Molecular Phylogeny of the Sawfly Subfamily Nematinae (Hymenoptera: Tenthredinidae)
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Systematic Entomology (2006),31, 569–583 DOI: 10.1111/j.1365-3113.2006.00336.x Molecular phylogeny of the sawfly subfamily Nematinae (Hymenoptera: Tenthredinidae) TOMMI NYMAN1 , ALEXEY G. ZINOVJEV2 , VELI VIKBERG3 and BRIAN D. FARRELL4 1Department of Biology, University of Oulu, Oulu, Finland, 2Zoological Institute, Russian Academy of Sciences, St. Petersburg, Russia, 3Liinalammintie 11 as. 6, Turenki, Finland, 4Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts, U.S.A. Abstract. Nematinae is one of the largest subfamilies in the sawfly family Tenthredinidae, but internal relationships are unknown in the absence of any formal phylogenetic analysis. To understand the internal phylogeny of Nematinae, we sequenced a portion of the mitochondrial cytochrome oxidase I gene and the nuclear elongation factor-1a gene from thirteen outgroup taxa and sixty-eight nematine species, the ingroup taxa of which represent all major genera and subgenera within the subfamily. Maximum parsimony and Bayesian phyloge- netic analyses of the DNA sequence data show that: (1) Nematinae are monophy- letic in a broad sense which includes Hoplocampa, Susana and the tribe Cladiini, which have been classified often into separate subfamilies; together with Craterocercus, these taxa form a paraphyletic basal grade with respect to the remaining Nematinae, but among-group relationships within the grade remain weakly resolved; (2) the remainder of the ingroup, Nematinae s. str, is monophy- letic in all combined-data analyses; (3) within Nematinae s. str, the ‘Higher’ Nematinae is divided into three groups, Mesoneura and the large tribes Nematini and Pristiphorini; (4) although the traditional classifications at the tribal level are largely upheld, some of the largest tribes and genera are obviously para- or polyphyletic; (5) according to rate-smoothed phylogenies dated with two fossil calibration points, Nematinae originated 50–120 million years ago. In addition, the results from all Bayesian analyses provide strong and consistent support for the monophyly of Tenthredinidae, which has been difficult to demonstrate in previous parsimony analyses of morphological and molecular data. Introduction in the north temperate region (Marlatt, 1896; Kouki et al., 1994; Kouki, 1999) and, in many Arctic areas, nematines are The cosmopolitan sawfly family Tenthredinidae includes the only sawflies present (Benson, 1958; Smith, 1979; Gauld over 6000 species divided into six subfamilies (Goulet, & Bolton, 1988). The southernmost naturally occurring 1992; Taeger & Blank, 1998). One of the largest is nematine species occur in Brazil (Malaise, 1942; Smith, Nematinae, which comprises over 1000 species. Nematinae 2003) and Borneo (Benson, 1963). Nematine larvae rank has a primarily northern distribution: by contrast with most amongst the principal insect herbivores in many habitats, other insect taxa, the diversity of nematines reaches its peak and some species associated with trees are considered as serious pests. For example, Hoplocampa species damage fruits of orchard trees, and Anoplonyx and Pristiphora spe- cies can damage spruce and larch forests severely (Smith, Correspondence: Tommi Nyman, Department of Biology, 1979; Gauld & Bolton, 1988; Viitasaari, 2002). University of Oulu, PO Box 3000, FI-90014 Oulu, Finland. Despite their ubiquity and ecological importance, the E-mail: [email protected] phylogenetic relationships amongst nematine taxa remain # 2006 The Authors Journal compilation # 2006 The Royal Entomological Society 569 570 T. Nyman et al. unknown. The subfamily has been divided traditionally Materials and methods into some eight to nine tribes and approximately forty genera (cf. Smith, 1979; Zhelochovtsev, 1988, 1994; Abe Taxon sampling & Smith, 1991; Lacourt, 1998, 1999; Taeger et al., 1998). Because the definition of Nematinae is ambiguous, some The three largest nematine genera, Pristiphora, Nematus nematine groups (especially the tribe Cladiini, and the and Pachynematus s.l., have proven to be particularly genera Susana and Hoplocampa) have been classified complex from a taxonomic perspective, because attempts frequently as separate subfamilies (e.g. Yuasa, 1922; Ross, to divide them into smaller genera or subgenera have led 1937, 1951; Maxwell, 1955; Goulet, 1992; Lacourt, 1998, to difficulties in classifying many species (Benson, 1958; 1999). To date, no formal morphology-based phylogenetic Smith, 1979; Viitasaari, 2002). Here, we follow mainly analyses of the Nematinae have been performed, partly the nomenclature of the maximally divisive (sub)generic because of the limited morphological divergence amongst classifications of Zhelochovtsev (1988, 1994) and Lacourt groups and partly as a result of difficulties that follow from (1998, 1999) to ensure a broad enough taxon sample. the broad Holarctic distributions of many nematine The sixty-eight ingroup taxa included in the phylogenetic species and genera (Benson, 1958, 1962; Smith, 1979; analysis (Table 1) represent all major genera within Goulet, 1992). A phylogenetic hypothesis presented Nematinae, and most subgenera of the large genera. by Ross (1937), although not a formal analysis, was based The missing genera are rare and (near) monotypic on a philosophy of minimizing morphological (Adelomos Ross, Neodineura Taeger, Megadineura changes along the tree (Fig. 1), and later Maxwell Malaise, Katsujia Togashi and Nepionema Benson), or (1955) drew a tree on the basis of larval anatomy. their generic status is disputed (for example, Benson However, the two phylogenies include few nematine genera (1963) and Abe & Smith (1991) consider the Asian and are directly contradictory in the placement of many Moricella Rohwer a synonym of Mesoneura). The largest taxa. missing genus is Kerita Ross, which includes three The purpose of this study was to gain a more robust Nearctic species (Smith, 1976). hylogenetic hypothesis of the subfamily Nematinae. To establish the phylogenetic position of Nematinae, we For this, we used DNA sequence data from the mitochon- included thirteen outgroup taxa that supposedly represent drial cytochrome oxidase I gene and the nuclear different levels of divergence (Table 1). Sterictiphora, elongation factor-1a gene to reconstruct the relationships Diprion and Abia represent three other families from the amongst thirteen outgroup taxa and sixty-eight superfamily Tenthredinoidea (Argidae, Diprionidae and nematine species that represent all tribes and all main Cimbicidae, respectively). Of these, Sterictiphora was used genera within the Nematinae. Maximum parsimony and to root the trees, in accordance with results from phyloge- Bayesian phylogenetic analyses of the sequence data netic analyses by Rasnitsyn (1988), Vilhelmsen (1997), support the monophyly of the subfamily in a broad sense, Ronquist et al. (1999) and Schulmeister (2003). The ten give a relatively well-resolved overall view of the non-nematine tenthredinid species represent all five other nematine radiation, and provide a framework for further subfamilies within the family Tenthredinidae (Taeger & studies. Blank, 1998). All specimens have been deposited as voucher Fig. 1. Ross’s (1937) phylogenetic hypoth- esis of the Tenthredinidae. The subfamily Nematinae (and Cladiinae) is on the lower right-hand side of the tree. # 2006 The Authors Journal compilation # 2006 The Royal Entomological Society, Systematic Entomology, 31, 569–583 # Journal compilation 2006 The Authors Table 1. Taxa and samples used in the study, and collection dates and localities. Classification follows mainly Zhelochovtsev (1988, 1994) and Lacourt (1998, 1999). Ingroup tribes that are para- or polyphyletic are indicated, and tribes that should be lowered to a subtribal rank in order to make Pristiphorini and Nematini monophyletic are given in parentheses (see Fig. 3). Tribe Genus (subgenus) species Sex/stage (host, if larva) Location Date Collector ‘Susaninae’ Susana annulata Smith / Butte County, CA, U.S.A. iv.2002 H. J. Jacobson # (included in ingroup) 2006 The Royal Entomological Society, Hoplocampini Hoplocampa oregonensis (Ashmead) / Elk mtn, BC, Canada 17.vii.2002 T. Nyman (polyphyletic) Hoplocampa marlatti Rohwer / Cambridge, MA, U.S.A. 5.v.2002 T. Nyman Caulocampus acericaulis (MacGillivray) / Aneaster, ON, Canada 17–20.v.1995 B. DeJonge Caulocampus matthewsi Smith / Petersham, MA, U.S.A. 8–15.v.2002 T. Nyman Cladiini Cladius comari Stein ? Mekrija¨rvi, Finland 8.vii.2001 T. Nyman Priophorus pallipes (Serville) Larva, Betula pubescens Laboratory colony, Finland 12.iv.2000 A. Kause Trichiocampus aeneus (Zaddach) Larva, Salix phylicifolia Hausja¨rvi, Finland 2.ix.2001 V. Vikberg Mesoneurini Mesoneura opaca (Fabricius) Larva, Quercus sp. Overijse, Belgium 26.v.2001 J.-L. Boeve´ (polyphyletic) Craterocercus fraternalis (Norton) / Hardy County, WV, U.S.A. 17.4.-3.v.2002 D. R. Smith Pseudodineurini Pseudodineura fuscula (Klug) / Nana Aseme, Estonia 21.4.2002 M. Heidemaa Pseudodineura parva (Norton) ? Petersham, MA, U.S.A. 14–22.v.2002 T. Nyman Endophytus anemones (Hering) Larva, Anemone nemorosa Etzen, Austria 5.v.2002 E. Altenhofer Dineurini Platycampus luridiventris (Falle´n) ? Joensuu, Finland 11.vi.2001 T. Nyman Systematic Entomology Anoplonyx apicalis (Brischke) Larva, Larix sibirica Janakkala, Finland 1.ix.2002 V. Vikberg Dineura virididorsata (Retzius) Larva, Betula pubescens Janakkala, Finland 7.vii.2002 V. Vikberg Hemichroa (Hemichroa) crocea (Geoffroy) Larva, Alnus glutinosa Grimminge, Belgium 4.ix.2002 J.-L. Boeve´ Hemichroa