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Revision of the European Lysiphlebus Species (Hymeno- Ptera: Braconidae: Aphidiinae) on the Basis of COI and 28SD2 Molecular Markers and Morphology

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Revision of the European Lysiphlebus Species (Hymeno- Ptera: Braconidae: Aphidiinae) on the Basis of COI and 28SD2 Molecular Markers and Morphology 76 (2): 179 – 213 18.7.2018 © Senckenberg Gesellschaft für Naturforschung, 2018. Revision of the European Lysiphlebus species (Hymeno- ptera: Braconidae: Aphidiinae) on the basis of COI and 28SD2 molecular markers and morphology Željko Tomanović *, 1, Milana Mitrović 2, Andjeljko Petrović 1, Nickolas G. Kavallieratos 3, Vladimir Žikić 4, Ana Ivanović 1, Ehsan Rakhshani 5, Petr Starý 6 & Christoph Vorburger 7 1 University of Belgrade - Faculty of Biology, Institute of Zoology, Studentski trg 16, 11000 Belgrade, Serbia; Željko Tomanović * [ztoman@ bio.bg.ac.rs]; Andjeljko Petrović [[email protected]]; Ana Ivanović [[email protected]] — 2 Institute for Plant Protection and Environ- ment, Department of Plant Pests, Banatska 33, 11000 Belgrade, Serbia; Milana Mitrović [[email protected]] — 3 Agricultural University of Athens, Department of Crop Science, Laboratory of Agricultural Zoology and Entomology, 75 Iera Odos str., 11855 Athens, Greece; Nickolas G. Kavallieratos [[email protected]] — 4 University of Niš, Faculty of Sciences and Mathematics, Department of Bi- ology and Ecology, Višegradska 33, 18000 Niš, Serbia; Vladimir Žikić [[email protected]] — 5 Department of Plant Protection, College of Agriculture, University of Zabol, Zabol, P.O. Box: 98615–538, I.R. Iran; Ehsan Rakhshani [[email protected]] — 6 Institute of Entomol- ogy, Biology Centre, Laboratory of Aphidology, AVCR, Branišovska 31, 370 05 České Budějovice, Czech Republic; Petr Starý [[email protected]. cz] — 7 Institute of Integrative Biology, ETH Zürich, and EAWAG, Swiss Federal Institute of Aquatic Science and Technology, Überlandstraße 133, 8600 Dübendorf, Switzerland; Christoph Vorburger [[email protected]] — * Corresponding author Accepted 02.iii.2018. Published online at www.senckenberg.de/arthropod-systematics on 29.vi.2018. Editors in charge: Christian Schmidt & Klaus-Dieter Klass Abstract. Members of the genus Lysiphlebus Foerster are medium-sized endoparasitoid aphidiine wasps with over 30 species distributed worldwide. They attack numerous aphid hosts, and some species are important biological control agents. All European Lysiphlebus species are revised based on sequence information from the mitochondrial COI barcoding gene and the nuclear 28SD2 gene, morphological traits, and on information about their host specifcity. The taxonomic status of 13 European Lysiphlebus species is confrmed, while 11 are rede- scribed and illustrated. The following four Lysiphlebus species are synonymized: L. melandriicola Starý, 1961 [= L. fabarum (Marshall, 1896)], L. hirtus Starý, 1985 (= L. confusus Tremblay & Eady, 1978), L. hispanus Starý, 1973 (= L. desertorum Starý, 1965), and L. safavii Starý, 1985 (= L. hirticornis Mackauer, 1960). Two new Lysiphlebus species are described: L. volkli sp.n. and L. brachycaudi sp.n. Our results, based on both COI and 28SD2, confrm the existence of three monophyletic species groups within the genus: (1) the ‘fabarum’ group, which includes L. fabarum, L. cardui (Marshall, 1896), L. confusus, L. hirticornis, L. brachycaudi sp.n., and L. volkli sp.n.; (2) the ‘testaceipes’ group, which includes L. testaceipes (Cresson, 1880), L. orientalis Starý & Rakhshani, 2010, L. fritzmuelleri Mackauer, 1960, L. balcanicus Starý, 1998, L. desertorum, [and probably L. dissolutus (Nees, 1811)]; and (3) the ‘alpinus’ group, consisting solely of L. alpinus Starý, 1971. Geometric morphometrics of fore wing shape proved to be a powerful tool to delineate sibling species within the ‘fabarum’ group. We were able to confrm for the frst time sexual lines of L. cardui and L. confusus. Furthermore, an additional potentially asexual Lysiphlebus taxon in Europe is revealed based on the discovery of an asexual line of L. volkli sp.n. in Iran. An illustrated key for identifcation of the European Lysiphlebus species is provided. Key words. Lysiphlebus, Europe, phylogeny, barcoding, revision, L. volkli sp.n., L. brachycaudi sp.n. 1. Introduction With more than 30 species around the world, Lysiphle­ 1961, 1975). The diversity of this genus has been best ex- bus Foerster, 1862, represents a moderately species-rich plored in Europe, where 14 species have been described genus of solitary endoparasitoid aphidiine wasps (STARÝ (KAVALLIERATOS et al. 2004; STARÝ 2006; VAN ACHTERBERG ISSN 1863-7221 (print) | eISSN 1864-8312 (online) 179 Tomanović et al.: Revision of the European Lysiphlebus species 2013); in Asia, where eight species have been described There are serious doubts about the taxonomic status (STARÝ 1965, 1979; TAKADA 1968); and in America (North of some Lysiphlebus species inhabiting Europe. This and South), where fve species have been described (PIKE primarily applies to the L. fabarum species group (i.e., et al. 2000). In contrast, the African fauna has been poor- L. fabarum, L. confusus, L. cardui) and other European ly explored, and only two imported species are known Lysiphlebus spp. (i.e., L. hirtus, L. safavii, L. melandrii­ in Australia (CARVER & FRANZMANN 2001). Lysiphlebus cola) because they show little genetic differentiation when spp. attack mostly small aphid hosts from various genera analysed using several molecular markers (BELSHAW et al. (e.g., Aphis L., 1758, Brachycaudus van der Goot, 1913). 1999; SANDROCK et al. 2011) and also exhibit weak and Interestingly, most of the European species are strictly inconsistent morphological differentiation (STARÝ 1961, monophagous or exhibit narrow oligophagous host speci- 1985). For some species (e.g., L. safavii and L. hirtus), fcity (i.e., L. fritzmuelleri Mackauer, 1960, L. hirticornis only the type material is available, without any additional Mackauer, 1960, L. balcanicus Starý, 1998, L. hispanus records for many years after the original description (VAN Starý, 1973, L. safavii Starý, 1985, L. hirtus Starý, 1985, ACHTERBERG 2013). The restricted number of diagnostic L. melandriicola Starý, 1961, L. alpinus Starý, 1971), morphological characters in Lysiphlebus taxonomy com- while the host specifcity of members of the L. fabarum bined with existing sympatric asexual and sexual lines group ranges from oligophagous to broadly oligophagous in several species (SANDROCK et al. 2011; Petrović et al. [i.e., L. fabarum (Marshall, 1896), L. confusus Tremblay 2015) make Lysiphlebus a taxonomically and biologi- & Eady, 1978, L. cardui (Marshall, 1896)]. For exam- cally very complex group. There is a long history of dif- ple, L. fabarum is recorded from over 150 aphid species ferent opinions concerning the taxonomic position of the (KAVALLIERATOS et al. 2004; STARÝ 2006; RAKHSHANI et genus Adialytus Foerster and its relationships with Lysi­ al. 2013). As in the case of native European species, in phlebus. Some authors treated Adialytus as a subgenus of North and South America some species such as L. favi­ Lysiphlebus (STARÝ 1975; TREMBLAY & EADY 1978) or a dus (Gahan, 1911) and L. utahensis (Smith, 1944) have separate genus, due to the more reduced fore wing vena- a very narrow host range (PIKE et al. 2000), while others tion and host range pattern mainly restricted to Chaito- like L. testaceipes (Cresson, 1880) are broadly oligopha- phorinae and Thelaxinae aphid hosts (MACKAUER 1968; gous. Meanwhile, L. testaceipes has become a cosmo- MARSH 1971; MESCHELOFF & ROSEN 1990; STARÝ 2005; politan species and parasitizes approximately 100 aphid RAKHSHANI et al. 2012). Lysiphlebus species are common species (PIKE et al. 2000). model organisms in evolutionary and ecological research Lysiphlebus fabarum and L. testaceipes parasitize (VÖLKL 1994; NYABUGA et al. 2010; ROUCHET & VORBUR­ many pest aphids in vegetable crops, orchards, legumi- GER 2014), with apparent biocontrol importance and good nous plants, cereal crops and ornamental plants (KAV­ prospects for mass production and use in biological con- ALLIERATOS et al. 2004, 2010, 2013; BENELLI et al. 2016; trol programs (STARÝ et al. 1988a,b; HAGVAR & HOFSVANG KAVALLIERATOS et al. 2016; Yu et al. 2016). Also, it is well 1991; BENELLI et al. 2016), but they have surprisingly known that L. testaceipes was introduced from Cuba to rarely been taxonomically investigated. We agree with the Mediterranean part of France for the control of cit- the assertion of the “unsatisfactory nature of the current rus aphids (STARÝ 1988a). In addition, L. testaceipes classifcation” by BELSHAW et al. (1999), since there are parasitizes some new exotic immigrants in Europe, only a few old revisionary and taxonomic studies devot- viz., the grapevine aphid, Aphis illinoisensis Shimer, ed to Lysiphlebus (MACKAUER 1960; STARÝ 1961, 1975). 1866 (HAVELKA et al. 2011) and Siphonatrophia cupressi Over the last decades, only a few studies have contained (Swain, 1918) on plants of the family Cupressaceae (RA­ descriptions of new species (STARÝ 1971, 1985; STARÝ & BASSE et al. 2005). The recently described L. orientalis REMAUDIÈRE 1973; STARÝ et al. 1998; STARÝ et al. 2010) from China represents a good candidate for mass releases or dealt with species groups within the genus Lysiphlebus on soybean crops in the USA against the soybean aphid, (RAKHSHANI et al. 2013; STARÝ et al. 2014; Petrović et al. Aphis glycines Matsumura, 1917 (RAGSDALE et al. 2011). 2015; PARREÑO et al. 2017). Lysiphlebus orientalis has been recently recorded in Eu- The objectives of the present study were as follows: rope (Serbia), where it is involved in several new aphid- (i) to resolve the taxonomic status of several species that plant associations and has adopted new aphid hosts in belong to
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