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Multivariate ratio analysis and DNA markers reveal a new Australian species and three synonymies in eucalypt-gall-associated Megastigmus (Hymenoptera: Megastigmidae)

Published online by Cambridge University Press:  27 May 2020

Ngoc Hoan Le Open the ORCID record for Ngoc Hoan Le [Opens in a new window] ,
Helen F. Nahrung Open the ORCID record for Helen F. Nahrung [Opens in a new window] ,
Jess A. T. Morgan  and
Simon A. Lawson Open the ORCID record for Simon A. Lawson [Opens in a new window]
Ngoc Hoan Le*
Affiliation:
Forest Industries Research Centre, University of the Sunshine Coast, Sippy Downs, QLD4556, Australia
Helen F. Nahrung
Affiliation:
Forest Industries Research Centre, University of the Sunshine Coast, Sippy Downs, QLD4556, Australia
Jess A. T. Morgan
Affiliation:
Department of Agriculture and Fisheries, EcoSciences Precinct, PO Box 267, BrisbaneQueensland4001, Australia
Simon A. Lawson
Affiliation:
Forest Industries Research Centre, University of the Sunshine Coast, Sippy Downs, QLD4556, Australia
*
Author for correspondence: Ngoc Hoan Le, Email: [email protected]
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Abstract

The genus Megastigmus Dalman, 1820 (Hymenoptera: Megastigmidae) contains potential biocontrol agents of the invasive eucalypt galling chalcid Leptocybe spp. (Hymenoptera: Eulophidae), with several species reported in various parts of the world. Species discrimination is challenging due to intraspecific morphological variation, difficulty in measuring sizes of body parts, and the lack of information regarding the global distribution of parasitic Megastigmus. We used two species commonly associated with Leptocybe in its native range to review taxonomic methods and determine the most reliable morphological characters in species delimitation. We examined size variation of body characters, and conducted species discrimination using multivariate ratio analysis, mitochondrial Cytochrome c oxidase subunit 1 (COI) and nuclear 28S rDNA (28S) sequences. Morphological traits were effective in species delimitation yet revealed high variation in several characters employed in current keys. Knowledge generated on morphology and DNA justified the description of a new species, M. manonae, sp. n., the first record of M. pretorianensis in Australia, and revised diagnostic characters for M. zvimendeli. Based on these diagnostic characters and molecular data, we synonymize three species (M. judikingae, syn. n., from Australia, M. sichuanensis, syn. n., from China and M. icipeensis, syn. n., from Kenya) with M. zvimendeli. Our findings highlight the importance of molecular markers in assisting taxonomic decision-making and the need for coordinated work in identifying Megastigmus associated with Leptocybe spp.

Keywords

LeptocybeMegastigmus manonaeMegastigmus zvimendelimorphologyparasitoidsspecies discrimination
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 110 , Issue 6 , December 2020 , pp. 709 - 724
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Auger-Rozenberg, MA, Kerdelhué, C, Magnoux, E, Turgeon, J, Rasplus, JY and Roques, A (2006) Molecular phylogeny and evolution of host-plant use in conifer seed chalcids in the genus Megastigmus (Hymenoptera: Torymidae). Systematic Entomology 31, 47–64.CrossRefGoogle Scholar
Baur, H and Leuenberger, C (2011) Analysis of ratios in multivariate morphometry. Systematic Biology 60, 813–825.CrossRefGoogle ScholarPubMed
Baur, H, Kranz-Baltensperger, Y, Cruaud, A, Rasplus, JY, Timokhov, AV and Gokhman, VE (2014) Morphometric analysis and taxonomic revision of Anisopteromalus Ruschka (Hymenoptera: Chalcidoidea: Pteromalidae) – an integrative approach. Systematic Entomology 39, 691–709.CrossRefGoogle ScholarPubMed
Boivin, T, Henri, H, Vavre, F, Gidoin, C, Veber, P, Candau, JN, Magnoux, E, Roques, A and Auger-Rozenberg, MA (2014) Epidemiology of asexuality induced by the endosymbiotic Wolbachia Across phytophagous wasp species: host plant specialization matters. Molecular Ecology 23, 2362–2375.CrossRefGoogle ScholarPubMed
Borowiec, N, La Salle, J, Brancaccio, L, Thaon, M, Warot, S, Branco, M, Ris, N, Malausa, J-C and Burks, R (2019) Ophelimus mediterraneus sp. n. (Hymenoptera, Eulophidae): a new Eucalyptus Gall wasp in the Mediterranean region. Bulletin of Entomological Research, 109, 678–694.CrossRefGoogle Scholar
Bouček, Z (1988) Australasian Chalcidoidea (Hymenoptera). A Biosystematic Revision of Genera of Fourteen Families, with a Reclassification of Species. Wallingford, UK: C.A.B International.Google Scholar
Boykin, LM, Armstrong, KF, Kubatko, L and De Barro, P (2012) Species delimitation and global biosecurity. Evolutionary Bioinformatic Online 8, 1–37.Google ScholarPubMed
Branco, M, Battisti, A and Mendel, Z (2016) Foliage feeding invasive insects: defoliators and Gall makers. In Paine, TD and Lieutier, F. (Eds.) Insects and diseases of mediterranean forest systems. Cham, Switzerland: Springer International Publishing, pp. 211–238.CrossRefGoogle Scholar
Bush, SJ, Dittrich-Schröder, G, Neser, S, Gevers, C, Baffoe, KO, Slippers, B and Hurley, BP (2017) First record of Quadrastichus Mendeli, a parasitoid of Leptocybe invasa, in South Africa. Southern Forests, 80, 275–277.CrossRefGoogle Scholar
Castro, L, Austin, A and Dowton, M (2002) Contrasting rates of mitochondrial molecular evolution in parasitic Diptera and Hymenoptera. Molecular Biology and Evolution 19, 1100–1113.CrossRefGoogle ScholarPubMed
Collins, RA, Boykin, LM, Cruickshank, RH and Armstrong, KF (2012) Barcoding's next top model: an evaluation of nucleotide substitution models for specimen identification. Methods in Ecology and Evolution 3, 457–465.CrossRefGoogle Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) Jmodeltest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle ScholarPubMed
DeSalle, R, Egan, MG and Siddall, M (2005) The unholy trinity: taxonomy, species delimitation and DNA barcoding. Philosophical Transactions of the Royal Society B: Biological Sciences 360, 1905–1916.CrossRefGoogle ScholarPubMed
Dittrich-Schröder, G, Harney, M, Neser, S, Joffe, T, Bush, S, Hurley, BP, Wingfield, MJ and Slippers, B (2014) Biology and host preference of Selitrichodes Neseri: a potential biological control agent of the Eucalyptus Gall wasp, Leptocybe invasa. Biological Control 78, 33–41.CrossRefGoogle Scholar
Dittrich-Schröder, G, Hoareau, TB, Hurley, BP, Wingfield, MJ, Lawson, S, Nahrung, HF and Slippers, B (2018) Population genetic analyses of complex global insect invasions in managed landscapes: a Leptocybe Invasa (Hymenoptera) case study. Biological Invasions 20, 2395–2420.CrossRefGoogle Scholar
Doğanlar, M (2015) Diagnosis of Megastigmus Spp. (Hymenoptera: Torymidae) reared from galls of Leptocybe invasa FISHER & LASALLE, 2004, (Hymenoptera: Eulophidae) on Eucalyptus Spp. (Myrtaceae), with description of a new species from South Africa. Entomofauna 36, 561–580.Google Scholar
Doğanlar, M and Hassan, E (2010) Review of Australian species of Megastigmus (Hymenoptera: Torymidae) associated with Eucalyptus, with descriptions of new species. Australian Journal of Basic and Applied Sciences 4, 5059–5150.Google Scholar
Doğanlar, M, Huang, Z-Y, Guo, C-H, Lu, W, Yang, Z-D, Yang, X-H and Zheng, X-L (2017) A new species of Megastigmus (Hymenoptera: Torymidae: Megastigminae) from China. Munis Entomology & Zoology 12, 368–374.Google Scholar
Evans, N and Paulay, G (2012) DNA Barcoding methods for invertebrates. In Walker, JM. (Ed.) DNA Barcodes. New York: Humana Press, pp. 47–77.CrossRefGoogle Scholar
FAO (2012) Forest pest species profile – Leptocybe invasa. pp. 1–2. http://www.fao.org/forestry/13569-05912e0e2fe9054c3ed4904ae597e3310.pdfGoogle Scholar
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.Google ScholarPubMed
Gibson, GAP, Read, JD and Fairchild, R (1998) Chalcid wasps (Chalcidoidea): illustrated glossary of positional and morphological terms. http://www.canacoll.org/Hym/Staff/Gibson/apss/chglintr.htm. (accessed April 2020).Google Scholar
Graham, MWRDV (1969) The Pteromalidae of North-Western Europe (Hymenoptera-Chalcidoidea). London: British Museum (Natural History), pp. 9–11.Google Scholar
Grissell, EE (1999) An Annotated Catalog of World Megastigminae (Hymenoptera: Chalcidoidea: Torymidae). Gainesville, Florida: American Entomological Institute, p. 93.Google Scholar
Grissell, EE (2006) A new species of Megastigmus Dalman (Hymenoptera: Torymidae), galling seed capsules of Eucalyptus Camaldulensis Dehnhardt (Myrtaceae) in South Africa and Australia. African Entomology 14, 87–94.Google Scholar
Guindon, S, Dufayard, J-F, Lefort, V, Anisimova, M, Hordijk, W and Gascuel, O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.CrossRefGoogle ScholarPubMed
Hajibabaei, M, Singer, GA, Hebert, PD and Hickey, DA (2007) DNA Barcoding: how it complements taxonomy, molecular phylogenetics and population genetics. Trends in Genetics 23, 167–172.CrossRefGoogle ScholarPubMed
Hernández, CM, Aquino, DA, Cuello, EM, Andorno, AV and Botto, EN (2015) Primera cita de Megastigmus zebrinus Grissell de Argentina (Hymenoptera: Torymidae) asociado a agallas de Leptocybe Invasa (Hymenoptera: Eulophidae). Revista de la Sociedad Entomologica Argentina 74, 75–77.Google Scholar
Huang, Z-Y, Liu, J-Y, Zhang, Y-J, Guo, C-H, Yang, Z-D, Lu, W and Zheng, X-L (2017) Scanning electron microscopy of antennal sensilla of Megastigmus sichuanensis Doğanlar et Zheng (Hymenoptera: Torymidae). Zoologischer Anzeiger 271, 25–32.CrossRefGoogle Scholar
Huang, ZY, Li, J, Lu, W, Zheng, XL and Yang, ZD (2018) Parasitoids of the eucalyptus gall wasp Leptocybe Spp. a global review. Environmental Science and Pollution Research 25, 29983–29995.CrossRefGoogle ScholarPubMed
Janšta, P, Cruaud, A, Delvare, G, Genson, G, Heraty, J, Křížková, B and Rasplus, J-Y (2018) Torymidae (Hymenoptera, Chalcidoidea) revised: molecular phylogeny, circumscription and reclassification of the family with discussion of its biogeography and evolution of life-history traits. Cladistics 34, 627–651.CrossRefGoogle Scholar
Kelly, J, La Salle, J, Harney, M, Dittrich-Schröder, G and Hurley, BP (2012) Selitrichodes Neseri n. sp, a new parasitoid of the eucalyptus gall wasp Leptocybe Invasa Fisher & La Salle (Hymenoptera: Eulophidae: Tetrastichinae). Zootaxa 3333, 50–57.CrossRefGoogle Scholar
Kim, I-K, Mendel, Z, Protasov, A, Blumberg, D and La Salle, J (2008) Taxonomy, biology, and efficacy of two Australian parasitoids of the eucalyptus gall wasp, Leptocybe Invasa Fisher & La Salle. Zootaxa 1910, 1–20.CrossRefGoogle Scholar
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549.CrossRefGoogle ScholarPubMed
Lanfear, R, Frandsen, PB, Wright, AM, Senfeld, T and 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.Google Scholar
Le, NH, Nahrung, HF, Griffiths, M and Lawson, SA (2018) Invasive Leptocybe Spp. and their natural enemies: global movement of an insect fauna on eucalypts. Biological Control 125, 7–14.CrossRefGoogle Scholar
Mendel, Z, Protasov, A, Fisher, N and La Salle, J (2004) Taxonomy and biology of Leptocybe Invasa gen. & sp. n. (Hymenoptera: Eulophidae), an invasive gall inducer on Eucalyptus. Australian Journal of Entomology 43, 101–113.CrossRefGoogle Scholar
Mendel, Z, Protasov, A, La Salle, J, Blumberg, D, Brand, D and Branco, M (2017) Classical biological control of two Eucalyptus Gall wasps; main outcome and conclusions. Biological Control 105, 66–78.CrossRefGoogle Scholar
Milliron, HE (1949) Taxonomic and biological investigations in the genus Megastigmus with particular reference to the taxonomy of the Nearctic species (Hymenoptera: Chalcidoidea; Callimomidae). American Midland Naturalist 41, 257–420.CrossRefGoogle Scholar
Narendran, T and Sureshan, P (1988) A contribution to our knowledge of Torymidae of India (Hymenoptera: Chalcidoidea). Bollettino del Laboratorio di Entomologia Agraria Filippo Silvestri, Portici 45, 37–47.Google Scholar
Narendran, T, Girish Kumar, P and Vastrad, A (2010) Two new species of Megastigmus Dalman (Hymenoptera: Torymidae) from India, with a revised key to Indian species. Records of the Zoological Survey of India 110, 1–6.Google Scholar
Noyes, JS (2020) Universal Chalcidoidea Database. http://www.nhm.ac.uk/chalcidoids.Google Scholar
Nugnes, F, Gebiola, M, Monti, MM, Gualtieri, L, Giorgini, M, Wang, J and Bernardo, U (2015) Genetic diversity of the invasive gall wasp Leptocybe Invasa (Hymenoptera: Eulophidae) and of its Rickettsia endosymbiont, and associated sex-ratio differences. PLoS One 10, 1–19.CrossRefGoogle ScholarPubMed
Phạm, QT, Dell, B and Isobel Burgess, T (2009) Susceptibility of 18 eucalypt species to the gall wasp Leptocybe Invasa in the nursery and young plantations in Vietnam. ScienceAsia 35, 113–117.Google Scholar
Price, PW (2005) Adaptive radiation of gall-inducing insects. Basic and Applied Ecology 6, 413–421.CrossRefGoogle Scholar
Price, PW, Fernandes, GW and Waring, GL (1987) Adaptive nature of insect galls. Environmental Entomology 16, 15–24.CrossRefGoogle Scholar
Protasov, A, Doĝanlar, M, La Salle, J and Mendel, Z (2008) Occurrence of two local Megastigmus species parasitic on the eucalyptus gall wasp Leptocybe Invasa in Israel and Turkey. Phytoparasitica 36, 449–459.CrossRefGoogle Scholar
Puillandre, N, Lambert, A, Brouillet, S and Achaz, G (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21, 1864–1877.CrossRefGoogle ScholarPubMed
Ramanagouda, S, Vastrad, A, Narendran, T, Basavanagoud, K and Viraktamath, S (2011) Current status of eucalyptus gall wasp and its native parasitoids in Karnataka. Journal of Biological Control 25, 193–197.Google Scholar
Ripley, B, Venables, B, Bates, DM, Hornik, K, Gebhardt, A and Firth, D (2018) Support functions and datasets for Venables and Ripley's MASS R package version 7.3-29.Google Scholar
Rokas, A, Nylander, JA, Ronquist, F and Stone, GN (2002) A maximum-likelihood analysis of eight phylogenetic markers in gallwasps (Hymenoptera: Cynipidae): implications for insect phylogenetic studies. Molecular Phylogenetics and Evolution 22, 206–219.CrossRefGoogle ScholarPubMed
Roques, A and Skrzypczyńska, M (2003) Seed-infesting chalcids of the genus Megastigmus Dalman, 1820 (Hymenoptera: Torymidae) native and introduced to the West Palearctic region: taxonomy, host specificity and distribution. Journal of Natural History 37, 127–238.CrossRefGoogle Scholar
Roques, A., Copeland, R.S., Soldati, L., Denux, O. and Auger-Rozenberg, M.-A. (2016) Megastigmus seed chalcids (Hymenoptera, Torymidae) radiated much more on Angiosperms than previously considered. I-Description of 8 new species from Kenya, with a key to the females of Eastern and Southern Africa. Zookeys, 51–124.CrossRefGoogle ScholarPubMed
RStudio Team (2019) RStudio: Integrated Development for R. Boston, MA: RStudio, Inc.Google Scholar
Sangtongpraow, B and Charernsom, K (2013) Evaluation of parasitism capacity of Megastigmus Thitipornae Dogănlar & Hassan (Hymenoptera: Torymidae), the local parasitoid of Eucalyptus Gall wasp, Leptocybe Invasa Fisher & La Salle (Hymenoptera: Eulophidae). Kasetsart Journal (Natural Science) 47, 191–204.Google Scholar
Scheffer, SJ and Grissell, E (2003) Tracing the geographical origin of Megastigmus transvaalensis (Hymenoptera: Torymidae): an African wasp feeding on a South American plant in North America. Molecular Ecology 12, 415–421.CrossRefGoogle Scholar
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics (Oxford, England) 30, 1312–1313.CrossRefGoogle ScholarPubMed
Tavaré, S and Miura, R (1986) Some mathematical questions in biology: DNA sequence analysis. Lectures on Mathematics in the Life Sciences 17, 57–86.Google Scholar
Viggiani, G, Laudonia, S and Bernardo, U (2002) Aumentano gli insetti dannosi agli eucalipti. Informatore Agrario 58, 2.Google Scholar
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