Abstract
The tribe Holcobraconini (Braconidae: Doryctinae) is a group of parasitoid wasps mainly found in the tropical and subtropical regions of the world. It contains seven genera (Holcobracon Cameron, Ivondrovia Shenefelt & Marsh, Liodoryctes Szépligeti, Monarea Szépligeti, Nervellius Roman, Odontobracon Cameron and Zombrus Marshall), most of which are characterized by having the m-cu vein of the hind wing long and strongly curved towards the apex of wing. Some studies, however, found that three doryctine genera that lack the above feature (Binarea Brullé, Liobracon Szépligeti and Odontodoryctes Granger) might be closely related to holcobraconines. Here, we reconstructed the phylogenetic relationships among species of six holcobraconine genera and the three putative closely related genera using four gene markers and estimated the times of origin and diversification within the tribe. The holcobraconine genera were intermingled in a clade with the above three genera. Liobracon and Zombrus were not recovered as monophyletic. Acanthodoryctes Turner, Antidoryctes Belokobylskij & Quicke and Priosphys Enderlein were also included within the Holcobraconini based on morphology. Based on molecular evidence and on morphological examination of the genera involved, Holcobraconini is proposed to comprise 13 genera for which we include morphological diagnoses. The origin of the tribe probably occurred during the late Palaeocene to mid Eocene, 44.43 to 58.15 Mya. At least two main dispersal events from the Ethiopian to the other biogeographic regions could have led to the current geographic distribution of the Holcobraconini associated with the global increase of temperature during the Late Palaeocene to Middle Eocene.
Similar content being viewed by others
References
Bains, S., Corfield, R. M., & Norris, R. D. (1999). Mechanisms of climate warming at the end of the Paleocene. Science, 285, 724–727.
Belokobylskij, S. A. (1992). On the classification and phylogeny of the braconid wasps of subfamilies Doryctinae and Exothecinae (Hymenoptera, Braconidae). Part I. On the classification, 1. Entomologicheskoe Obozrenie, 71(4), 900–928 (In Russian). English translation Entomological Review, 72, 109–137.
Belokobylskij, S. A., & Quicke, D. L. J. (2000). Seven new genera of the subfamily Doryctinae (Hymenoptera: Braconidae) from the Old World. Journal of Hymenoptera Research, 9, 111–141.
Belokobylskij, S. A., & Samartsev, K. G. (2011). First records of the tribe Holcobraconini and the genus Zombrus Marshall, 1897 (Hymenoptera: Braconidae: Doryctinae) in Europe. Zoosystematica Rossica, 20, 310–318.
Belokobylskij, S. A., Zaldivar-Riverón, A., & Quicke, D. L. J. (2004). Phylogeny of the parasitic wasp genera of the subfamily Doryctinae (Hymenoptera: Braconidae) from morphological evidence. Zoological Journal of the Linnean Society, 142, 369–404.
Belokobylskij, S. A., Zaldívar-Riverón, A., & Coronado-Blanco, J. M. (2014). Phylogenetic affinities of Monarea Szépligeti, 1904 (Hymenoptera: Braconidae, Doryctinae), with description of a new species from Mexico. Zootaxa, 3795, 421–430.
Belokobylskij, S. A., Zaldívar-Riverón, A., & Castaneda-Osorio, R. (2018). Revision of the Afrotropical genus Ivondrovia Shenefelt & Marsh, 1976 with description of a new species (Hymenoptera: Braconidae: Doryctinae). ZooKeys, 747, 87–100.
Braet, Y. (2014). A new Neotropical species of the doryctine wasp tribe Holcobraconini (Hymenoptera: Braconidae), and new records of additional genera. Bulletin de la Société Royale Belge d’Entomologie, 150, 56–65.
Cameron, P. (1887). Hymenoptera. In F. D. Godman & O. Salvin, Biologia Centrali-Americana; or, Contributions to the knowledge of the fauna and flora of Mexico and Central America. Zoology, 1, 329–422, 471–472.
Ceccarelli, F. S., Sharkey, M. J., & Zaldívar-Riverón, A. (2012). Species identification in the taxonomically neglected, highly diverse, neotropical parasitoid wasp genus Notiospathius (Braconidae: Doryctinae) based on an integrative molecular and morphological approach. Molecular Phylogenetics and Evolution, 62, 485–495.
Currano, E. D., Kattler, K. R., & Flynn, A. (2011). Paleogene insect herbivory as a proxy for pCO2 and ecosystem stress in the Bighorn Basin, Wyoming, USA. Berichte der Geologischen Bundes-Anstalt, 85, 61.
Dowton, M., Belshaw, R., Austin, A. D., & Quicke, D. L. J. (2002). Simultaneous molecular and morphological analysis of braconid relationships (Insecta: Hymenoptera: Braconidae) indicates independent mt-tRNA gene inversions within a single wasp family. Journal of Molecular Evolution, 54, 210–226.
Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969–1973.
Gillespie, J. J., Yoder, M. J., & Wharton, R. A. (2005). Predicted secondary structure for 28S and 18S rRNA from Ichneumonoidea (Insecta: Hymenoptera: Apocrita): Impact on sequence alignment and phylogeny estimation. Journal of Molecular Evolution, 61, 114–137.
Gingerich, P. D. (2006). Environment and evolution through the Paleocene–Eocene thermal maximum. Trends in Ecology and Evolution, 21, 246–253.
Hebert, P. D. N., Cywinska, A., Ball, S. L., & De Waard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society London B: Biological Sciences, 270, 313–321.
Jardine, P. (2011). The Paleocene-Eocene thermal maximum. Palaeontology Online, 1, 1–7.
Kass, R. E., & Raftery, A. E. (1995). Bayes factors. Journal of the American Statistical Association, 90, 773–795.
Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780.
Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T., & Calcott, B. (2016). PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34, 772–773.
Long, K. D., van Achterberg, C., & Hoa, D. T. (2018). New record of the genus Zombrus Marshall, 1897 (Hymenoptera: Braconidae: Doryctinae), with description of three new species from Vietnam. Zootaxa, 4420, 279–291.
Marsh, P. M. (1988). Revision of the tribe Odontobraconini in the Western Hemisphere (Hymenoptera: Braconidae: Doryctinae). Systematic Entomology, 13, 443–464.
Marsh, P. M. (2002). The Doryctinae of Costa Rica (excluding the genus Heterospilus). Memoirs of the American Entomological Institute, 70, 1–216.
McInerney, F. A., & Wing, S. L. (2011). The Paleocene-Eocene thermal maximum: a perturbation of carbon cycle, climate, and biosphere with implications for the future. Annual Review of Earth and Planetary Sciences, 39, 489–516.
McLoughlin, S. (2001). The breakup history of Gondwana and its impact on pre-Cenozoic floristic provincialism. Australian Journal of Botany, 49, 271–300.
Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE) (pp. 1–8).
Morrone, J. J. (2015). Biogeographical regionalisation of the world: a reappraisal. Australian Systematic Botany, 28, 81–90.
Piel, W. H., Chan, L., Dominus, M. J., Ruan, J., Vos, R. A., & Tannen, V. (2009). TreeBASE v. 2: a database of phylogenetic knowledge. London: e-BioSphere 2009.
Quicke, D. L. J., & Belshaw, R. (1999). Incongruence between morphological data sets: an example from the evolution of endoparasitism among parasitic wasps (Hymenoptera: Braconidae). Systematic Biology, 48, 436–454.
Quicke, D. L. J., Tunstead, J., Falco, J. V., & Marsh, P. M. (1992). Venom gland and reservoir morphology in the Doryctinae and related braconid wasps (Insecta, Hymenoptera, Braconidae). Zoologica Scripta, 21, 403–416.
Rahman, M. H., Fitton, M. G., & Quicke, D. L. J. (1998). Ovipositor internal microsculpture and other features in doryctine wasps (Insecta, Hymenoptera, Braconidae). Zoologica Scripta, 27, 333–343.
Rambaut, A., Suchard, M. A., Xie, D., & Drummond, A. J. (2014). Tracer v1. 6. Available at: http://beast.bio.ed.ac.uk/Tracer
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. Systematic Biology, 61, 539–542.
Samacá-Sáenz, E., Belokobylskij, S. A., Quicke, D. L. J., & Zaldivar-Riveron, A. (2016). Systematics of the Neotropical braconid wasps of the Pedinotus genus group (Doryctinae). Systematic Entomology, 41, 481–491.
Sanderson, M. J. (2002). Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Molecular Biology and Evolution, 19, 101–109.
Seton, M., Müller, R. D., Zahirovic, S., Gaina, C., Torsvik, T., Shephard, G., Talsma, A., Gurnus, M., Turner, M., Maus, S., & Chandler, M. (2012). Global continental and ocean basin reconstructions since 200 ma. Earth-Science Reviews, 113, 212–270.
Sharkey, M. J., & Wharton, R. A. (1997). Morphology and terminology. In R. A. Wharton, P. M. Marsh, & M. J. Sharkey (Eds.), Manual of the New World Genera of the Family Braconidae (Hymenoptera) (pp. 19–37). Washington, DC: International Society of Hymenopterists, Special Publ. 1.
Shenefelt, R. D., & Marsh, P. M. (1976). Pars 13. Braconidae 9, Doryctinae. In J. van der Vecht & R. D. Shenefelt (Eds.), Hymenopterorum Catalogus (nova edito) (pp. 1263–1424). The Hague: W. Junk Publishers.
Stadler, T. (2009). On incomplete sampling under birth-death models and connections to the sampling-based coalescent. Journal of Theoretical Biology, 261, 58–66.
Vos, R. A., Balhoff, J. P., Caravas, J. A., Holder, M. T., Lapp, H., Maddison, W. P., Midford, P. E., Priyam, A., Sukumaran, J., Xia, X., & Stoltzfus, A. (2012). NeXML: rich, extensible, and verifiable representation of comparative data and metadata. Systematic Biology, 61, 675–689.
Xie, W., Lewis, P. O., Fan, Y., Kuo, L., & Chen, M.-H. (2011). Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Systematic Biology, 60, 150–160.
Yu, D. S. K., van Achterberg, C., & Horstmann, K. (2016). Taxapad, Ichneumonoidea 2015. Database on flash-drive, Ottawa, Ontario. http://www.taxapad.com/index.php. Accessed 16 Nov 2017.
Zaldivar-Riverón, A., Mori, M., & Quicke, D. L. J. (2006). Systematics of the cyclostome subfamilies of braconid parasitic wasps (Hymenoptera: Ichneumonoidea): a simultaneous molecular and morphological Bayesian approach. Molecular Phylogenetics and Evolution, 38, 130–145.
Zaldivar-Riverón, A., Belokobylskij, S. A., León-Regagnon, V., Martinez, J. J., Briceno, R., & Quicke, D. L. J. (2007). A single origin of gall association in a group of parasitic wasps with disparate morphologies. Molecular Phylogenetics and Evolution, 44, 981–999.
Zaldivar-Riverón, A., Belokobylskij, S. A., León-Regagnon, V., Briceno, R., & Quicke, D. L. J. (2008). Molecular phylogeny and historical biogeography of the cosmopolitan parasitic wasp subfamily Doryctinae (Hymenoptera: Braconidae). Invertebrate Systematics, 22, 345–363.
Zaldívar-Riverón, A., Martínez, J. J., Belokobylskij, S. A., Pedraza-Lara, C., Shaw, S. R., Hanson, P. E., & Varela-Hernández, F. (2014). Systematics and evolution of gall formation in the plant-associated genera of the wasp subfamily Doryctinae (Hymenoptera: Braconidae). Systematic Entomology, 39, 633–659.
Acknowledgements
We thank Mike Sharkey for donating part of the examined material, Cristina Mayorga and Guillermina Ortega for their help at the CNIN IB UNAM, Susana Guzmán for taking the digital pictures and Laura Márquez and Nelly López for their help with the DNA sequencing. RCO thanks the postgraduate program in Biological Sciences of the Universidad Nacional Autónoma de México (UNAM) for all the support given during his MSc studies. The present work is submitted as a requirement of the Programa de Posgrado en Ciencias Biológicas-UNAM (campo de conocimiento en sistemática) for RCO to obtain his MSc degree.
Funding
This work was supported by grants given by DGAPA-UNAM, Mexico (PAPIIT IN207016) and the Consejo Nacional de Ciencia y Tecnología (CONACyT; Proyecto Ciencia Básica convocatoria 2014 No. 220454) to AZR, and by grants given by of the Russian Foundation for Basic Research (project No. 19–04–00027) and the Russian State Research Project No. АААА-А19-119020690101-6 to SAB. This work was supported by an MSc scholarship given by CONACyT to RCO.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Figure S1
Chronogram derived from the Bayesian relaxed molecular clock analysis performed with BEAST and the concatenated data set showing divergence time estimates for selected clades. Black circles near branches represent the PP values ≥ 0.95; blue bars represent the 95% highest posterior densities (HPD) interval of clades (PNG 759 kb)
Figure S2
Priosphys denticulata Enderlain, 1920 (holotype, female). a habitus, lateral view; b head, dorsal view; c head, front view; d head, lateral view; e hind coxa, lateral view; f basal segments of antenna; g fore tibia; h metasoma, dorsolateral view; i first metasomal tergite; j second-fourth metasomal tergites; k apical part of metasoma (PNG 72.9 kb)
Table S1
Species assignment, localities and DNA vouchers and Genbank accession numbers of the taxa included in the study. Asterisks (*) indicate specimens whose sequences were combined in a single terminal. (PDF 115 kb)
Table S2
Primers and annealing temperatures used for PCRs. (PDF 57 kb)
Table S3
Evolutionary models used for the Bayesian MCMC analysis. (PDF 60 kb)
Rights and permissions
About this article
Cite this article
Castañeda-Osorio, R., Belokobylskij, S.A., Braet, Y. et al. Systematics and evolution of the parasitoid wasp genera of the tribe Holcobraconini (Hymenoptera: Braconidae: Doryctinae). Org Divers Evol 19, 409–422 (2019). https://doi.org/10.1007/s13127-019-00407-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13127-019-00407-1