Systematic Entomology (2015), 40, 570–591 DOI: 10.1111/Syen.12122
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Systematic Entomology (2015), 40, 570–591 DOI: 10.1111/syen.12122 Phylogeny of the parasitic wasp subfamily Euphorinae (Braconidae) and evolution of its host preferences JULIA STIGENBERG1, CHARLES ANDREW BORING2 and FREDRIK RONQUIST3 1Entomology Section, Department of Zoology, Swedish Museum of Natural History, Stockholm, Sweden, 2Department of Recent Invertebrates, Sam Noble Museum of Natural History, Norman, OK, U.S.A. and 3Department of Bioinformatics and Genetics, Swedish Museum of Natural History, Stockholm, Sweden Abstract. The braconid subfamily Euphorinae is a large, cosmopolitan group of endoparasitoid wasps. The majority of species attack adult hosts, a strategy that is rare among parasitic wasps, but there are also many species that attack nymphs and larval stages. Euphorine hosts may belong to a variety of insect orders (Coleoptera, Hemiptera, Hymenoptera, Neuroptera, Psocoptera, Orthoptera and Lepidoptera) although most euphorine tribes are confined to Coleoptera. Here we investigate the phylogenetic relationships of the Euphorinae based on molecular data (3 kb of nucleotide data from four markers: 18S, 28S, CAD and COI) and propose a higher-level classification based upon the resulting phylogeny. We also infer the evolution of host associations and discuss the diversification of the Euphorinae. Results from both Bayesian inference and maximum-likelihood analysis show that the subfamily, as previously circumscribed, is paraphyletic. We propose that the subfamily be expanded to include the tribes Meteorini and Planitorini (Mannokeraia + Planitorus), so that it corresponds to a clade that is strongly supported as monophyletic in our analyses. Based on our results, a revised higher classification of the Euphorinae is proposed, in which 52 extant genera and 14 tribes are recognized. We reinstate the genus Microctonus belonging to the tribe Perilitini, and synonymize Ussuraridelus with Holdawayella, Sinuatophorus with Eucosmophorus. Furthermore, we propose the following tribal rearrangements: Spathicopis and Stenothremma are transferred to Perilitini; Tuberidelus, Eucosmopho- rus and Plynops to Cosmophorini; Ecclitura to Dinocampini; Chrysopophthorus, Holdawayella and Wesmaelia to Helorimorphini; Proclithroporus and Heia to Towne- silitini. The monotypic tribe Cryptoxilonini is synonymized with Cosmophorini. The genera Pygostolus and Litostolus are placed in a separate tribe, Pygostolini, previously recognized as a subtribe among the Centistini. Parsimony-based ancestral state recon- structions suggest that the ancestor of Euphorinae was a parasitoid of lepidopteran larvae, and that a host shift to larval Coleoptera occurred only in one clade of the Meteorini, some members of which secondarily shifted back to larval lepidopteran hosts. In the remainder of the subfamily, there was an initial shift from larval to adult coleopterans, followed by subsequent shifts to adults or larvae of Hemiptera, Hymenoptera, Neuroptera, Orthoptera and Psocoptera. Introduction nymphal and larval stages, especially when they co-occur with adults in the same habitat (Obrycki et al., 1985; Shaw, 1985). Parasitoid wasps rarely attack adult hosts, but this is the predom- The diversity of euphorine hosts is exceptional, including rep- inant mode of parasitism among the Euphorinae (Hymenoptera: resentatives from seven different orders of insects: Coleoptera, Braconidae). Target hosts of the Euphorinae also include Hemiptera, Hymenoptera, Neuroptera, Orthoptera, Psocoptera and Lepidoptera (Shaw, 1988; Chen & van Achterberg, 1997). Correspondence: Julia Stigenberg, Swedish Museum of Natural A robust phylogeny of the Euphorinae is most desirable in order History, P.O. Box 50007, SE-10405 Stockholm, Sweden. E-mail: [email protected] 570 © 2015 The Authors. Systematic Entomology published by John Wiley & Sons Ltd on behalf of The Royal Entomological Society. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. Phylogeny of the Euphorinae 571 to understand transitions in host associations. This would bring based on data from four gene regions (18S, CAD, 28S and COI), insight into the origin of adult parasitism and further transitions and the dataset includes representatives from 42 of the 49 cur- in host associations within this group. rently recognized extant genera (Yu & van Achterberg, 2011). Shaw (1985) presented a tribal classification for 37 euphorine Based on the results, we propose a revised higher-level classifi- genera following a phylogenetic analysis of 68 external morpho- cation of the Euphorinae. We also map host preferences onto the logical characters. In his PhD dissertation, McDonald (2001) euphorine phylogeny and discuss the evolutionary implications. re-evaluated the morphological characters and the cladistic methods used by Shaw and proposed a new phylogeny. Although the results had important implications for euphorine classifica- Materials and methods tion, the dissertation was never published and the work went largely unnoticed. Since 1985, 23 additional genera or subgen- Taxon sampling era have been described and placed in the Euphorinae. As the known diversity has expanded, a need has arisen for a reclassifi- A total of 217 taxa were sampled out of which 16 species cation of the Euphorinae genera. Since Shaw’s revision, most of represented outgroups (Table S1). Two additional taxa (Asia- the new insights into the phylogenetic relationships of Euphori- centistes sp. and Tainiterma sp.) were initially considered part nae have come from molecular analyses of higher-level rela- of the ingroup, but were shown in the analysis to belong to tionships in the Ichneumonoidea or Braconidae (Dowton et al., the outgroup. The taxon sampling of the ingroup comprised 1998; Belshaw et al., 2000; Belshaw & Quicke, 2002; Dowton representatives from 52 genera, including exemplars of sev- et al., 2002; Li et al., 2003; Shi et al., 2005; Pitz et al., 2007; Sha- eral subgenera (Table S1). All tribes within the Euphorinae ranowski et al., 2011). The results from these studies have shown were represented. Several included genera have never before dramatically different results with respect to tribal and inter- been incorporated in a molecular analysis: Allurus, Asiacentistes generic relationships of the Euphorinae. This is not surprising (see discussion regarding placement), Betelgeuse, Bracteodes, because the scope of those studies included only a few of the 49 Centistina, Cryptoxilos, Heia, Litostolus, Mama, Myiocephalus, recognized, extant genera of Euphorinae. The most recent phy- Napo, Plynops, Proclithrophorus, Rilipertus, Eucosmophorus, logeny of the Braconidae by Sharanowski et al. (2011) showed Spathicopis, Stenothremma, Syntretellus, Tainiterma (see dis- ≥ high support [posterior probability (PP) 0.95] for the mono- cussion regarding placement), Townesilitus, Tuberidelus and phyly of the euphoroid complex in all their concatenated anal- Holdawayella. yses. The euphoroid complex (sensu Sharanowski et al., 2011) The inclusion of Cenocoelini, Ecnomios, Mannokeraia and includes, in addition to Euphorinae, also the subfamilies Ceno- Planitorus in our analysis was based on the results of Shara- coelinae, Ecnomiinae, Neoneurinae and Meteorinae, the latter nowski et al. (2011). The Meteorini are heavily represented in two of which are sometimes treated as tribes within the Euphori- our dataset due to the availability of material and sequences nae. This study includes additional representatives to further test (Stigenberg & Ronquist, 2011), as well as to the ambiguous the monophyly of the euphorid complex. placement of Meteorini in previous analyses (Dowton et al., The uncertainty concerning phylogenetic relationships is 1998; Belshaw et al., 2000; Belshaw & Quicke, 2002; Dowton reflected in disagreement with respect to the classification. The et al., 2002; Shi et al., 2005; Pitz et al., 2007; Sharanowski et al., lineage including Meteorus and Zele is recognized by many 2011), either at the base of Braconidae or at other various posi- authors as a separate subfamily, the Meteorinae (Shaw, 1985, tions within Braconidae. 1988, 2004; Maeto, 1990; Shaw & Huddleston, 1991; Hanson Outgroups included 11 braconid and 5 ichneumonid taxa. Due & Gauld, 1995; Wharton et al., 1997; Zitani et al., 1998; Li to the placements of Asiacentistes and Tainiterma in preliminary et al., 2003), but many others treat it among the Euphorinae as analyses we included several possible sister taxa to stabilize their the tribe Meteorini (Huddleston & Short, 1978; van Achterberg, placement: Cenocoelius (three spp.; Cenocoelinae), Blacus (two 1984; Chen & van Achterberg, 1997; Belokobylskij, 2000b; Sti- spp.) and Diospilus (Brachistinae), Wroughtonia (Helconinae) genberg & Ronquist, 2011). Both classifications may well be and Homolobus (Homolobinae). We also included several dif- consistent with the true phylogeny; there is little argument that ferent ichneumonids as well as several cyclostome braconids as the Meteorus + Zele lineage either forms the sister-group to the a more functional outgroup to help root the tree. Euphorinae or a basal clade inside the Euphorinae. If the for- mer is true, then the decision on the subfamily or tribal status of the lineage is simply subjective, reflecting the author’s views of how the morphological and biological