Integrative approach untangles the misconceptions about the range and identity of two stingless bees from the Brazilian semiarid region

References

• Allendorf, F., & Luikart, G. (2007). Conservation and the genetics of populations. Oxford: Blackwell Publishing.
   Google Scholar
• Alves, R. M. O., Carvalho, C. A. L., Waldschmidt, A. M., Paixão, J. F., Souza, B. A., Santos, L. O. F., … Oliveira, M. P. (2016). Melipona mandacaia Smith, (1863) A abelha da Caatinga do Velho Chico. Curitiba: CRV.
   Google Scholar
• Bandelt, H. J., Forster, P., & Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16(1), 37–48. doi:10.1093/oxfordjournals.molbev.a026036
   PubMed Web of Science ®Google Scholar
• Barbosa, A. M. (2015). fuzzySim: Applying fuzzy logic to binary similarity indices in ecology. Methods in Ecology and Evolution, 6(7), 853–858. doi:10.1111/2041-210X.12372
   Web of Science ®Google Scholar
• Batalha-Filho, H., Melo, G. A. R., Waldschmidt, A. M., Campos, L. A. O., & Fernandes-Salmoão, T. M. (2009). Geographic distribution & spatial differentiation in the color pattern of abdominal stripes of the Neotropical stingless bee Melipona quadrifasciata (Hymenoptera: Apidae). Zoologia (Curitiba), 26(2), 213–219. doi:10.1590/S1984-46702009000200003
   Google Scholar
• Batalha-Filho, H., Waldschmidt, A. M., & Alves, R. M. O. (2011). Distribuição potencial da abelha sem ferrão endêmica da Caatinga, Melipona mandacaia (Hymenoptera, Apidae). Magistra, 23(3), 129–133.
   Google Scholar
• Batalha-Filho, H., Waldschmidt, A. M., Campos, L. A. O., Tavares, M. G., & Fernandes-Salomão, T. M. (2010). Phylogeography and historical demography of the Neotropical stingless bee Melipona quadrifasciata (Hymenoptera, Apidae): Incongruence between morphology and mitochondrial DNA. Apidologie, 41(5), 534–547. doi:10.1051/apido/2010001
   Web of Science ®Google Scholar
• Bini, L. M., Diniz-Filho, J. A., Rangel, T. F. L. V. B., Bastos, R. P., & Pinto, M. P. (2006). Challenging Wallacean and Linnean shortfalls: Knowledge gradients and conservation planning in a biodiversity hotspot. Diversity and Distributions, 12(5), 475–482. doi:10.1111/j.1366-9516.2006.00286.x
   Web of Science ®Google Scholar
• Camargo, J. M. F., & Pedro, S. R. M. (2013). Meliponini Lepeletier, 1836. In Moure, J. S., Urban, D., & Melo, G.A.R. (Eds.), Catalogue of bees (hymenoptera, Apoidea) in the Neotropical Region. Retrieved from http://www.moure.cria.org.br/catalogue
   Google Scholar
• Corander, J., & Marttinen, P. (2006). Bayesian identification of admixture events using multi-locus molecular markers. Molecular Ecology, 15(10), 2833–2843. doi:10.1111/j.1365-294X.2006.02994.x
   PubMed Web of Science ®Google Scholar
• Corander, J., Waldmann, P., & Sillanpaa, M. J. (2003). Bayesian analysis of genetic differentiation between populations. Genetics, 163(1), 367–374.
   PubMed Web of Science ®Google Scholar
• Drummond, A. J., & Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 8(7), 214–222. doi:10.1186/1471-2148-7-214
   Web of Science ®Google Scholar
• Frankham, R., Ballou, J. D., & Briscoe, D. A. (2010). Introduction to conservation genetics (2nd ed.). Cambridge: Cambridge University Press.
   Google Scholar
• Fujisawa, T., & Barraclough, T. D. (2013). Delimiting species using single-locus data & the generalized mixed yule coalescent approach: A revised method & evaluation on simulated data sets. Systematic Biology, 62(5), 707–724. doi:10.1093/sysbio/syt033
   PubMed Web of Science ®Google Scholar
• Garcia-Cuenca, A. F., Dumas, Z., & Schwander, T. (2016). Extreme genetic diversity in asexual grass thrips populations. Journal of Evolutionary Biology, 29, 887–899. doi:10.1111/jeb.12843
   PubMed Web of Science ®Google Scholar
• Gibbs, J. (2009). Integrative taxonomy identifies new (and old) species in the Lasioglossum (Dialictus) tegulare (Robertson) species group (Hymenoptera, Halictidae). Zootaxa, 2032(1), 1–38. doi:10.11646/zootaxa.2032.1.1
   Google Scholar
• Gonçalves, J. A. (1973). Ocorrência e Abundância de abelhas indígenas no estado do Céara (Brasil). Boletim da Sociedade Cearense de Agronomia, 14, 1–13.
   Google Scholar
• Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor & analysis program for Windows 95-98 (NT). Nucleic Acids Symposium Series, 41, 95–98.
   Google Scholar
• Hebert, P. D. N., Cywinska, A., Ball, S. L., & Waard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270(1512), 313–321. doi:10.1098/rspb.2002.2218
   PubMed Web of Science ®Google Scholar
• 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, 101(41), 14812–14817.
   PubMed Web of Science ®Google Scholar
• Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25(15), 1965–1978. doi:10.1002/joc.1276
   Web of Science ®Google Scholar
• Hortal, J., Bello, F., Diniz-Filho, J. A., Lewinsohn, T. M., Lobo, J. M., & Ladle, R. J. (2015). Seven shortfalls that beset large-scale knowledge of biodiversity. Annual Review of Ecology, Evolution, and Systematics, 46(1), 523–549. doi:10.1146/annurev-ecolsys-112414-054400
   Web of Science ®Google Scholar
• Huelsenbeck, J. P., & Ronquist, F. (2001). MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics, 17(8), 754–755. doi:10.1093/bioinformatics/17.8.754
   PubMed Web of Science ®Google Scholar
• Iftikhar, R., Ashfaq, M., Rasool, A., & Hebert, P. D. N. (2016). DNA barcode analysis of thrips (Thysanoptera) diversity in Pakistan reveals cryptic species complexes. PLoS One, 11(1), e0146014–21. doi:10.1371/journal.pone.0146014
   PubMed Web of Science ®Google Scholar
• Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16(2), 111–120. doi:10.1007/BF01731581
   PubMed Web of Science ®Google Scholar
• Landaverde-González, P., Moo-Valle, H., Murray, T. E., Paxton, R. J., Quezada-Euán, J. J. G., & Huseman, M. (2017). Sympatric lineage divergence in cryptic Neotropical sweat bees (Hymenoptera: Halictidae: Lasioglossum). Organisms Diversity & Evolution, 17(1), 251–265. doi:10.1007/s13127-016-0307-1
   Web of Science ®Google Scholar
• Lepeletier, A. L. M. (1836). Histoire Naturelle des Insectes-Hyménoptéres. Paris: Librairie Encyclopédique de Roret.
   Google Scholar
• Librado, P., & Rozas, J. (2009). DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25(11), 1451–1452. doi:10.1093/bioinformatics/btp187
   PubMed Web of Science ®Google Scholar
• Lomolino, M. V. (2004). Conservation biogeography. In Frontiers of biogeography: New directions in the geography of nature. Sunderland: Sinauer.
   Google Scholar
• Lynch, M., & Walsh, B. (1998). Genetics and analysis of quantitative traits Sunderland. The American Journal of Human Genetics, 68(2), 548–549.
   Google Scholar
• Machado, C. A., Jousselin, E., Kjellberg, F., Compton, S. G., & Herre, E. A. (2001). Phylogenetic relationships, historical biogeography and character evolution of g-pollinating wasps. Proceedings of the Royal Society of London. Series B: Biological Sciences, 268(1468), 685–694. doi:10.1098/rspb.2000.1418
   PubMed Web of Science ®Google Scholar
• Miranda, E. A., Batalha-Filho, H., Congrains, C., Carvalho, A. F., Ferreira, K. M., & Del Lama, M. A. (2016). Phylogeography of Partamona rustica (Hymenoptera, Apidae), an endemic stingless bee from the Neotropical dry forest diagonal. PLoS One, 11(10), e0164441–19. doi:10.1371/journal.pone.0164441
   PubMed Web of Science ®Google Scholar
• Monaghan, M. T., Wild, R., Elliot, M., Fujisawa, T., Balke, M., Inward, D. J. G., … Vogler, A. P. (2009). Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Systematic Biology, 58(3), 298–311. doi:10.1093/sysbio/syp027
   PubMed Web of Science ®Google Scholar
• Moreau, C. S., Bell, C. D., Vila, R., Archibald, S. B., & Pierce, N. E. (2006). Phylogeny of the ants: Diversification in the age of angiosperms. Science, 312(5770), 101–104. doi:10.1126/science.1124891
   PubMed Web of Science ®Google Scholar
• Muñoz, I., Dall′Olio, R., Lodesani, M., & De la Rúa, P. (2014). Estimating introgression in Apis mellifera siciliana populations: Are the conservation islands really effective? Insect Conservation and Diversity, 7(6), 563–571. doi:10.1111/icad.12092
   Web of Science ®Google Scholar
• Murray, J. T., Fitzpatrick, U., Brown, M. J. F., & Paxton, R. (2008). Cryptic species diversity in a widespread bumble bee complex revealed using mitochondrial DNA RFLPs. Conservation Genetics, 9(3), 653–666. doi:10.1007/s10592-007-9394-z
   Web of Science ®Google Scholar
• Okita, K. M., Sato, T., Kato, K., Hosada, A., Terayma, M., & Masuko, K. (2013). The spatial distribution of mtDNA and phylogeographic analysis of the ant Cardiocondyla kagutsuchi (Hymenoptera: Formicidae) in Japan. Sociobiolgy, 60(2), 129–134.
   Web of Science ®Google Scholar
• Posada, D. (2008). jModelTest: Phylogenetic model selection & averaging. Molecular Biology and Evolution, 25(7), 1253–1256. doi:10.1093/molbev/msn083
   PubMed Web of Science ®Google Scholar
• Pradhan, V., Kamble, Y., Ladniya, V., & Mogul, M. (2017). A overview of species identification by DNA barcoding. International Journal of Current Microbiology and Applied Sciences, 4(4), 127–140.
   Google Scholar
• R Development Core Team. (2009). R: A language and environment for statistical computing. R Vienna: Foundation for Statistical Computing. Retrieved from http://www.R-project.org
   Google Scholar
• Rambaut, A., & Drummond, A. J. (2009). Tracer (Version 1.5). Retrieved from http://tree.bio.ed.ac.uk/software/TRACER
   Google Scholar
• Rambaut, A., & Drummond, A. J. (2015). TreeAnnotator (v1.8.4). Institute of Evolutionary Biology, University of Edinburgh. Retrieved from http://beast.bio.ed.ac.uk/
   Google Scholar
• Reid, N., & Carstens, B. (2012). Phylogenetic estimation error can decrease the accuracy of species delimitation: A Bayesian implementation of the general mixed Yule-coalescent model. BMC Evolutionary Biology, 12(1), 196. doi:10.1186/1471-2148-12-196
   PubMedGoogle Scholar
• Reino, L., Ferreira, M., Martínez-Solano, I., Segurado, P., Xu, C., & Barbosa, A. M. (2016). Favourable areas for co-occurrence of parapatric species: Niche conservatism and niche divergence in Iberian tree frogs and midwife toads. Journal of Biogeography, 44(1), 1–11. doi:10.1111/jbi.12850
   Web of Science ®Google Scholar
• Saitou, N., & Nei, M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4(4), 406–425. doi:10.1093/oxfordjournals.molbev.a040454
   PubMed Web of Science ®Google Scholar
• Schwarz, H. F. (1932). The genus Melipona the type genus of the Meliponidae or stingless bees. Bulletin of the American Museum of Natural History, 63(4), 231–460.
   Google Scholar
• Silveira, F. A., Melo, G. A. R., & Almeida, E. A. B. (2002). Abelhas Brasileiras: Sistemática e Identificação. Belo Horizonte: IDMA.
   Google Scholar
• Smith, F. (1863). Descriptions of Brazilian honey bees belonging to the Genera Melipona and Trigona, which were exhibited, together with samples of their honey and wax, in the Brazilian court of the international exhibition of 1862. Transactions of the Royal Entomological Society of London, 11(6), 497–512. doi:10.1111/j.1365-2311.1863.tb01298.x
   Google Scholar
• Stamatakis, A. (2014). RAxML version 8: A tool for phylogenetic analysis and post-analysis of lage phylogenies. Bioinformatics, 30(9), 1312–1313. doi:10.1093/bioinformatics/btu033
   PubMed Web of Science ®Google Scholar
• Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30(12), 2725–2729. doi:10.1093/molbev/mst197
   PubMed Web of Science ®Google Scholar
• Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research, 22(22), 4673–4680. doi:10.1093/nar/22.22.4673
   PubMed Web of Science ®Google Scholar
• Tyagi, K., Kumar, V., Singha, D., Chandra, K., Laskar, B. A., Kundu, S., … Chatterjee, S. (2017). DNA barcoding studies on Thrips in India: Cryptic species and species complexes. Nature, 7(4898), 1–14.
   Google Scholar
• Waldschmidt, A. M., Fernandes-Salomão, T. M., Barros, E. G., & Campos, L. A. O. (1997). Extraction of genomic DNA from Melipona quadrifasciata (Hymenoptera: Apidae, Meliponinae). Brazilian Journal of Genetics, 20(3), 421–423. doi:10.1590/S0100-84551997000300011
   Web of Science ®Google Scholar
• Waldschmidt, A. M., Marco-Júnior, P., Barros, E. G., & Campos, L. A. O. (2002). Genetic analysis of Melipona quadrifasciata Lep. (Hymanoptera: Apidae, Meliponini) with RAPD markers. Brazilian Journal of Biology, 62(4B), 923–928. doi:10.1590/S1519-69842002000500022
   PubMedGoogle Scholar
• Waldschmidt, M., Barros, E. G., & Campos, L. A. O. (2000). A molecular marker distinguishes the subspecies Melipona quadrifasciata quadrifasciata and Melipona quadrifasciata anthidioides (Hymenoptera, Apidae, Meliponini). Genetics and Molecular Biology, 23(3), 609–611. doi:10.1590/S1415-47572000000300019
   Web of Science ®Google Scholar
• Warren, D. L., Glor, R. E., & Turelli, M. (2008). Environmental niche equivalency versus conservatism: Quantitative approaches to niche evolution. Evolution, 62(11), 2868–2883. doi:10.1111/j.1558-5646.2008.00482.x
   PubMed Web of Science ®Google Scholar
• Williams, P. H., Brown, M. J. F., Carolan, J. C., An, J., Goulson, D., Aytekin, A. M., … Xie, Z. (2012). Unveiling cryptic species of the bumblebee subgenus Bombus s. str. worldwide with COI barcodes (Hymenoptera: Apidae). Systematics and Biodiversity, 10(1), 21–56. doi:10.1080/14772000.2012.664574
   Web of Science ®Google Scholar
• Zayed, A. (2009). Bees genetics and conservation. Apidologie, 40(3), 237–262. doi:10.1051/apido/2009026
   Web of Science ®Google Scholar
• Zayed, A., & Packer, L. (2005). Complementary sex determination substantially increases extinction proneness of haplodiploid populations. Proceedings of the National Academy of Sciences, 102(30), 10742–10746. doi:10.1073/pnas.0502271102
   PubMed Web of Science ®Google Scholar