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A Molecular Phylogeny of the Palaearctic and O.Pdf CSIRO PUBLISHING Invertebrate Systematics, 2017, 31, 427–441 http://dx.doi.org/10.1071/IS17005 A molecular phylogeny of the Palaearctic and Oriental members of the tribe Boarmiini (Lepidoptera : Geometridae : Ennominae) Nan Jiang A,D, Xinxin Li A,B,D, Axel Hausmann C, Rui Cheng A, Dayong Xue A and Hongxiang Han A,E AKey Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, No. 1 Beichen West Road, Chaoyang District, Beijing 100101, China. BUniversity of Chinese Academy of Sciences, 19A Yuquan Road, Shijingshan District, Beijing 100049 China. CSNSB – Zoologische Staatssammlung München, Münchhausenstraße 21, Munich 81247, Germany. DThese authors contributed equally to this work. ECorresponding author. Email: [email protected] Abstract. Owing to the high species diversity and the lack of a modern revision, the phylogenetic relationships within the tribe Boarmiini remain largely unexplored. In this study, we reconstruct the first molecular phylogeny of the Palaearctic and Oriental members of Boarmiini, and infer the relationships among tribes within the ‘boarmiine’ lineage. One mitochondrial (COI) and four nuclear (EF-1a, CAD, RpS5, GAPDH) genes for 56 genera and 96 species of Boarmiini mostly from the Palaearctic and Oriental regions were included in the study. Analyses of Bayesian inference and maximum likelihood recovered largely congruent results. The monophyly of Boarmiini is supported by our results. Seven clades and seven subclades within Boarmiini were found. The molecular results coupled with morphological studies suggested the synonymisation of Zanclopera Warren, 1894, syn. nov. with Krananda Moore, 1868. The following new combinations are proposed: Krananda straminearia (Leech, 1897) (comb. nov.), Krananda falcata (Warren, 1894) (comb. nov.), and Krananda fulva (Yazaki, 1994) (comb. nov.).Our results also supported themonophyly of the ‘boarmiine’ lineage. Boarmiini were recovered as sister to the remaining taxa within the ‘boarmiine’ lineage, and Macariini were recovered as sister to Abraxini, Eutoeini and Cassymini. Additional keywords: ‘boarmiine’ lineage, new combinations, new synonym, systematics, taxonomy. Received 11 January 2017, accepted 10 March 2017, published online 23 June 2017 Introduction Holloway (1994, 1997)andBeljaev(2006a, 2006b, 2016) The geometrid subfamily Ennominae is the largest subfamily of proposed a morphology-based hypothesis about the tribal Geometridae, which contains over 10 000 described species system of the Ennominae. However, the tribal relationships placed in approximately 1100 genera (Scoble 1999; Pitkin within the Ennominae are poorly understood in all present 2002; Scoble and Hausmann 2007). The monophyly of the studies (Skou and Sihvonen 2015). Ennominae is well supported by recent morphological and Boarmiini is the most species-rich tribe within the molecular studies (Wahlberg et al. 2010; Sihvonen et al. 2011; ‘boarmiine’ lineage, currently comprising more than 150 Skou and Sihvonen 2015). Within Ennominae, the tribes can be genera and 5000 species globally, mainly distributed across divided into two groups based on the structure of the pupal the Palaearctic and Oriental biogeographic regions (Wehrli cremaster: the ‘boarmiine’ lineage including Boarmiini, 1938–1954; Holloway 1994; Scoble 1999; Pitkin 2002; Scoble Macariini, Abraxini, Eutoeini, Cassymini (cremaster with setae and Hausmann 2007). D1,SD1 and L1 reduced, D2 fused into a stem) and the ‘ennomine’ Some species of the tribe are polyphagous, but others are lineage including Baptini, Caberini, Ennomini, Ourapterygini highly specialised (Holloway 1994). Many species of Boarmiini and so on (cremaster with setae D1,SD1,L1 and D2 present, D2 are considered serious crop or forest pests, such as Ascotis separated) (Forbes 1948; McGuffin 1977; Viidalepp et al. selenaria (Denis & Schiffermüller, 1775), Biston panterinaria 2007). This morphology-based hypothesis was later supported (Bremer & Grey, 1853) and Ectropis obliqua (Prout, 1915). by some recent molecular studies (Viidalepp et al. 2007;Wahlberg Several morphological characters have been used to define et al. 2010;Õunapet al. 2011; Sihvonen et al. 2011). In addition, Boarmiini: the male forewing usually has a fovea; the male Journal compilation Ó CSIRO 2017 www.publish.csiro.au/journals/is 428 Invertebrate Systematics N. Jiang et al. abdomen usually has a transverse comb of setae on the third sequence data from seven nuclear and one mitochondrial loci, sternite; in the male genitalia, the uncus is usually tapered and and showed that the Boarmiini were characterised by polytomies triangular; the socii are usually weak or absent; the cucullus of resulting from a rapid radiation. In addition, little phylogenetic the valva is usually well developed and strongly covered with signal was found in their morphological study. Considering the setae; the sacculus often has sclerotised structures; a pair of recent progress in understanding the higher-level systematics of cristae is often well developed, consisting of dense tufts in the other groups of Lepidoptera (e.g. Sihvonen et al. 2011, 2015; anellus, near the base of the valva; the coremata are usually not Zahiriet al. 2011, 2012, 2013;Regieret al. 2015; Wang et al. 2015; developed; the signum of the female genitalia is variable Rota et al. 2016;Õunapet al. 2016), it is clear that molecular (Holloway 1994; Pitkin 2002; Young 2008). However, no characters are a valuable tool for resolving the phylogeny of the universal character has been identified that uniquely defines Boarmiini (Wahlberg et al. 2010). the tribe (Holloway 1994; Pitkin 2002). In addition, the delimitation and taxonomic positions of The genus Boarmia Treitschke, 1825 was established some genera of Boarmiini have remained unclear. For example, based on Geometra roboraria Schiffermüller, 1775 from a recent morphological study has indicated that Zanclopera Austria, which was designated as the type species by Warren, 1894 may be a synonym of Krananda Moore, 1868 Duponchel (1829). The genus Hypomecis Hübner, 1821 was (Holloway 1994). established based on Cymatophora umbrosaria Hübner, 1813 Our main goal here is to test the monophyly and composition from North America. Later, Boarmia was considered as a of Boarmiini, examine the relationships among some genera of synonym of Hypomecis by Inoue (1982a, 1982b). Hampson Boarmiini from the Palaearctic and Oriental regions and test (1895) presented a wider concept of Boarmia, and included 27 hypotheses regarding the groups previously proposed within genera from India. Pierce (1914) treated this group as Boarmiinae, the tribe, to infer the relationships among tribes within the and illustrated the genitalia of 10 genera and 17 species from the ‘boarmiine’ lineage. These results, taken together, will provide British Islands. Prout (1912–1916) mainly followed Hampson’s the first basis for a thorough revision of the classification of treatment, and divided Palaearctic Boarmia into eleven sections, Boarmiini, and a phylogenetic framework for studying the mainly based on the male antennae and the wing venation. evolutionary history of Boarmiini species. Wehrli (1938–1954) considered Prout’s sections as subgenera and described nine new subgenera on the basis of external Materials and methods characters and the male genitalia. Later, many subgenera were Taxon sampling raised to generic rank (e.g. Inoue 1956, 1982a, 1982b; Herbulot ‘ ’ 1963). McGuffin(1977) gave a detailed description of 17 genera A total of 111 species from 67 genera of the boarmiine lineage of Nearctic Boarmiini, and presented the first graphic illustration were included for this study, covering all the tribes previously ‘ ’ of a hypothesis on the phylogeny of Boarmiini based on the included within the boarmiine lineage. This sample includes morphological characters of the immature stages and adults. Sato 27 species from 24 genera that had been used previously for (1984) carried out a taxonomic study on the genus Hypomecis constructing the phylogenies of Wahlberg et al. (2010) and and its allied genera from Japan. He divided 27 genera of Sihvonen et al.(2011). The present study is restricted to Boarmiini into six genus-groups based on the characters of egg, Palaearctic and Oriental samples, with a few exceptions. The larva, pupa and adults. Pitkin (2002) reviewed the Neotropical tribe Boarmiini is represented by 96 species assigned to 56 genera of the Ennominae, and 20 genera were included in genera, Macariini by three genera and three species, Cassymini fi fi Boarmiini. Recently, many new genera and species of Boarmiini by ve genera and ve species, Eutoeini by two genera and four were described from the Oriental region (Sato 1995a, 1995b, 1996, species, and Abraxini by one genus and three species. The 1999, 2002, 2005, 2008, 2013, 2014, 2016; Sato and Wang 2004, outgroup included 10 species from 10 genera, among them six 2005, 2006, 2007, 2016;SatoandFu2010). species from Gnophini, one species from Ourapterygini, one Holloway (1994) proposed a broad concept of the tribe species from Ennomini, and two species from Geometrinae. Boarmiini, including the taxa Amphidasini, Ascotini, Bistonini, A list of taxa with the collecting localities, voucher codes and Braccini, Bupalini, Cheimatobiini, Cleorini, Eubyjini, Gnophini, GenBank accession numbers is provided in Table 1. Hyberniini, Melanolophini, Milioniini, Selidosemini, Sionini and fi Theriini. The broad concept was supported by the morphological DNA extraction, ampli cation and
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