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Issue: Vol. 4353 No. 3: 24 Nov. 2017
Type: Article
Published: 2017-11-24
DOI: 10.11646/zootaxa.4353.3.4
Page range: 467–484
Abstract views: 112
PDF downloaded: 63

Description of two new species closely related to Doryctobracon areolatus (Szépligeti, 1911) (Hymenoptera, Braconidae), based on morphometric and molecular analyses

Departamento de Entomologia e Acarologia, ESALQ, Universidade de São Paulo (USP), Caixa Postal 9, 13418-900, Piracicaba, SP.
Departamento de Entomologia e Acarologia, ESALQ, Universidade de São Paulo (USP), Caixa Postal 9, 13418-900, Piracicaba, SP.
Universidade Federal de São Carlos UFSCAR, Caixa Postal 676, CEP 13565-905, São Carlos, SP
Departamento de Entomologia e Acarologia, ESALQ, Universidade de São Paulo (USP), Caixa Postal 9, 13418-900, Piracicaba, SP.
Hymenoptera geometric morphometry canonical variate analysis ITS2 28S-D2 rDNA molecular taxonomy

Abstract

This study clarifies the identity of two morphs that appear similar but not identical to the braconid wasp Doryctobracon areolatus (Szépligeti), by analyses of fore wing morphometry and the ITS2 and D2 region of 28S ribosomal DNA. Wing measurements of D. areolatus and the two morphs, one with a yellow stigma and one with a brown stigma, from several Brazilian localities, were taken and subjected to geometric morphometry. Evaluation of 20 anatomical points on the fore wing by means of multivariate analysis revealed that these morphs consistently differ from D. areolatus. Intraspecific size variation in both molecular markers (ITS2 and 28S-D2 rDNA) was also detected among populations of D. areolatus from the states of Amapá, São Paulo, Goiás, and Tocantins, but no such difference was observed among samples of the two morphs. However, high sequence variability was observed for both markers among D. areolatus and these morphs. Morphometric analysis yielded similar results and produced dendrogram congruent with those based on the molecular markers, also indicating that D. areolatus corresponds to a complex of cryptic species. Therefore, our morphometric and molecular data, in addition to revealing that D. areolatus includes cryptic species, showed that the unidentified morphs actually represent two distinct, previously undescribed species of Doryctobracon. These new taxa are formally described herein, as D. whartoni sp. nov. and D. adaimei sp. nov.

 

References

  1. Adaime, R., Nascimento, D.B., Deus, E.G., Souza, G.D. & Oliveira, L.P.S. (2007) Hospedeiros e parasitóides de Anastrepha spp. (Diptera: Tephritidae) em Itaubal do Piririm, Estado do Amapá, Brasil. Ciência Rural, 37, 557–560.
    https://doi.org/10.1590/S0103-84782007000200041

    Aljanabi, S.M. & Martinez, I. (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research, 25, 4692–4693.
    https://doi.org/10.1093/nar/25.22.4692

    Baylac, M., Villemant, C. & Simbolotti, G. (2003) Combining geometric morphometrics with pattern recognition for the investigation of species complexes. Biological Journal of the Linnean Society, 80, 89–98.
    https://doi.org/10.1046/j.1095-8312.2003.00221.x

    Belshaw, R. & Quicke, D.L.J. (1997) A molecular phylogeny of the Aphidiinae (Hymenoptera: Braconidae). Molecular Phylogenetics and Evolution, 7, 281–293.
    https://doi.org/10.1006/mpev.1996.0400

    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 and Evolution, 22, 148–155.
    https://doi.org/10.1016/j.tree.2006.11.004

    Billah, M.K., Kimani-Njogu, S.W., Wharton, R.A., Wooley, J.B. & Masiga, D. (2008) Comparison of five allopatric fruit fly parasitoid population (Psyttalia species) (Hymenoptera: Braconidae) from coffee fields using morphometric and molecular methods. Bulletin of Entomological Research, 98, 63–75.
    https://doi.org/10.1017/S000748530700541X

    Bomfim, D.A., Uchôa-Fernandes, M.A. & Bragança, M.A.L. (2007) Hosts and Parasitoids of Fruit Flies (Diptera: Tephritoidea) in the State of Tocantins, Brazil. Neotropical Entomology, 36, 984–986.
    https://doi.org/10.1590/S1519-566X2007000600025

    Braga Filho, J.R., Veloso, W.R.S., Naves, R.V. & Ferreira, G.A. (2001) Entomofauna associada aos frutos do bacupari, Salacia crassifolia (Mart.) Peyr, nos cerrados do Brasil central. Pesquisa Agropecuária Tropical, 31, 47–54.

    Canal Daza, N.A. & Zucchi, R.A. (2000) Parasitóides - Braconidae. In: Malavasi, A. & Zucchi, R.A. Moscas-das-frutas de importância econômica no Brasil. Conhecimento básico e aplicado, Holos-FAPESP Press, Ribeirão Preto, SP, pp. 119–126.

    Ciociola Jr., A.I., Querino, R.B., Zucchi, R.A. & Stouthamer, R. (2001) Molecular tool for identification of closely related species of Trichogramma (Hymenoptera: Trichogrammatidae): T. rojasi Nagajara & Nagarkatti and T. lasallei Pinto. Neotropical Entomology, 30, 575–578.
    https://doi.org/10.1590/S1519-566X2001000400010

    Costa Lima, A. (1937) Vespa do gênero Opius, parasitas de larvas de moscas-das-frutas (Hymenoptera: Braconidae). O Campo, 8, 22–32.

    Deus, E.G. & Adaime, R. (2013) Dez anos de pesquisas sobre moscas-das-frutas (Diptera: Tephritidae) no estado do Amapá: avanços obtidos e desafios futuros. Biota Amazônia, 3, 157–168.
    https://doi.org/10.18561/2179-5746/biotaamazonia.v3n3p157-168

    Deus, E.G., Adaime, R., Nascimento, D.B., Marinho, C.F. & Zucchi, R.A. (2010) Hospedeiros e parasitóides de espécies de Anastrepha (Diptera, Tephritidae) em dois municípios do Estado do Amapá. Revista de Agricultura, 84, 194–203.

    Eitam, T.H., Sivinski, J. & Aluja, M. (2003) Use of Host Fruit Chemical Cues for Laboratory Rearing of Doryctobracon areolatus (Hymenoptera: Braconidae), a Parasitoid of Anastrepha spp. (Diptera: Tephritidae) Avi. The Florida Entomologist, 86, 211–216.
    https://doi.org/10.1653/0015-4040(2003)086[0211:UOHFCC]2.0.CO;2

    Fouly, H.M., Wilkinson, H.T. & Chen, W. (1997) Restriction analysis of internal transcribe spacers and the small subunit gene of ribosomal DNA among four Gaeumannomyces species. Mycologia, 89, 590–597.
    https://doi.org/10.2307/3760996

    Gallego, D. & Galián, J. (2001) The internal transcribed spacers (ITS1 and ITS2) of the rDNA differentiates the bark beetles forest pests Tomicus destruens and T. piniperda. Insect Molecular Biology, 10, 415–420.
    https://doi.org/10.1046/j.0962-1075.2001.00279.x

    Greene, E. (1989) A diet-induced developmental polymorphism in a caterpillar. Science, 243, 643–646.
    https://doi.org/10.1126/science.243.4891.643

    Jesus, C.R., Pereira, J.D.B., Oliveira, M.N., Silva, R.A., Souza Filho, M.F., Costa Neto, S.V., Marinho, C.F. & Zucchi, R.A. (2008) New records of fruit flies (Diptera: Tephritidae), wild hosts and parasitoids (Hymenoptera: Braconidae) in the Brazilian Amazon. Neotropical Entomology, 37, 733–734.
    https://doi.org/10.1590/S1519-566X2008000600017

    Jesus, C.R., Adaime, R., Oliveira, M.N., Silva, W.R., Costa Neto, S.V. & Souza Filho, M.F. (2012) Anastrepha (Diptera: Tephritidae) species, their hosts and parasitoids (Hymenoptera: Braconidae) in five municipalities of the state of Amapá, Brazil. The Florida Entomologist, 95, 694–705.
    https://doi.org/10.1653/024.095.0320

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

    Lenormand, T. (2002) Gene flow and the limits to natural selection. Trends in Ecology & Evolution, 17, 183–372.
    https://doi.org/10.1016/S0169-5347(02)02497-7

    Leon, J.H., Logarzo, G.A. & Triapitsyn, S.V. (2006) Preliminary evidence from reproductive compatibility studies suggests that Gonatocerus tuberculifemur as a cryptic species complex, or a new species identified: development and utility of molecular diagnostic markers. In: Pierce’s Disease Research Symposium. San Diego, California, pp. 44–47.

    Leonel Junior, F.L., Zucchi, R.A. & Canal Daza, N.A. (1996) Parasitismo de moscas-das-frutas (Diptera: Tephritidae) por Braconidae (Hymenoptera) em duas localidades do Estado de São Paulo. Anais da Sociedade Entomológica do Brasil, 25, 199–206.

    Monteiro, L.R. & Reis, S.F. (1999) Princípios de morfometria geométrica. Holos Editora, Ribeirão Preto, SP, 188 pp.

    Moraes, D.A. (2003) A Morfometria Geométrica e a “Revolução na Morfometria”: localizando mudanças na forma dos organismos URL. Available from: https://www.ufpe.br/mastozoologia/images/documentos/astua_de_moraes_2003_morfo
    metria_geometrica.pdf (accessed 29 March 2012)

    Mound, L.A. (2005) Fighting, flight and fecundity: Behavioural determinants of Thysanoptera structural diversity. In: Ananthakrishnan, T.N. & Whitman, D.W. (Eds.), Insects and Phenotypic Plasticity. Science Publishers Inc., Enfield, NH, pp. 81–105.

    Müller, T., Philippi, N., Dandekar, T., Schultz, J. & Wolf, M. (2007) Distinguishing species. RNA 13, 1469–1472.
    https://doi.org/10.1261/rna.617107

    Murillo, F.D., Cabrera-Mireles H., Barrera, J.F., Liedo, P. & Montoya, P. (2015) Doryctobracon areolatus (Hymenoptera, Braconidae) a parasitoid of early developmental stages of Anastrepha obliqua (Diptera, Tephritidae). Journal of Hymenoptera Research, 46, 91–105.
    https://doi.org/10.3897/JHR.46.5586

    Nunes, A.M., Nava, D.E., Müller F.A., Gonçalves, R.S. & Garcia, M.S. (2011) Biology and parasitic potential of Doryctobracon areolatus on Anastrepha fraterculus larvae. Pesquisa Agropecuária Brasileira, 46, 669–671.
    https://doi.org/10.1590/S0100-204X2011000600014

    Ovruski, S.M. (2003) Nuevos aportes a la taxonomía de las especies de Opiinae (Hymenoptera: Braconidae), parasitoides de Anastrepha fraterculus (Wiedemann) (Diptera: Tephritidae) en la provincia de Tucumán, Argentina. Acta Zoológica Lilloana, 47, 15–44.

    Parra, J.R.P., Botelho, P.S.M., Correa-Ferreira, B.S. & Bento, J.M.S. (2002) Controle biológico no Brasil: parasitóides e predadores. Manole Press, São Paulo, SP, 609 pp.

    Pigliucci, M. (2001) Phenotypic plasticity. In: Fox, C.W., Roff, D.A. & Fairbairn, D.J. Evolutionary Ecology: Concepts and Case Studies. Oxford University Press, New York, NY, pp. 58–69.

    Porter, C.H. & Collins, F.H. (1991) Species-diagnostic differences in a ribosomal DNA Internal Transcribe Spacer from the sibling species Anopheles freeborni and Anopheles hermsi (Diptera: Culicidae). The American Journal of Tropical Medicine and Hygiene, 45, 271–279.
    https://doi.org/10.4269/ajtmh.1991.45.271

    Rohlf, F.J. (2004) tpsDig Version 1.40. Department of Ecology and Evolution, Stony Brook University, Stone Brook, New York.

    Rohlf, F.J. (2007) tpsRewl Version 1.45. Department of Ecology and Evolution, Stony Brook University. Stony Brook, New York.

    Schlichting, C.D. & Pigliucci, M. (1998) Phenotypic Evolution: A Reaction Norm Perspective. Sinauer Associates Press, Sunderland, MA, 387 pp.

    Sharkey, M.J. & Wharton, R.A. (1997) Morphology and Terminology. In: Wharton, R.A., Marsh, P.M. & Shakey, M.J. (Eds.), Manual of the New World Genera of the Family Braconidae (Hymenoptera), Special Publication of the International Society of Hymenopterists. Vol. l. Allen Press, New York, pp. 19–37.

    Silva, I.M.M.S., Honda, J., Van Kan, F., Hu, J., Neto, L., Pintureau, B. & Stouthamer, R. (1999) Molecular differentiation of five Trichogramma species occurring in Portugal. Biological Control, 16, 177–184.
    https://doi.org/10.1006/bcon.1999.0755

    Silva, W.R. & Adaime, R. (2007) Levantamento de moscas-das-frutas e de seus parasitóides no município de Ferreira Gomes, Estado do Amapá. Ciência Rural 37, 265–268.
    https://doi.org/10.1590/S0103-84782007000100043

    Silva, R.A., R., Lima, A.L., Xavier, S.L.O., Silva, W.R., Marinho, C.F. & Zucchi, R.A. (2011) Anastrepha species (Diptera: Tephritidae), their hosts and parasitoids in southern Amapá State, Brazil. Biota Neotropica, 11, 431–436.
    https://doi.org/10.1590/S1676-06032011000300037

    Stouthamer, R., Jochemsen, P., Platner, G. & Pinto, J.D. (2000) Crossing incompatibility between Trichogramma minutum and T. platneri (Hymenoptera: Trichogrammatidae): Implications for application in biological control. Environmental Entomology, 29, 832–837.
    https://doi.org/10.1603/0046-225X-29.4.832

    Stouthamer, R., Rugman-Jones, P., Thu, P.Q., Eskalen, A., Thibault, T., Hulcr, J. Wang, L.-J, Jordal, B.H., Chen, C.-Y., Cooperband, M., Lin, C.-S., Kamata, N., Lu, S.-S., Masuya, H., Mendel, Z., Rabaglia, R., Sanguansub, S., Shinh, H.-H., Sittichaya, W. & Zong, S. (2017) Tracing the origin of a cryptic invader: phylogeography of the Euwallacea fornicates (Coleoptera: Curculionidae: Scolytinae) species complex. Agricultural and Forest Entomology.
    https://doi.org/10.1111/afe.12215

    Slatkin, M. (1973) Gene flow and selection in a cline. Genetics, 75, 733–756.

    Szépligeti, G. (1911) Zwei neue Braconiden aus Brasilien. Bollettino del Laboratorio di Zoologia Generale e Agraria della R. Scuola Superiore d'Agricoltura in Portici, 5, 285–286.

    Taylor, D.B., Moon, R., Gibson, G. & Szalanski, A. (2006) Genetic and morphological comparisons of new and world populations of Spalangia Species (Hymenoptera: Pteromalidade). Annals of the Entomological Society of America, 99, 799–808.
    https://doi.org/10.1603/0013-8746(2006)99[799:GAMCON]2.0.CO;2

    Uvarov, B. (1966) Grasshoppers and Locusts. Vol. I. Cambridge University Press, Cambridge, pp.

    Veloso, V.R.S., Ferreira, G.A., Fernandes, P.M., Canal Daza, N.A. & Zucchi, R.A. (1996) Ocorrência e índice de infestação de Anastrepha spp. (Dip., Tephritidae) em Pouteria gardneriana Radlk. e Pouteria ramiflora (Mart.) Radlk. (Sapotaceae), nos cerrados de Goiás. Anais das escolas de agronomia e veterinaria, 26, 109–120.

    Viereck, H.L. (1911) Descriptions of six new genera and thirty-one new species of Ichneumon flies. Proceedings of the United States National Museum, 40, 173–196.
    https://doi.org/10.5479/si.00963801.1812.173

    Villemant, C., Simbolotti, G. & Kenis, M. (2007) Discrimination of Eubazus (Hymenoptera, Braconidae) sibling species using geometric morphometrics analysis of wing venation. Systematic Entomology, 32, 625–634.
    https://doi.org/10.1111/j.1365-3113.2007.00389.x

    Walker, A.K. & Wharton, R.A. (2011) A review of New World Eurytenes s. str. (Hymenoptera, Braconidae, Opiinae). Journal of Hymenoptera Research, 20, 23–46.
    https://doi.org/10.3897/jhr.29.877

    Weekers, P.H.H., De Jonckheere, J.F. & Dumont, H. (2001) Phylogenetic relationships inferred from Ribosomal ITS Sequences and Biogeographic patterns in Representatives of the genus Calopteryx (Insecta: Odonata) of the West Mediterranean and adjacent West European Zone. Molecular Phylogenetics and Evolution, 20, 88–99.
    https://doi.org/10.1006/mpev.2001.0947

    Wharton, R.A. (1997a) Subfamily Opiinae. In: Wharton, R.A., Marsh, P.M. & Sharkey, M.J. (Eds.), Manual of the New World Genera of the Family Braconidae (Hymenoptera). Allen Press, Lawrence, KS, pp. 379–390.

    Wharton, R.A. (1997b) Generic relationships of Opiinae Braconidae (Hymenoptera) parasitic on fruit-infesting Tephritidae (Diptera). Contributions of the American Entomological Institute, Ann Arbor, 30, 1–53.

    Whitman, D.W. & Agrawal, A.A. (2009) What is phenotypic plasticity and why is it important? In: Whitman, D.W. & Ananthakrishnan, T.N. (Eds.), Phenotypic Plasticity of Insects: Mechanisms and Consequences. Science Publishers, Enfield, NH, pp. 1–63.
    https://doi.org/10.1201/b10201-2

    Yoder, M.J., Mikó, I., Seltmann, K., Bertone, M.A. & Deans, A.R. (2010) A gross anatomy ontology for Hymenoptera. PLos ONE, 5 (12), e15991.

    https://doi.org/10.1371/journal.pone.0015991

    Zucchi, R.A. (2002) A taxonomia e o controle biológico de pragas. In: Parra, J.P., Botelho, P.S., Corrêa-Ferreira, B.S. & Bento, J.M.S. (Eds.), Controle Biológico no Brasil: Parasitóides e predadores. Manole Press, São Paulo, SP, pp. 17–24.

    Zucchi, R.A., Marinho, C.F. & Adaime, R. (2011) First record of the fruit fly parasitoid Doryctobracon crawfordi (Viereck) (Hymenoptera: Braconidae) in Brazil. Neotropical Entomology, 40, 711–712.
    https://doi.org/10.1590/S1519-566X2011000600014