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A Phylogenetic Analysis of the Megadiverse Chalcidoidea (Hymenoptera)

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A Phylogenetic Analysis of the Megadiverse Chalcidoidea (Hymenoptera) UC Riverside UC Riverside Previously Published Works Title A phylogenetic analysis of the megadiverse Chalcidoidea (Hymenoptera) Permalink https://escholarship.org/uc/item/3h73n0f9 Journal Cladistics, 29(5) ISSN 07483007 Authors Heraty, John M Burks, Roger A Cruaud, Astrid et al. Publication Date 2013-10-01 DOI 10.1111/cla.12006 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Cladistics Cladistics 29 (2013) 466–542 10.1111/cla.12006 A phylogenetic analysis of the megadiverse Chalcidoidea (Hymenoptera) John M. Heratya,*, Roger A. Burksa,b, Astrid Cruauda,c, Gary A. P. Gibsond, Johan Liljeblada,e, James Munroa,f, Jean-Yves Rasplusc, Gerard Delvareg, Peter Jansˇtah, Alex Gumovskyi, John Huberj, James B. Woolleyk, Lars Krogmannl, Steve Heydonm, Andrew Polaszekn, Stefan Schmidto, D. Chris Darlingp,q, Michael W. Gatesr, Jason Motterna, Elizabeth Murraya, Ana Dal Molink, Serguei Triapitsyna, Hannes Baurs, John D. Pintoa,t, Simon van Noortu,v, Jeremiah Georgea and Matthew Yoderw aDepartment of Entomology, University of California, Riverside, CA, 92521, USA; bDepartment of Evolution, Ecology and Organismal Biology, Ohio State University, Columbus, OH, 43210, USA; cINRA, UMR 1062 CBGP CS30016, F-34988, Montferrier-sur-Lez, France; dAgriculture and Agri-Food Canada, 960 Carling Avenue, Ottawa, ON, K1A 0C6, Canada; eSwedish Species Information Centre, Swedish University of Agricultural Sciences, PO Box 7007, SE-750 07, Uppsala, Sweden; fInstitute for Genome Sciences, School of Medicine, University of Maryland, Baltimore, MD, 21201, USA; gCirad, INRA, UMR 1062 CBGP CS30016, F-34988, Montferrier-sur-Lez, France; hDepartment of Zoology, Charles University, Vinicna 7, CZ-128 44, Praha 2, Czech Republic; iSchmalhausen Institute of Zoology, National Academy of Sciences of Ukraine, Kiev, 30 01601, Ukraine; jNatural Resources Canada, c/o Canadian National Collection of Insects, 960 Carling Ave, Ottawa, ON, K1A 0C6, Canada; kDepartment of Entomology, Texas A&M University, College Station, TX, 77843, USA; lDepartment of Entomology, State Museum of Natural History Stuttgart, Rosenstein 1, 70191, Stuttgart, Germany; mBohart Museum of Entomology, University of California, Davis, CA, 95616, USA; nDepartment of Entomology, Natural History Museum, London, SW7 5BD, UK; oStaatliche Naturwissenschaftliche Sammlungen Bayerns, Zoologische Staatssammlung, Munchhausenstr.€ 21, 81247, Munich, Germany; pDepartment of Natural History, Royal Ontario Museum, Toronto, ON, M5S 2C6, Canada; qDepartment of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, M5S 1A1, Canada; rSystematic Entomology Laboratory, USDA, ARS, PSI, c/o National Museum of Natural History, Washington, DC, 20013, USA; sAbt. Wirbellose Tiere, Naturhistorisches Museum der Burgergemeinde Bern, Bernastrasse 15, 3005, Bern, Switzerland; tPO Box 2266, Waldport, OR, 97394, USA; uNatural History Department, Iziko South African Museum, PO Box 61, Cape Town, 8000, South Africa; vDepartment of Zoology, University of Cape Town, Private Bag, Rondebosch, 7701, South Africa; wIllinois Natural History Survey, University of Illinois, Champaign, IL, 61820, USA Accepted 19 September 2012 Abstract Chalcidoidea (Hymenoptera) is extremely diverse with an estimated 500 000 species. We present the first phylogenetic analysis of the superfamily based on both morphological and molecular data. A web-based, systematics workbench mx was used to score 945 character states illustrated by 648 figures for 233 morphological characters for a total of 66 645 observations for 300 taxa. The matrix covers 22 chalcidoid families recognized herein and includes 268 genera within 78 of 83 subfamilies. Morphological data were analysed alone and in combination with molecular data from ribosomal 18S (2105 bp) and 28S D2–D5 expansion regions (1812 bp). Analyses were analysed alone and in combined datasets using implied-weights parsimony and likelihood. Proposed changes in higher classification resulting from the analyses include: (i) recognition of Eriaporidae, revised status; (ii) recognition of Cynipencyrtidae, revised status; (iii) recognition of Azotidae, revised status; (iv) inclusion of Sycophaginae in Agaonidae, revised sta- tus; (v) reclassification of Aphelinidae to include Aphelininae, Calesinae, Coccophaginae, Eretmocerinae and Eriaphytinae; (vi) inclusion of Cratominae and Panstenoninae within Pteromalinae (Pteromalidae), new synonymy; (vii) inclusion of Epichrysomalli- nae in Pteromalidae, revised status. At a higher level, Chalcidoidea was monophyletic, with Mymaridae the sister group of Rotoiti- dae plus the remaining Chalcidoidea. A eulophid lineage was recovered that included Aphelinidae, Azotidae, Eulophidae, Signiphoridae, Tetracampidae and Trichogrammatidae. Eucharitidae and Perilampidae were monophyletic if Eutrichosomatinae (Pteromalidae) was included, and Eupelmidae was monophyletic if Oodera (Pteromalidae: Cleonyminae) was included. Likelihood recovered a clade of Eupelmidae + (Tanaostigmatidae + (Cynipencyrtus + Encyrtidae). Support for other lineages and their impact on the classification of Chalcidoidea is discussed. Several life-history traits are mapped onto the new phylogeny. © The Willi Hennig Society 2013. © 2012 Her Majesty the Queen in Right of Canada Cladistics © The Willi Hennig Society 2013 Reproduced with the permission of the Minister of Agriculture and Agri-Food Canada. J.M. Heraty et al. / Cladistics 29 (2013) 466–542 467 Without question, Chalcidoidea is one of the most whereas many other species appear to be narrowly oli- megadiverse groups of insects. Their morphological gophagous or monophagous, for example, some Aphy- diversity is staggering (Fig. 1). They range in size from tis or Aphelinus (Aphelinidae). Species attack all life such veritable giants as females of Leptofoenus (Ptero- stages from eggs to adults and, as internal parasitoids, malidae), which exceed 20 mm, to the minute and mor- often multiple life stages. Species can be primary, sec- phologically bizarre male of Dicopomorpha ondary, or even tertiary parasitoids, with some taxa echmepterygis (Mymaridae), the smallest known speci- required to parasitize their own species to complete men of which is 0.13 mm long. Males of D. echmeptery- development (heteronomous autoparasitism) (Hunter gis have lost eyes, ocelli, mouthparts, antennal and Woolley, 2001). Because of its members’ host flagellum, wings, tarsi except for a highly modified aroli- associations and life-history traits, Chalcidoidea is one um, and virtually any other feature that places them as of the most important groups for biological control of parasitic wasps (Fig. 1a). Other bizarrities include male other insects in both natural and agricultural ecosys- fig wasps, which can be reduced to turtle-like fighting tems (Noyes and Hayat, 1994; Heraty, 2009). Some machines that bear no resemblance to their correspond- Chalcidoidea, especially Trichogramma (Trichogram- ing females and are hardly recognizable as chalcidoids, matidae) and Nasonia (Pteromalidae), are also model or the grotesquely enlarged scutellum (Fig. 1h) of organisms for numerous studies of sex determination, Galearia latreillei (Eucharitidae) and the dart-shaped the influence of bacterial endosymbionts and the genet- ovipositor sheaths (Fig. 1j) of Cameronella (Pteromali- ics of speciation (2223 publications and 34 155 cita- dae). Convergent morphology is also rampant, and tions from Web of Science, 17 August 2012). enlarged femora, enlarged acropleura, reductions in the However, there has not been a robust phylogenetic number of antennal and tarsal segments, as well as hypothesis to provide an evolutionary framework for reductions in wings and wing venation have all been these studies. proposed as being independently derived in very dis- Members of the Chalcidoidea appear to have under- tantly related taxonomic groups. Matching their great gone their spectacular radiation in a relatively short morphological diversity is their numerical diversity, time. Both Mymaridae and Mymarommatoidea occur with estimates of more than 500 000 species, of which in Cretaceous amber deposits, with the first mymarids only about 22 506 have been described (Heraty, 2009; recorded from upper Albian deposits, 97–110 Ma Noyes, 2011). The extreme numerical and morphologi- (Gibson et al., 2007; Poinar and Huber, 2011). “Eulo- cal diversity has resulted in a large number of higher phoid” fossils have been found in mid-Cretaceous taxa being described relative to other superfamilies of (Yoshimoto, 1975; Schmidt et al., 2010) and lower- parasitic Hymenoptera, with 19 families and 83 subfam- Cretaceous amber (Kaddumi, 2005; photo of Minu- ilies prior to the present study (Noyes, 2011). As a toma yathribi Kaddumi suggests Tetracampidae: result, no single individual has previously been able to Bouceklytinae; J.T.H.), but otherwise the greatest conduct a comprehensive phylogenetic analysis based diversity of Chalcidoidea does not appear until the on morphology, and there have been only a few propos- Eocene with the appearance of most family groups, als for higher-level relationships of Chalcidoidea that including Eucharitidae, Eupelmidae and Torymidae either are not phylogenetic (Grissell, 1987; Gibson, (Gibson, 2008; Heraty and Darling, 2009). Their rapid 1990; Noyes, 1990) or are based on only limited charac- post-Cretaceous diversification parallels similar radia- ter systems and relatively few taxa (Gibson, 1986a; tions in the angiosperms and insects (Wiegmann et al., Heraty et
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