Male Terminalia of Ceraphronoidea: Morphological Diversity in an Otherwise Monotonous Taxon
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Insect Systematics & Evolution 44 (2013) 261–347 brill.com/ise Male terminalia of Ceraphronoidea: morphological diversity in an otherwise monotonous taxon István Mikóa,*, Lubomir Masnerb, Eva Johannesc, Matthew J. Yoderd and Andrew R. Deansa aDepartment of Entomology, Pennsylvania State University, 501 ASI Building, University Park, PA 16802, USA bAgriculture and Agri-Food Canada, Ottawa, ON, Canada K1A 0C6 cNCSU-NSCORT, Department of Plant Biology, 2115 Gardner Hall Box 7612, North Carolina State University Raleigh, NC 27695, USA dIllinois Natural History Survey, 1816 South Oak Street, MC 652, Champaign, IL 61820, USA *Corresponding author, e-mail: [email protected] Published 25 October 2013 Abstract The skeletomuscular system of male terminalia in Evaniomorpha (Hymenoptera) is described and the functional morphology of male genitalia is discussed. Confocal laser scanning microscopy is the primary method used for illustrating anatomical phenotypes, and a domain-specific anatomy ontology is employed to more explicitly describe anatomical structures. A comprehensive data set of ceraphronoid male genitalia is analyzed, yielding the first phylogeny of the superfamily. One hundred and one taxa, including three outgroups, are scored for 48 characters. Ceraphronoidea are recovered as sister to the remaining Evaniomorpha in the implied weighting analyses. Numerous character states suggest that Ceraphronoidea is a relatively basal apocritan lineage. Ceraphronoidea, Ceraphronidae, and Megaspilinae are each retrieved as monophyletic in all analyses. Megaspilidae is not recovered as monophyletic. Lagynodinae is monophy- letic in the implied weighting analyses with strong support and is a polytomy in the equal weighting analy- sis. Lagynodinae shares numerous plesiomorphies with both Megaspilinae and Ceraphronidae. Relationships among genera are weakly corroborated. Masner is sister of Ceraphronidae. Trassedia is nested within Ceraphronidae based on the present analysis. Because of this and numerous features shared between it and Ceraphron we transfer Trassedia from Megaspilidae to Ceraphronidae. Dendrocerus forms a single monophyletic clade, with modest support, together with some Conostigmus species. This result challenges the utility of such traditional diagnostic characters as ocellar arrangement and shape of the male flagel- lomeres. Aphanogmus is monophyletic in the implied weighting, but remains a polytomy with Ceraphron in the equal weighting analysis. Gnathoceraphron is always nested within a well-supported Aphanogmus clade. Cyoceraphron and Elysoceraphron are nested within Ceraphron and Aphanogmus, respectively. The male genitalia prove to be a substantial source of phylogenetically relevant information. Our results indi- cate that a reclassification of Ceraphronoidea both at the family and generic level is necessary but that more data are required. Keywords Cladistic analysis; CLSM; conjunctiva; Figshare; fusion © Koninklijke Brill NV, Leiden, 2013 DOI 10.1163/1876312X-04402002 Downloaded from Brill.com10/07/2021 09:32:22AM via free access <UN> <UN> 262 I. Mikó et al. / Insect Systematics & Evolution 44 (2013) 261–347 Introduction Hymenoptera, which includes sawflies, wasps, bees, and ants, is one of the four most species-rich insect orders, with more than 145 000 known species (Huber 2009) and perhaps more than 1 million species remaining to be described (Sharkey 2007). The evolutionary history of Hymenoptera has yet to be resolved, though recent efforts have edged closer towards a robust estimate (Vilhelmsen et al. 2010; Heraty et al. 2011). The emerging evolutionary topology reveals a highly supported basal grade of herbivo- rous hymenopterans (sawflies and woodwasps, known as “Symphyta”), leading to an extraordinarily diverse and notorious rapid radiation of Apocrita (Whitfield & Kjer 2008). Most apocritan superfamilies are robustly monophyletic, but the relationships between them are weakly resolved. Perhaps the most uncertain is the position of the small hyperparasitoid lineage, Ceraphronoidea (Sharanowski et al. 2010, Sharkey et al. 2012), a putatively basal apocritan (Vilhelmsen et al. 2010). Ceraphronoidea was recently cataloged by Johnson & Musetti (2004) and currently includes four families: Ceraphronidae, Megaspilidae, and the fossil groups Stigmaphronidae and Radiophronidae. These four families include 27 valid genera (plus 28 generic concepts now considered junior synonyms) and 613 valid species (plus 235 species-level concepts now considered junior synonyms). Ceraphronoidea is one of the smallest of the major apocritan clades, yet they are the fourth most com- monly collected hymenopterans (Martínez de Murgía et al. 2001; Schmitt 2004). Most ceraphronoids are parasitoids of entomophagous insects that develop in weakly concealed environments, inside cocoons or puparia or hosts that are prepupae (Haviland 1920; Withycombe 1924; Kamal 1939), a lifestyle that is probably the ground plan biology for the clade. Many of their hosts are primary parasitoids or predators of economically important insects (e.g., predators of the coffee berry borer (Evans et al. 2005), spider mite predators (Diptera: Cecidomyiidae) (Oatman 1985), and parasitoids of lepidopteran pests on oil palm (Polaszek & Dessart 1996). Despite their abundance and economic importance, only one systematist, Paul Dessart (active 1962–2001, deceased 2001), has worked on the group in modern times, and his core revisionary hypotheses have never been tested phylogenetically. It is widely accepted that Apocrita is monophyletic, with Orussoidea as its sister lineage (Rasnitsyn 1988, 2002; Ronquist et al. 1999; Vilhelmsen 2003; Schulmeister 2003a; Sharkey 2007; Heraty et al. 2011). However, our knowledge of the phylogeny of the suborder remains incomplete, and the relationships between putatively basal apocritans (Ceraphronoidea, Evanioidea, Trigonalidae and Megalyroidea, together referred to as Evaniomorpha) remain elusive (Heraty et al. 2011). The importance of Evaniomorpha for resolving the phylogeny of Hymenoptera is broadly recognized, and exemplars are usually involved in analyses attempting to resolve higher-level phyloge- nies (Shcherbakov 1981; Gibson 1985, 1999; Heraty et al. 1994; Vilhelmsen 1996; 2000a,b, 2003; Schulmeister 2003b). Unfortunately, Ceraphronoidea has been excluded from most of these analyses and in some morphology-based analyses that did include ceraphronoid exemplars, character states were misinterpreted, probably due to their minute size. Numerous observations, however, indicate, that unlike other Downloaded from Brill.com10/07/2021 09:32:22AM via free access <UN> <UN> I. Mikó et al. / Insect Systematics & Evolution 44 (2013) 261–347 263 apocritans some Ceraphronoidea share putatively plesiomorphic character states with “Symphyta”, including: (1) presence of a propleural arm-postoccipital muscle, shared with some Tenthredinoidea (Vilhelmsen et al. 2010), (2) presence of a metanoto- metacoxal muscle, shared with most non-apocritan Hymenoptera (Vilhelmsen et al. 2010), (3) presence of a posterior apical spur on the protibia, shared with most non- apocritan Hymenoptera (Rasnitsyn 1988), (4) presence of a median mesoscutal sulcus that corresponds to an internal ridge, shared with most non-apocritan Hymenop- tera and with basal Apocritan lineages (Megalyroidea, Stephanoidea) (Gibson 1985), (5) presence of a mesonotal and mesofurcal depressor of the mesotrochanter with this muscle inserting distinctly ventrally of the site of insertion of the mesonotal depressor on the mesotrochanter (pers. obs.). This latter state of the mesotrochanteral extracoxal depressor complex was considered by Gibson (1999) to represent the hypothetical ancestor of Apocrita, though he did not observe the ceraphronoid furcal muscle in his studies. The collective phenome of ceraphronoid wasps is not only relatively monotonous (i.e., lacking distinct apomorphies) compared to other microhymenoptera (e.g., Chalcidoidea, Platygastroidea), but the few possibly suitable morphological variables (e.g., body shape, sculpture) are often affected by allometry (Fig. 1). Male genitalia, however, provide a source of discrete and size-independent characters. The utility of male genitalia in species delimitation was recognized relatively early and from the mid Fig. 1. Bright field images of undescribed species ofCeraphron showing the body size variability and related allometric changes. This figure is published in colour in the online edition of this journal, which can be accessed via http://booksandjournals.brillonline.com/content/1876312x. Downloaded from Brill.com10/07/2021 09:32:22AM via free access <UN> <UN> 264 I. Mikó et al. / Insect Systematics & Evolution 44 (2013) 261–347 20th century became the key element in species diagnoses (majority of Paul Dessart’s publications since 1963; Teodorescu 1967; Takada 1973). Male genitalia characters are certainly informative for higher level classification of basal Hymenoptera (Schulmeister 2003b) and have been successfully applied in generic level phylogenetic studies within Apocrita (Rozen 1951; Andena et al. 2007; Owen et al. 2007; Brajković et al. 2010; Žikić et al. 2011). While ceraphronoid male genitalia serve as an important source of species diagnostic characters their phylogenetic signal has never been tested. Here we provide the first phylogenetic analysis of Ceraphronoidea, based exclusively on 48 morphological characters related to the skeletomuscular system of the male terminalia. Materials and Methods Depositories