.fed.us/wildflowers/pollinators/documents/BumbleBeeGuideEast2011.pdf. (accessed date: 24 April, 2018)

Dorchin, A., López-Uribe, M.M., Praz, C.J., Griswold, T. & Danforth, B.N. (2018). Phylogeny, new generic-level classification, and historical biogeography of the Eucera complex (Hymenoptera: Apidae). Molecular Phylogenetics and Evolution 119: 81–92. doi: 10.1016/j.ympev.2017.10.007

Duennes, M.A., Petranek, C., de Bonilla, E.P.D., Mérida-Rivas, J., Martinez-López, O., Sagot, P., Vandame, R. & Cameron, S.A. (2017). Population genetics and geometric morphometrics of the Bombus ephippiatus species complex with implications for its use as a commercial pollinator. Conservation Genetics 18: 553–572. doi: 10.1007/s10592-016-0903-9

Ferrari, B.R. & Melo, G.A.R. (2014). Deceiving colors: recognition of color morphs as separate species in orchid bees is not supported by molecular evidence. Apidologie 45: 641–652. doi: 10.1007/s13592-014-0280-7

Folmer, Black, Hoeh, Lutz & Vrijenhoek (1994). DNA primers for amplification of mitochondrial cytochrome c. Molecular Marine Biology and Biotechnology 3: 294-299

Freitas, F.V., Santos Júnior, J.E., Santos, F.R. & Silveira, F.A. (2018). Species delimitation and sex associations in the bee genus Thygater, with the aid of molecular data, and the description of a new species. Apidologie 1-13. doi: 10.1007/s13592-018-0576-0

Garzón-Orduña, I.J., Brower, A.V.Z., Kamilari, M., Iribar, A. & Murienne, J. (2018). Cracking the Code: Examination of Species Delimitations amongHamadryas Butterflies with DNA Barcodes Suggests Caribbean Cracker is Hamadryas februa Hübner (Nymphalidae: Biblidinae). Journal of the Lepidopterists’ Society 72: 53–73. doi: 10.18473/lepi.72i1.a6

Grella, M.D., Savino, A.G., Paulo, D.F., Mendes, F.M., Azeredo-Espin, A.M.L., Queiroz, M.M.C., Thyssen, P.J. & Linhares, A.X. (2015). Phenotypic polymorphism of Chrysomya albiceps (Wiedemann) (Diptera: Calliphoridae) may lead to species misidentification. Acta Tropica 141: 60–72. doi: 10.1016/j.actatropica.2014.09.011

Hajibabaei, M., Singer, G.A.C., Hebert, P.D.N. & Hickey, D.A. (2007). DNA barcoding: how it complements taxonomy, molecular phylogenetics and population genetics. Trends in Genetics 23: 167–172. doi: 10.1016/j.tig.2007.02.001

Hebert, P.D.N., Cywinska, A., Ball, S.L. & deWaard, J.R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society Biological Sciences 270: 313–321. doi: 10.1098/rspb.2002.2218

Hebert, P.D.N., Penton, E.H., Burns, J.M., Janzen, D.H. & Hallwachs, W. (2004). Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America 101: 14812–14817. doi: 10.1073/pnas.0406166101

Hebert, P.D.N., Ratnasingham, S., Zakharov, E.V., Telfer, A.C., Levesque-Beaudin, V., Milton, M.A., Pedersen, S., Jannetta, P. & deWaard, J.R. (2016). Counting animal species with DNA barcodes: Canadian insects. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 371(1702). doi: 10.1098/rstb.2015.0333

Hill, G.E. (2016). Mitonuclear coevolution as the genesis of speciation and the mitochondrial DNA barcode gap. Ecology and Evolution 6: 5831–5842. doi: 10.1002/ece3.2338

Hines, H.M. & Williams, P.H. (2012). Mimetic colour pattern evolution in the highly polymorphicBombus trifasciatus (Hymenoptera: Apidae) species complex and its comimics. Zoological journal of the Linnean Society 166: 805–826. doi: 10.1111/j.1096-3642.2012.00861.x

Hines, H.M., Witkowski, P., Wilson, J.S. & Wakamatsu, K. (2017). Melanic variation underlies aposematic color variation in two hymenopteran mimicry systems. Plos One 12: e0182135. doi: 10.1371/journal.pone.0182135

Huang, J., Wu, J., An, J. & Williams, P.H. (2015). Newly discovered colour-pattern polymorphism of Bombus koreanus females (Hymenoptera: Apidae) demonstrated by DNA barcoding. Apidologie 46: 250–261. doi: 10.1007/s13592-014-0319-9

Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A. (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649. doi: 10.1093/bioinformatics/bts199

Kumar, S., Stecher, G. and Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33: 1870–1874. doi: 10.1093/molbev/msw054

Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. and Calcott, B. (2017). Partitionfinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34: 772–773. doi: 10.1093/molbev/msw260

Lecocq, T., Dellicour, S., Michez, D., Dehon, M., Dewulf, A., De Meulemeester, T., Brasero, N., Valterová, I., Rasplus, J.-Y. and Rasmont, P. 2015. Methods for species delimitation in bumblebees (Hymenoptera, Apidae,Bombus ): towards an integrative approach. Zoologica scripta 44: 281–297. doi: 10.1111/zsc.12107

McKay, B.D., Mays, H.L., Yao, C.-T., Wan, D., Higuchi, H. and Nishiumi, I. 2014. Incorporating color into integrative taxonomy: analysis of the varied tit (Sittiparus varius) complex in East Asia. Systematic Biology 63: 505–517. doi: 10.1093/sysbio/syu016

Michener, C.D. (2007). The bees of the world. Baltimore: Johns Hopkins University Press, 992 p

Miyanaga, R., Maeta, Y. & Sakagami, S.F. (1999). Geographical variation of sociality and size-linked color patterns in Lasioglossum (Evylaeus) apristum (Vachal) in Japan (Hymenoptera, Halictidae). Insectes sociaux 46: 224–232. doi: 10.1007/s000400050138

Nemésio, A. (2009). Orchid bees (Hymenoptera: Apidae) of the Brazilian Atlantic Forest. Zootaxa 2041: Magnolia Press, 242 p

Packer, L., Monckton, S.K., Onuferko, T.M. & Ferrari, R.R. (2018).

Validating taxonomic identifications in entomological research. Insect Conservation and Diversity 11: 1–12. doi: 10.1111/icad.12284

Packer, L. & Ruz, L. (2017). DNA barcoding the bees (Hymenoptera: Apoidea) of Chile: species discovery in a reasonably well know bee fauna with the description of a new species of Lonchopria (Colletidae). Genome 60: 414–430. doi: 10.1139/gen-2016-0071

Padial, J.M., Miralles, A., De la Riva, I. & Vences, M. (2010). The integrative future of taxonomy. Frontiers in Zoology 7:16. doi: 10.1186/1742-9994-7-16

Rodrílguez, F.P., Sarmiento, C.E. & González-Soriano, E. (2015). Morphological variability and evaluation of taxonomic characters in the genus Erythemis Hagen, 1861 (Odonata: Libellulidae: Sympetrinae). Insecta Mundi 0428: 1-68. Center for Systematic Entomology, Inc.

Ronquist, F. & Huelsenbeck, J.P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. doi: 10.1093/bioinformatics/btg180

Sheffield, C.S., Hebert, P.D.N., Kevan, P.G. & Packer, L. (2009).

DNA barcoding a regional bee (Hymenoptera: Apoidea) fauna and its potential for ecological studies. Molecular Ecology Resources 9 Suppl s1:196–207. doi: 10.1111/j.1755-0998.2009.02645.x.

Sigovini, M., Keppel, E. & Tagliapietra, D. (2016). Open Nomenclature in the biodiversity era. Methods in Ecology and Evolution 7: 1217–1225. doi: 10.1111/2041-210X.12594

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. Annals of the Entomological Society of America 87: 651–701.

Terrell, E.E. (1963). Symbols and terms for morphological intergradation and hybridization. Taxon 12: 105–108.

Urban, D. (1973). As espécies sulamericanas do gênero Melissodes (Latreille, 1829) (Hymenoptera: Apoidea). Revista Brasileira de Biologia 33: 201-220.

Uy, J.A.C., Moyle, R.G., Filardi, C.E. & Cheviron, Z.A. (2009). Difference in plumage color used in species recognition between incipient species is linked to a single amino acid substitution in the melanocortin-1 receptor. The American Naturalist 174: 244–254. doi: 10.1086/600084

Vodă, R., Dapporto, L., Dincă, V. & Vila, R. (2015). Cryptic matters: overlooked species generate most butterfly beta-diversity. Ecography 38: 405–409. doi: 10.1111/ecog.00762

White, T.E. & Kemp, D.J. (2016). Colour polymorphism. Current Biology 26: R517–R518. doi: 10.1016/j.cub.2016.03.017

Wheeler, Q. D., & N. I. Platnick. (2000). The phylogenetic species concept (sensu Wheeler and Platnick). In Q. D. Wheeler & R. Meier (Eds.), Species concepts and phylogenetic theory: A debate. New York: Columbia University Press.




DOI: http://dx.doi.org/10.13102/sociobiology.v65i4.3464

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