Molecular phylogenetic analyses and morphological variation point to taxonomic problems among four genera of parasitoid doryctine wasps (Hymenoptera : Braconidae)
Marco Gebiola A B F , Antonio P. Garonna C , Umberto Bernardo A and Sergey A. Belokobylskij D E
+ Author Affiliations
- Author Affiliations
A CNR – Istituto per la Protezione Sostenibile delle Piante, Via Università, 133, Portici 80055, NA, Italy.
B Department of Entomology, 410 Forbes Building, The University of Arizona, Tucson, AZ 86721, USA.
C Laboratorio di Entomologia ‘E. Tremblay’, Dipartimento di Agraria, Università degli Studi di Napoli ‘Federico II’, Via Università 100, 80055 Portici, Italy.
D Zoological Institute, Russian Academy of Sciences, St Petersburg, 199034, Russia.
E Museum and Institute of Zoology, Polish Academy of Sciences, Warsaw, 00–679, Poland.
F Corresponding author. Email: marco.gebiola@gmail.com
Invertebrate Systematics 29(6) 591-609 https://doi.org/10.1071/IS14064
Submitted: 18 December 2014 Accepted: 27 September 2015 Published: 22 December 2015
Abstract
Doryctinae (Hymenoptera : Braconidae) is a large and diverse subfamily of parasitic wasps that has received much attention recently, with new species and genera described and phylogenies based on morphological and/or molecular data that have improved higher-level classification and species delimitation. However, the status of several genera is still unresolved, if not controversial. Here we focus on two related groups of such genera, Dendrosoter Wesmael–Caenopachys Foerster and Ecphylus Foerster–Sycosoter Picard & Lichtenstein. We integrated morphological and molecular (COI and 28S–D2 genes) evidence to highlight, by phylogenetic analyses (maximum likelihood and Bayesian) and a posteriori morphological examination, previously overlooked variation, which is here illustrated and discussed. Monophyly of Dendrosoter and Caenopachys and the presence of synapomorphic morphological characters support synonymy of Caenopachys under Dendrosoter. Low genetic differentiation and high variability for putatively diagnostic morphological characters found in both C. hartigii (Ratzeburg) and C. caenopachoides (Ruschka) supports synonymy of D. caenopachoides under D. hartigii, syn. nov. Morphological and molecular evidence together also indicate independent generic status for Sycosoter, stat. rev., which is here resurrected. This work represents a further advancement in the framework of the ongoing effort to improve systematics and classification of the subfamily Doryctinae.
Additional keywords: 28S–D2, Caenopachys, COI, Dendrosoter, Doryctinae, Ecphylus, integrative taxonomy, Sycosoter.
References
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, 900–928.Belokobylskij, S. A. (1993). Contribution to the taxonomy of Braconidae (Hymenoptera) of the Russian Far East. Russian Entomological Journal 2, 87–103.
Belokobylskij, S. A. (1996a). Parasitism on the beetles (Coleoptera) as important stage in the evolution of braconid wasps (Hymenoptera, Braconidae). Part I. Entomologicheskoe Obozrenie 75, 660–676.
Belokobylskij, S. A. (1996b). Parasitism on the beetles (Coleoptera) as important stage in the evolution of braconid wasps (Hymenoptera, Braconidae). Part II. Entomologicheskoe Obozrenie 75, 790–814.
Belokobylskij, S. A. (1998). Subfam. Doryctinae. In ‘Opredelitel’ Nasekomykh Dal’nego Vostoka Rossii. Setchatokryloobraznye, Skorpionnitzy, Perepionchatokrylye [Key to the Insects of the Russian Far East. Neuropteroidea, Mecoptera, Hymenoptera]’. (Ed. P. A. Lehr.) pp. 50–109. (Dal’nauka: Vladivostok, Russia). [In Russian]
Belokobylskij, S. A. (2002). Two new Oriental genera of Doryctinae (Hymenoptera, Braconidae) from termite nests. Journal of Natural History 36, 953–962.
| Two new Oriental genera of Doryctinae (Hymenoptera, Braconidae) from termite nests.Crossref | GoogleScholarGoogle Scholar |
Belokobylskij, S. A. (2009). The genus Ecphylus Foerster (Hymenoptera, Braconidae, Doryctinae) of Japan. Zoosystematica Rossica 18, 83–98.
Belokobylskij, S. A., and Maetô, K. (2009). ‘Doryctinae (Hymenoptera, Braconidae) of Japan. (Fauna Mundi. Vol. 1).’ (Warshawska Drukarnia Naukowa: Warszawa, Poland.)
Belokobylskij, S. A., and Tobias, V. I. (1986). Subfam. Doryctinae. In ‘Opredelitel’ Nasekomykh Evropeyskoy Chasti SSSR. Hymenoptera [Keys to Insects of the USSR European Part. Hymenoptera]’. (Ed. G. S. Medvedev.) pp. 21–72. (Nauka: Leningrad, Russia.) [In Russian]
Belokobylskij, S. A., Iqbal, M., and Austin, A. D. (2004a). Systematics, distribution and diversity of the Australasian doryctine wasps (Hymenoptera, Braconidae, Doryctinae). Records of the South Australian Museum. Monograph Series 8, 1–150.
Belokobylskij, S. A., Zaldívar-Riverón, A., and Quicke, D. L. J. (2004b). Phylogeny of the genera of the parasitic wasps subfamily Doryctinae (Hymenoptera: Braconidae) based on morphological evidence. Zoological Journal of the Linnean Society 142, 369–404.
| Phylogeny of the genera of the parasitic wasps subfamily Doryctinae (Hymenoptera: Braconidae) based on morphological evidence.Crossref | GoogleScholarGoogle Scholar |
Brues, C. T. (1923). Termitobracon, a termitophilous braconid from British Guiana. Zoologica 3, 427–432.
Campbell, B., Steffen-Campbell, J., and Werren, J. (1993). Phylogeny of the Nasonia species complex (Hymenoptera: Pteromalidae) inferred from an internal transcribed spacer (ITS2) and 28S rDNA sequences. Insect Molecular Biology 2, 225–237.
| Phylogeny of the Nasonia species complex (Hymenoptera: Pteromalidae) inferred from an internal transcribed spacer (ITS2) and 28S rDNA sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmvFOnur4%3D&md5=175e8996a35fc9ea52250ab8fef936d0CAS | 9087560PubMed |
Ceccarelli, F. S., Sharkey, M. J., and 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.
| Species identification in the taxonomically neglected, highly diverse, Neotropical parasitoid wasp genus Notiospathius (Braconidae: Doryctinae) based on an integrative molecular and morphological approach.Crossref | GoogleScholarGoogle Scholar | 22079550PubMed |
Cushman, R. A. (1923). A new subfamily of Braconidae (Hymenoptera) from termite nests. Proceedings of the Entomological Society of Washington 25, 54–55.
Fahringer, J. (1930). Palaearktischen Region. Opuscula Braconologica 3, 1–160.
Foerster, A. (1862). Synopsis der Familien und Gattungen der Braconen. Verhandlungen des Naturhistorischen Vereines der Preussischen Rheinlande und Westphalens 19, 225–288.
Foerster, A. (1878). Kleine Monographien parasitischer Hymenopteren. Verhandlungen des Naturhistorischen Vereines der Preussischen Rheinlande und Westphalens 35, 42–82.
Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 1:CAS:528:DyaK2MXjt12gtLs%3D&md5=c84f72a2d796a7fee91c4e2e01175599CAS | 7881515PubMed |
Gebiola, M., Bernardo, U., Viggiani, G., Monti, M. M., and Navone, P. (2009). Pnigalio agraules (Walker) and Pnigalio mediterraneus Ferrière and Delucchi (Hymenoptera: Eulophidae): two closely related valid species. Journal of Natural History 43, 2465–2480.
| Pnigalio agraules (Walker) and Pnigalio mediterraneus Ferrière and Delucchi (Hymenoptera: Eulophidae): two closely related valid species.Crossref | GoogleScholarGoogle Scholar |
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symposium Series 41, 95–98.
| 1:CAS:528:DC%2BD3cXhtVyjs7Y%3D&md5=f1de1a25ccd9666b647db6a2245a60cfCAS |
Hebert, P. D. N., Penton, E. H., Burns, J. M., Janzen, D. H., and 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.
| Ten species in one: DNA barcoding reveals cryptic species in the Neotropical skipper butterfly Astraptes fulgerator.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVyju7g%3D&md5=779b1bd0f1967ad399e1391eed756639CAS |
Katoh, K., and Toh, H. (2008). Recent developments in the MAFFT multiple sequence alignment program. Briefings in Bioinformatics 9, 286–298.
| Recent developments in the MAFFT multiple sequence alignment program.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpt1artrs%3D&md5=236425aba2026540cc17978d4fca1cdaCAS | 18372315PubMed |
Kennedy, B. H. (1970). Dendrosoter protuberans (Hymenoptera: Braconidae) an introduced larval parasitoid of Scolytus multistriatus. Annals of the Entomological Society of America 63, 351–358.
| Dendrosoter protuberans (Hymenoptera: Braconidae) an introduced larval parasitoid of Scolytus multistriatus.Crossref | GoogleScholarGoogle Scholar |
Kistner, D. H., Jacobson, R. J., and Elliot, D. E. (2000). Some interesting Braconidae that live with termites and their behavior (Hymenoptera; Isoptera: Termitidae, Nasutitermitinae). Sociobiology 36, 257–264.
Lanfear, R., Calcott, B., Ho, S. Y. W., and Guindon, S. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.
| PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnt1ehsbg%3D&md5=69a56250f99303ede6ba715e4dc41f26CAS | 22319168PubMed |
Mancini, D., Priore, R., Battaglia, D., and van Achterberg, C. (2003). Caenopachys hartigii (Ratzeburg) (Hymenoptera: Braconidae: Doryctinae) confirmed for Italy, with notes on the status of the genus Caenopachys Foerster. Zoölogische Mededelingen , 459–470.
Marsh, P. M. (1993). Descriptions of new western hemisphere genera of the subfamily Doryctinae (Hymenoptera: Braconidae). Contributions of the American Entomological Institute 28, 1–58.
Marsh, P. M. (1997). Subfamily Doryctinae. In ‘Manual of the New World genera of the family Braconidae (Hymenoptera) 1’. (Eds R. A. Wharton, P. M. Marsh, M. J. Sharkey.) pp. 207–233. (The International Society of Hymenopterists: Washington, DC.)
Marsh, P. M. (2002). The Doryctinae of Costa Rica (excluding the genus Heterospilus). Memoirs of the American Entomological Institute 70, 1–319.
Marsh, P. M., Wild, A. I., and Whitfield, J. B. (2013). The Doryctinae (Braconidae) of Costa Rica: genera and species of the tribe Heterospilini. ZooKeys 347, 1–474.
| The Doryctinae (Braconidae) of Costa Rica: genera and species of the tribe Heterospilini.Crossref | GoogleScholarGoogle Scholar | 24222723PubMed |
Picard, F. (1928). Les variations des caractères sexuels secondaires chez les Braconides des genres Caenopachys Foerst. et Dendrosoter Wesm. Bulletin de la Société Zoologique de France 53, 50–56.
Picard, F., and Lichtenstein, J. L. (1917). Un braconide nouveau, Sycosoter lavagnei, n.g., n.sp., parasite de l’Hypoborus ficus Er. (Col.). Bulletin de la Société Entomologique de France 16, 284–287.
Ramírez, B. W., and Marsh, P. M. (1996). A review of the genus Psenobolus (Hymenoptera: Braconidae) from Costa Rica, an inquiline fig wasp with brachypterous males, with descriptions of two new species. Journal of Hymenoptera Research 5, 64–72.
Ronquist, F., Teslenko, M., van der Marsk, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across large model space. Systematic Biology 61, 539–542.
| MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across large model space.Crossref | GoogleScholarGoogle Scholar | 22357727PubMed |
Ruschka, F. (1916). Description of Ecphylus caudatus. In Wichmann H. Börkenkäfer Istriens. Mit einem Anhang über deren parasitische Hymenopteren. Entomologische Blätter. Zeitschrift fur Biololie und Systematik der Käfer 12, 11–29.
Ruschka, F. (1925). Beitrag zur Kenntnis der forstlichen Braconiden. Zeitschrift für Angewandte Entomologie 11, 197–202.
| Beitrag zur Kenntnis der forstlichen Braconiden.Crossref | GoogleScholarGoogle Scholar |
Russo, G. (1938). Contributo alla conoscenza dei Coleotteri Scolitidi Fleotribo: Phleotribus scarabaeoides (Bern.) Fauv. Parte seconda. Biografia, simbionti, danni e lotta. Bolletino Laboratorio di Entomologia Agraria di Portici 2, 1–420.
Shaw, S. R., and Edgerly, J. S. (1985). A new braconid genus (Hymenoptera) parasitizing webspinners (Embiidina) in Trinidad. Psyche 92, 505–512.
| A new braconid genus (Hymenoptera) parasitizing webspinners (Embiidina) in Trinidad.Crossref | GoogleScholarGoogle Scholar |
Shenefelt, R. D., and Marsh, P. M. (1976). Braconidae 9. Doryctinae. In ‘Hymenopterorum Catalogus. Pars 13’. (Eds J. van der Vecht, R. D. Shenefelt) pp. 1263–1424. (Dr W. Junk: Gravenhage, Netherlands.)
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
| RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFKlsbfI&md5=df50a1f20f2be0cbcb0dff3c135f1b17CAS | 16928733PubMed |
Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007). MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.
| MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVGrsL8%3D&md5=f8e53b258fd2c43c06c2d15a4352e345CAS | 17488738PubMed |
Telenga, N. A. (1941). ‘Fauna USSR. Hymenoptera. Fam. Braconidae, Subfam. Braconinae (continuation) and Sigalphinae.’ (AS USSR Publishing House: Moscow-Leningrad, Russia.) 5, 1–466.
Waterhouse, D. F., and Sands, D. P. A. (2001). ‘Classical Biological Control of Arthropods in Australia.’ ACIAR monograph no. 77. (Australian Centre for International Agricultural Research: Canberra.)
Wesmael, C. (1838). Monographie des Braconides de Belgique. Nouveaux Mémoires de l’Academie Royale des Sciences et Belle-Lettres de Bruxelles 11, 1–166.
Wharton, R. A. (1993). Bionomics of the Braconidae. Annual Review of Entomology 38, 121–143.
| Bionomics of the Braconidae.Crossref | GoogleScholarGoogle Scholar |
Wharton, R. A., and Hanson, P. E. (2005). Gall wasps in the family Braconidae (Hymenoptera). In ‘Biology, Ecology, and Evolution of Gall-inducing Arthropods’. (Eds A. Raman, W. C. Schaefer, T. M. Whiters.) pp. 495–505. (Science Publishers: Enfield, NH, USA.)
Yu, D. S., van Achterberg, C., and Horstman, K. (2012). ‘Taxapad 2012, Ichneumonoidea 2011.’ (Ottawa, Ontario, Canada.)
Zaldívar-Riverón, A., Belokobylskij, S. A., León-Regagnon, V., Martinez, J. J., Briceño, R., and 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, 981–992.
| A single origin of gall association in a group of parasitic wasps with disparate morphologies.Crossref | GoogleScholarGoogle Scholar | 17625923PubMed |
Zaldívar-Riverón, A., Belokobylskij, S. A., León-Regagnon, V., Briceño, R., and Quicke, D. L. J. (2008). Molecular phylogeny and historical biogeography of the cosmopolitan parasitic wasp subfamily Doryctinae (Hymenoptera: Braconidae). Invertebrate Systematics 22, 345–363.
| Molecular phylogeny and historical biogeography of the cosmopolitan parasitic wasp subfamily Doryctinae (Hymenoptera: Braconidae).Crossref | GoogleScholarGoogle Scholar |
Zaldívar-Riverón, A., Martinez, J. J., Ceccarelli, F. S., De Jasús-Bonilla, V. S., Rodriguez-Perez, A. C., Resendiz-Flores, A., and Smith, A. (2010). DNA barcoding a highly diverse group of parasitoid wasps (Braconidae: Doryctinae) from Mexican nature reserve. Mitochondrial DNA 21, 18–23.
| DNA barcoding a highly diverse group of parasitoid wasps (Braconidae: Doryctinae) from Mexican nature reserve.Crossref | GoogleScholarGoogle Scholar | 21271854PubMed |
Zaldívar-Riverón, A., Martinez, J. J., Belokobylskij, S. A., Pedraza-Lara, C., Shaw, S. R., Hanson, P. E., and Carela-Hernandez, 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.
| Systematics and evolution of gall formation in the plant-associated genera of the wasp subfamily Doryctinae (Hymenoptera: Braconidae).Crossref | GoogleScholarGoogle Scholar |
