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Tribal Classification and Phylogeny of Geometrinae (Lepidoptera

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Tribal Classification and Phylogeny of Geometrinae (Lepidoptera Zoological Journal of the Linnean Society, 2018, 184, 653–672. With 2 figures. Tribal classification and phylogeny of Geometrinae Downloaded from https://academic.oup.com/zoolinnean/article-abstract/184/3/653/4996193 by Institute of Zoology, CAS user on 05 November 2018 (Lepidoptera: Geometridae) inferred from seven gene regions XIAOSHUANG BAN1,2,†, NAN JIANG1,†, RUI CHENG1,†, DAYONG XUE1 AND HONGXIANG HAN1,* 1Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, No. 1 Beichen West Road, Chaoyang District, Beijing 100101, China 2University of Chinese Academy of Sciences, 19A Yuquan Road, Shijingshan District, Beijing 100049, China Received 30 September 2017; revised 18 January 2018; accepted for publication 27 February 2018 Despite recent progress in the molecular systematics of Geometridae, phylogenetic relationships within the sub- family Geometrinae remain largely unexplored. To infer the relationships among tribes, we performed a molecular phylogenetic analysis of Geometrinae based on 116 species representing 17 of the 18 recognized tribes, mainly from the Palaearctic and Oriental regions. Fragments of one mitochondrial and six nuclear genes were sequenced, yielding a total of 5805 bp of nucleotide data. Maximum likelihood and Bayesian analyses yielded largely congruent results. The monophyly of Geometrinae and most recognized tribes is supported. We present a new phylogenetic classifica- tion for Geometrinae composed of 13 tribes, two of which are proposed here as new: Ornithospilini trib. nov. and Agathiini trib. nov. A broad concept of Hemitheini is presented by the inclusion of nine subtribes, with Thalerini as a new synonym of Hemitheiti. The close relationship among Nemoriini, Synchlorini and Comibaenini, and the sister relationship between Timandromorphini and Geometrini is well supported. Monophyly of the genera Maxates, Berta, Lophophelma, Dooabia, Geometra and Tanaorhinus was found not to be supported. Hethemia syn. nov. is synonymized with Thalera, and six new combinations and two revised statuses are proposed. ADDITIONAL KEYWORDS: Insecta – molecular phylogeny – new taxa – revision. INTRODUCTION The subfamily Geometrinae, commonly known as emerald moths, is the third largest subfamily in Geometridae is one of the three most species-rich fami- Geometridae, with more than 2500 described spe- lies of Lepidoptera, with approximately 23 000 described cies in 268 genera worldwide (Scoble & Hausmann, species (Scoble, 1999; Scoble & Hausmann, 2007). 2007). Geometrinae is particularly diverse in trop- Caterpillars of this family are known as loopers or inch- ical areas, and the caterpillars mainly feed on various worms because of their looping gait, due to a reduced trees and shrubs (Pitkin, 1996). Holloway (1996) and number of abdominal prolegs. Geometridae has long Pitkin (1996) summarized the main defining charac- attracted the interest of dedicated researchers at leading ters of Geometrinae, among which the predominance institutions around the world, and much progress has of green pigment (geoverdin) is synapomorphic with been made towards a better understanding of geometrid Geometrinae (Cook et al., 1994) and the shape of the taxonomy and systematics (Pitkin, Han & James, 2007). ansa of the tympanal organ supports the monophyly of Geometrinae (Hausmann, 2001). The other characters *Corresponding author. E-mail: [email protected] are: wings are mostly green in colour, the frenulum †Xiaoshuang Ban, Nan Jiang and Rui Cheng contributed equally to the present paper. tends to be reduced, the third sternite of the male often [Version of Record, published online 15 May 2018; possesses a pair of setal patches, the socii of the male http://zoobank.org/urn:lsid:zoobank.org:pub:D2792250- genitalia are usually well developed, the vinculum is B5CA-4917-A2EA-EBCBE1B42E70] distally cruciform in structure, the sclerotization of the © 2018 The Linnean Society of London, Zoological Journal of the Linnean Society, 2018, 184, 653–672 653 654 X. BAN ET AL. aedeagus is usually reduced to a ventral strip along Geometrini. Pitkin (1996), Hausmann (1996) and Han its length, and the female genitalia have oblique and & Xue (2011a) raised Holloway’s subtribes to the tribal papillate ovipositor lobes and a bicornute signum. level. Hausmann (1996) recognized 15 tribes and Forum Both Hausmann (2001) and Han & Xue (2011a) men- Herbulot (2007) recognized 18 tribes for Geometrinae on tioned venation characters: forewing usually without a global basis. However, some tribal concepts remain con- Downloaded from https://academic.oup.com/zoolinnean/article-abstract/184/3/653/4996193 by Institute of Zoology, CAS user on 05 November 2018 an areole, hindwing with vein M2 close to M1 and far troversial. For example, Holloway (1996) favoured a wide from M3. Beljaev (2008) summarized 12 apomorphies concept of Hemitheini embracing Thalerini, Comostolini, of Geometrinae by adding the results of his study of Hemistolini, Jodini and Thalassodini, whereas these taxa the skeleto-muscular system of the male genitalia. were treated as valid tribes by Hausmann (1996, 2001). Since very early studies, the subfamily Geometrinae Later, Thalassodini were synonymized with Hemistolini in has been considered a natural entity; it was treated as Hausmann et al. (2016b). Beljaev (2016) proposed a much Group I in Lederer (1853), as Geometridae in Meyrick wider concept of Hemitheini by adding Rhomboristini (also (1892), as Geometrinae in Hampson (1895) and as Lophochoristini) and Microloxiini (also Hierochthoniini). Hemitheinae in Prout (1912, 1912–16, 1920–41). The The most likely reason for these controversies is that these monophyly of Geometrinae is also well supported by systematic concepts were mainly drawn from morpho- later molecular studies, such as those of Yamamoto & logical overviews and not based on phylogenetic analysis, Sota (2007) and Sihvonen et al. (2011). Holloway (1997) although they sometimes utilized phylogenetic hints. provided the first tentative phylogeny for Geometridae, The first morphology-based topology of Geometrinae which was established mostly based on characters of the was presented by Viidalepp (1981), who used vari- adult male and female abdomen, and showed a sister ous calculations to divide 26 genera into ten tribes relationship between Geometrinae and Desmobathrinae. based on 12 multi-state characters, erected the tribe Yamamoto & Sota (2007) found that Geometrinae was a Archaeobalbini and placed Pseudoterpnini sensu sister-group to Oenochrominae. In the molecular phylo- Herbulot, 1963 under Terpnini sensu Inoue, 1961 as a genetic analysis of Sihvonen et al. (2011), Oenochrominae subtribe. Stekolnikov & Kuznetzov (1981) presented s.s. or Oenochrominae s.s. + Desmobathrinae was consid- two supertribes, Geometridii and Comibaenidii, based ered a sister-group to Geometrinae with weak support. on the functional morphology of the male genitalia of Considerable progress has been made in systematics ten geometrid species; the former included Geometrini, within Geometrinae. The major global taxonomic revi- Ochrognesiini, Hemitheini and Hemistolini, and the lat- sion of Geometrinae was that of Prout (1912, 1934–38). ter included only Comibaenini. Cook (1993) conducted Subsequently, many regional works on Geometrinae the first cladistic analysis based on 45 geometrine gen- have been produced: Forbes (1948), Ferguson (1969, era and 24 multistate characters. Although he stated 1985) and McGuffin (1988) studied the Geometrinae that his dataset was insufficient to resolve the phyl- of North America, Inoue (1961) reviewed the Japanese ogeny of Geometrinae, the topology still showed that Geometrinae, Pitkin (1996) researched the neotropical many known tribes (such as Thalassodini, Hemitheini, Geometrinae, Holloway (1996) reviewed the Bornean Thalerini, Jodini, Hemistolini, Comostolini, Synchlorini Geometrinae, Hausmann (1996, 2001) investigated and Nemoriini) were grouped in one superclade, which Geometrinae from the Levant and neighbouring coun- somewhat supports some of the morphological results tries and Europe, McQuillan & Edwards (1996) studied mentioned above. Han (2005) conducted a preliminary Australian Geometrinae, Viidalepp (1996) produced a cladistic analysis of the tribe Geometrini, based on 71 checklist of Geometridae from the USSR and erected morphological characters, and found that the mono- a new tribe, Hierochthoniini, Han & Xue (2011a) stud- phyly of Geometra Linnaeus was doubtful, since the spe- ied Chinese representatives, Hausmann, Parisi & cies were clustered in several different clades, and the Sciarretta (2014) and Hausmann, Sciarretta & Parisi phylogenetic relationships among genera were unclear. (2016b) reviewed the Ethiopian Geometrinae (Parts The rapid development of DNA sequencing tech- I and II) and Beljaev (2016) published a catalogue of niques has accelerated the molecular phylogenetic Geometrinae in the insects of the Russian Far East. analysis of Geometridae (Abraham et al., 2001; Young, Almost all of these researchers allocated genera of 2006; Snäll et al., 2007; Yamamoto & Sota, 2007; Geometrinae to tribes or groups. However, due to the lack Õunap, Viidalepp & Saarma, 2008; Strutzenberger of a global review, there is no consensus regarding the sys- et al., 2010; Wahlberg et al., 2010; Õunap et al., 2011; tematic placement of tribes and groups within Geometrinae Sihvonen et al., 2011; Õunap, Viidalepp & Truuverk, and no clear understanding of the relationships between
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