Tribal classification and phylogeny of Geometrinae (Lepidoptera: Geometridae) inferred from seven gene regions

Tribal classification and phylogeny of Geometrinae (Lepidoptera: Geometridae) inferred from seven... Abstract Despite recent progress in the molecular systematics of Geometridae, phylogenetic relationships within the subfamily 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 classification 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. © 2018 The Linnean Society of London, Biological Journal of the Linnean Society, 2018, XX, 000–000 Insecta, molecular phylogeny, new taxa, revision INTRODUCTION Geometridae is one of the three most species-rich families of Lepidoptera, with approximately 23000 described species (Scoble, 1999; Scoble & Hausmann, 2007). Caterpillars of this family are known as loopers or inchworms because of their looping gait, due to a reduced number of abdominal prolegs. Geometridae has long attracted the interest of dedicated researchers at leading institutions around the world, and much progress has been made towards a better understanding of geometrid taxonomy and systematics (Pitkin, Han & James, 2007). The subfamily Geometrinae, commonly known as emerald moths, is the third largest subfamily in Geometridae, with more than 2500 described species in 268 genera worldwide (Scoble & Hausmann, 2007). Geometrinae is particularly diverse in tropical areas, and the caterpillars mainly feed on various trees and shrubs (Pitkin, 1996). Holloway (1996) and Pitkin (1996) summarized the main defining characters of Geometrinae, among which the predominance of green pigment (geoverdin) is synapomorphic with Geometrinae (Cook et al., 1994) and the shape of the ansa of the tympanal organ supports the monophyly of Geometrinae (Hausmann, 2001). The other characters are: wings are mostly green in colour, the frenulum tends to be reduced, the third sternite of the male often possesses a pair of setal patches, the socii of the male genitalia are usually well developed, the vinculum is distally cruciform in structure, the sclerotization of the aedeagus is usually reduced to a ventral strip along its length, and the female genitalia have oblique and papillate ovipositor lobes and a bicornute signum. Both Hausmann (2001) and Han & Xue (2011a) mentioned venation characters: forewing usually without an areole, hindwing with vein M2 close to M1 and far from M3. Beljaev (2008) summarized 12 apomorphies of Geometrinae by adding the results of his study of the skeleto-muscular system of the male genitalia. Since very early studies, the subfamily Geometrinae has been considered a natural entity; it was treated as Group I in Lederer (1853), as Geometridae in Meyrick (1892), as Geometrinae in Hampson (1895) and as Hemitheinae in Prout (1912, 1912–16, 1920–41). The monophyly of Geometrinae is also well supported by later molecular studies, such as those of Yamamoto & Sota (2007) and Sihvonen et al. (2011). Holloway (1997) provided the first tentative phylogeny for Geometridae, which was established mostly based on characters of the adult male and female abdomen, and showed a sister relationship between Geometrinae and Desmobathrinae. Yamamoto & Sota (2007) found that Geometrinae was a sister-group to Oenochrominae. In the molecular phylogenetic analysis of Sihvonen et al. (2011), Oenochrominae s.s. or Oenochrominae s.s. + Desmobathrinae was considered a sister-group to Geometrinae with weak support. Considerable progress has been made in systematics within Geometrinae. The major global taxonomic revision of Geometrinae was that of Prout (1912, 1934–38). Subsequently, many regional works on Geometrinae have been produced: Forbes (1948), Ferguson (1969, 1985) and McGuffin (1988) studied the Geometrinae of North America, Inoue (1961) reviewed the Japanese Geometrinae, Pitkin (1996) researched the neotropical Geometrinae, Holloway (1996) reviewed the Bornean Geometrinae, Hausmann (1996, 2001) investigated Geometrinae from the Levant and neighbouring countries and Europe, McQuillan & Edwards (1996) studied Australian Geometrinae, Viidalepp (1996) produced a checklist of Geometridae from the USSR and erected a new tribe, Hierochthoniini, Han & Xue (2011a) studied Chinese representatives, Hausmann, Parisi & Sciarretta (2014) and Hausmann, Sciarretta & Parisi (2016b) reviewed the Ethiopian Geometrinae (Parts I and II) and Beljaev (2016) published a catalogue of Geometrinae in the insects of the Russian Far East. Almost all of these researchers allocated genera of Geometrinae to tribes or groups. However, due to the lack of a global review, there is no consensus regarding the systematic placement of tribes and groups within Geometrinae and no clear understanding of the relationships between the tribes. Within Geometrinae, Holloway (1996) divided the subfamily into two tribes: Dysphaniini and Geometrini. The latter included almost all the geometrine species and almost all the known tribes as subtribes. Later, Holloway (2011) separated the tribe Pseudoterpnini from Geometrini. Pitkin (1996), Hausmann (1996) and Han & Xue (2011a) raised Holloway’s subtribes to the tribal level. Hausmann (1996) recognized 15 tribes and Forum Herbulot (2007) recognized 18 tribes for Geometrinae on a global basis. However, some tribal concepts remain controversial. For example, Holloway (1996) favoured a wide concept of Hemitheini embracing Thalerini, Comostolini, Hemistolini, Jodini and Thalassodini, whereas these taxa were treated as valid tribes by Hausmann (1996, 2001). Later, Thalassodini were synonymized with Hemistolini in Hausmann et al. (2016b). Beljaev (2016) proposed a much wider concept of Hemitheini by adding Rhomboristini (also Lophochoristini) and Microloxiini (also Hierochthoniini). The most likely reason for these controversies is that these systematic concepts were mainly drawn from morphological overviews and not based on phylogenetic analysis, although they sometimes utilized phylogenetic hints. The first morphology-based topology of Geometrinae was presented by Viidalepp (1981), who used various calculations to divide 26 genera into ten tribes based on 12 multi-state characters, erected the tribe Archaeobalbini and placed Pseudoterpnini sensuHerbulot, 1963 under Terpnini sensuInoue, 1961 as a subtribe. Stekolnikov & Kuznetzov (1981) presented two supertribes, Geometridii and Comibaenidii, based on the functional morphology of the male genitalia of ten geometrid species; the former included Geometrini, Ochrognesiini, Hemitheini and Hemistolini, and the latter included only Comibaenini. Cook (1993) conducted the first cladistic analysis based on 45 geometrine genera and 24 multistate characters. Although he stated that his dataset was insufficient to resolve the phylogeny of Geometrinae, the topology still showed that many known tribes (such as Thalassodini, Hemitheini, Thalerini, Jodini, Hemistolini, Comostolini, Synchlorini and Nemoriini) were grouped in one superclade, which somewhat supports some of the morphological results mentioned above. Han (2005) conducted a preliminary cladistic analysis of the tribe Geometrini, based on 71 morphological characters, and found that the monophyly of Geometra Linnaeus was doubtful, since the species were clustered in several different clades, and the phylogenetic relationships among genera were unclear. The rapid development of DNA sequencing techniques has accelerated the molecular phylogenetic analysis of Geometridae (Abraham et al., 2001; Young, 2006; Snäll et al., 2007; Yamamoto & Sota, 2007; Õunap, Viidalepp & Saarma, 2008; Strutzenberger et al., 2010; Wahlberg et al., 2010; Õunap et al., 2011; Sihvonen et al., 2011; Õunap, Viidalepp & Truuverk, 2016; Sihvonen, Staude & Mutanen, 2015). The most comprehensive taxon sampling at the tribal level was achieved by Sihvonen et al. (2011): 16 of 18 geometrine tribes sensuForum Herbulot (2007) and three genera of unknown affiliation were sampled, and a preliminary molecular phylogeny of Geometrinae was established on a global scale. Although the study included most tribes of Geometrinae, only one species was sampled for each of 11 tribes and a total of only 27 geometrine species in 25 genera representing Geometrinae were included. In addition, as the authors stated, the bootstrap values of most nodes were very low and most of the phylogenetic relationships in Geometrinae, with the exception of the position of the Dysphaniini, were not discussed. The relationships among the tribes of Geometrinae remain largely unexplored. This study aims to further investigate the phylogenetic relationships within Geometrinae at the tribal level, to test the monophyletic hypotheses of tribes, to revise the existing tribal classification within the subfamily and to revise the tribe Geometrini, which is mainly based on Palaearctic and Oriental genera, to cover almost all known tribes (except Dichordophorini) using one mitochondrial gene (COI) and six nuclear genes (EF-1α, CAD, GAPDH, RPS5, MDH and 28S). The results of this study will shed light on the tribal classification of the genera in Geometrinae, improve our understanding of the phylogenetic relationships within the subfamily at the global scale and provide a phylogenetic framework for studying the evolutionary history of Geometrinae. MATERIAL AND METHODS Taxon sampling A total of 116 species belonging to 56 genera representing 17 currently recognized Geometrinae tribes (with only one monobasic tribe, Dichordophorini, not sampled) were included in this study (Fig. 1). At least two species in each tribe, except Lophochoristini, were sampled to weaken the possible effects of long-branch attraction (Hedtke, Townsend & Hillis, 2006). These samples included 22 species of 19 genera downloaded from NCBI (https://www.ncbi.nlm.nih.gov/) that were sequenced by Canfield et al. (2008), Wahlberg et al. (2010), Mutanen, Wahlberg & Kaila (2010) and Sihvonen et al. (2011). We adopted 12 exemplars representing the other six subfamilies (Sterrhinae, Larentiinae, Archiearinae, Ennominae, Oenochrominae and Desmobathrinae) of Geometridae as outgroups. A list of taxa with the collecting localities, voucher codes and GenBank accession numbers is provided in the Supporting Information (Table S1). Some specimens are unidentified morphologically and molecularly on BOLD SYSTEMS due to insufficient taxonomy and constitute potential new species. A formal description of new species is, however, beyond the scope of this study. Figure 1. View largeDownload slide Representatives of the tribes of Geometrinae, sampled in the present study. A, Ornithospilini, Ornithospila esmeralda (Hampson); B, Agathiini, Agathia arcuata Moore; C–H, Hemitheini; C, Rhomboristiti, Rhomborista monosticta (Wehrli); D, Hemistoliti, Hemistola isommata Prout; E, Comostoliti, Comostola virago Prout; F, Hemitheiti, Hemithea aestivaria (Hübner); G, Joditi, Jodis irregularis (Warren); H, Thalassoditi, Thalassodes immissaria Walker; I, Xenozancla versicolor Warren; J, Dysphaniini, Dysphania militaris (Linnaeus); K, Pseudoterpnini, Pingasa rufofasciata Moore; L, Pseudoterpnini, Pachyodes novata Han & Xue; M, Chlorodontopera discospilata (Moore); N, Neohipparchini, Neohipparchus vallata (Butler); O, Aracimini, Aracima serrata Wileman; P, Nemoriini, Eucyclodes pastor Butler; Q, Comibaenini, Comibaena biplaga Walker; R, Iotaphora admirabilis (Oberthür); S, Timandromorphini, Timandromorpha discolor (Warren); T, Geometrini, Geometra papilionaria (Linnaeus); U, Geometrini, Tanaorhinus viridiluteata (Walker). Scale bar = 1 cm. Figure 1. View largeDownload slide Representatives of the tribes of Geometrinae, sampled in the present study. A, Ornithospilini, Ornithospila esmeralda (Hampson); B, Agathiini, Agathia arcuata Moore; C–H, Hemitheini; C, Rhomboristiti, Rhomborista monosticta (Wehrli); D, Hemistoliti, Hemistola isommata Prout; E, Comostoliti, Comostola virago Prout; F, Hemitheiti, Hemithea aestivaria (Hübner); G, Joditi, Jodis irregularis (Warren); H, Thalassoditi, Thalassodes immissaria Walker; I, Xenozancla versicolor Warren; J, Dysphaniini, Dysphania militaris (Linnaeus); K, Pseudoterpnini, Pingasa rufofasciata Moore; L, Pseudoterpnini, Pachyodes novata Han & Xue; M, Chlorodontopera discospilata (Moore); N, Neohipparchini, Neohipparchus vallata (Butler); O, Aracimini, Aracima serrata Wileman; P, Nemoriini, Eucyclodes pastor Butler; Q, Comibaenini, Comibaena biplaga Walker; R, Iotaphora admirabilis (Oberthür); S, Timandromorphini, Timandromorpha discolor (Warren); T, Geometrini, Geometra papilionaria (Linnaeus); U, Geometrini, Tanaorhinus viridiluteata (Walker). Scale bar = 1 cm. DNA extraction, amplification and sequencing We extracted total genomic DNA from adult unilateral legs that had been dried or freshly preserved in anhydrous ethanol using the DNeasy Blood and Tissue Kit (Qiagen, Beijing, China) following the protocol suggested by the manufacturer. In total, fragments of one mitochondrial protein-coding gene (COI), five nuclear protein-coding genes (EF-1α, CAD, GAPDH, RPS5 and MDH) and one nuclear rRNA gene (28S) were sequenced. These molecular markers have been widely used in reconstructing the phylogenies of different families of Lepidoptera (e.g. Wahlberg & Wheat, 2008; Rota & Wahlberg, 2012), especially Geometridae (e.g. Yamamoto & Sota, 2007; Wahlberg et al., 2010; Sihvonen et al., 2011). Several pairs of new primers were designed by PRIMER PREMIER 5.0 (Lalitha, 2000) based on sequences that were previously obtained using universal primers. The primer sequences and the annealing temperatures used for polymerase chain reactions (PCRs) are provided in the Supporting Information (Table S2), mainly from Folmer et al. (1994), Belshaw & Quicke (1997), Wahlberg & Wheat (2008) and our previous works (Cheng et al., 2016; Jiang et al., 2017). PCR was performed in a total volume of 25 μL; the reaction contained 12.5 μL of PCR 2×TSINGKETM Master Mix (TSINGKE, Beijing, China), 0.5 μL of each primer, 1 μL of the extracted DNA and 10.5 μL of ultrapure water. The cycling parameters were: a 5-min denaturing step at 95 °C followed by 30–40 cycles of 30 s at 94 °C, 30 s at a primer-specific annealing temperature, extension at 72 °C for 30 s to 1 min and final extension at 72 °C for 10 min. A 7-μL PCR mixture was examined on a 1.0% agarose gel to determine the quality and quantity of the PCR products before the sequencing reaction was performed. The remaining PCR product was sequenced using the same primers on an ABI PRISM 3730xl automated sequencer at BGI (Beijing Genomics Institute, China). Phylogenetic analyses The phylogenetic analyses were conducted both with, and excluding, the 28S rRNA gene fragment. The alignment of the 28S fragment is problematic due to the coexistence of a highly conserved core structure and highly variable regions (Gutell, 1996; Schnare et al., 1996; Marvaldi et al., 2009), and there is no consensus on how to use this gene fragment (Young, 2006; Mengual, Ståhls & Rojo, 2015; Õunap et al., 2016). In this study, all the 28S gene loci, after alignment by MAFFT, were used for phylogenetic analyses. Partial DNA sequences were downloaded from GenBank, due to the lack of samples. All sequences were manually edited using the SEQMAN module of the LASERGENE software package (DNASTAR, Madison, WI). Sequences of protein-coding genes were aligned using CLUSTALW as implemented in MEGA 6.0 (Tamura et al., 2013), and 28S rRNA segments D1 and D2 were concatenated and aligned in MAFFT v.6 (Katoh & Toh, 2008). Neighbour-joining trees for each gene were constructed using MEGA 6.0 to check the validity of each gene of every sample. Problematic sequences were re-analysed or removed from subsequent analyses. We obtained 153 samples yielding an assembly of 5805 bp of nucleotide data. A partition strategy based on the actual evolution rate of nucleotide data has been widely used in recent phylogenetic analyses (Õunap et al., 2016; Jiang et al., 2017). Rota & Wahlberg (2012) showed its advantages over partitioning by genes or codon positions in Lepidoptera. We partitioned the nucleotide dataset by the actual rate of evolution in the following analyses; the related substitution models are shown in the Supporting Information (Table S3). We used TIGER v.1.02 (Cummins & McInerney, 2011) to separate slowly evolving characters, which was expected to be more reliable for inferring deep divergences, from rapidly evolving characters, with the total bin number parameter set to 50. PARTITIONFINDER 1.1.1 (Lanfear et al., 2012) was used to select the most effective partitioning scheme according to the Bayesian information criterion (BIC) (Posada & Buckley, 2004) and to determine the best phylogenetic models for each dataset using the bins defined by TIGER. For the maximum likelihood (ML) analyses, PARTITIONFINDER was run with models = raxml and search = greedy options, whereas in the Bayesian analyses, models = mrbayes and search = greedy options were performed. The ML analyses were implemented in RAxML v.7.7.1 on the RAxML webserver (http://phylobench.vital-it.ch/raxml-bb/index.php) (Stamatakis et al., 2008) under the GTR+Gamma model for the final best-scoring ML tree. Bayesian phylogenetic reconstructions were generated using MRBAYES v.3.2 (Huelsenbeck & Ronquist 2001) on the CIPRES Science Gateway v. 3.1 (Miller, Pfeiffer & Schwartz, 2010), with the appropriate models and substitution rates. Four simultaneous Markov chains (one cold and three heated) were run for 10000 million generations until the split frequencies were below 0.01, sampling trees every 1000 generations and discarding 25% of the trees as burn-in. The software TRACER v.1.6 (Rambaut et al., 2014) was used both to estimate the sample sizes of the parameters in the Bayesian analyses and to check for the convergences or otherwise of the parallel MCMC runs. RESULTS The analyses conducted in this study are based on the sequence data from one mitochondrial gene region (1371 bp of COI), six nuclear gene regions (955 bp of EF-1α, 847 bp of CAD, 706 bp of GAPDH, 602 bp of RPS5, 474 bp of MDH and 850 bp of 28S rRNA). The final aligned data matrix contained 5805 nucleotide sites. The robustness of clades found is presented as posterior probabilities (PP, for the Bayesian analysis) or bootstrap values (BS, for the ML analysis). The two phylogenetic analyses (ML and Bayesian) of the combined datasets of seven gene regions yield almost identical topologies (Fig. 2). The analyses excluding 28S also yielded very similar topologies (Supporting Information, Fig. S1) except for several small differences in the terminal branches. Figure 2. View largeDownload slide View largeDownload slide Maximum likelihood phylogeny of the subfamily Geometrinae. Bootstrap support values from the ML analysis and posterior probabilities from Bayesian analysis indicated at the nodes as BS/PP. Figure 2. View largeDownload slide View largeDownload slide Maximum likelihood phylogeny of the subfamily Geometrinae. Bootstrap support values from the ML analysis and posterior probabilities from Bayesian analysis indicated at the nodes as BS/PP. The monophyly of Geometrinae is strongly supported in two phylogenetic analyses (PP = 1, BS = 100) in relation to the genera included in this study. Close to the root of Geometrinae, two genera, Ornithospila Warren and Agathia Guenée, branch off the main lineage, one after the other, with strong support. The tribes Rhomboristini, Heliotheini, Hemistolini, Comostolini, Hemitheini, Microloxiini, Thalerini, Lophochoristini, Jodini, Thalassodini and one unassigned genus Aporandria Warren are clustered in a clade with full support (PP = 1, BS = 100). In this clade, the tribe Rhomboristini is at the most basal position with very strong support (PP = 1, BS = 99). Three well-supported subclades within this clade are recognized: (1) Hemistolini and Comostolini constitute a monophyletic subclade with full support (PP = 1, BS = 100); (2) the monophyly of the subclade composed of Hemitheini, Microloxiini and Thalerini is well supported (PP = 1, BS = 94) – in this subclade, Thalerini is embedded in Hemitheini; (3) Jodini and Thalassodini, together with Aporandria, form a monophyletic clade (PP = 0.93, BS = 92) in which the monophyly of Thalassodini is fully supported, the sister relationship between Thalassodini and Aporandria is strongly supported and the monophyly of Jodini is not supported because Thalassodini + Aporandria form a sister-group to part of Jodini and are nested in Jodini. The genus Maxates Moore is shown as a non-monophyletic assemblage in which M. grandificaria Graeser and M. acutissima perplexata Prout cluster with Ecchloropsis Prout, and M. thetydaria Guenée, M. sp.1 and M. sp.2 cluster with Berta Walker and Jodis Hübner. The concept of Pseudoterpnini in Pitkin et al. (2007) is revealed to be polyphyletic. Pseudoterpna Hübner and Pingasa Moore form a monophyletic group with full support (PP = 1, BS = 100), and group with Dysphaniini with full support in Bayesian analyses but weak support in ML analyses (PP = 1, BS = 47), after clustering with Xenozancla Warren. However, many other genera (Herochroma Swinhoe, Metallolophia Warren, Absala Swinhoe, Actenochroma Warren, Metaterpna Yazaki, Limbatochlamys Rothschild, Psilotagma Warren, Dindica Moore, Dindicodes Prout, Lophophelma Prout and Pachyodes Guenée) are clustered in a separate clade with moderate support in Bayesian analyses (PP = 0.97) and weak support (BS = 57) in ML analyses. In this clade, the sister relationship between Limbatochlamys and Psilotagma is fully supported (PP = 1, BS = 100) and was first found in this study. The genera Dindica, Dindicodes, Lophophelma and Pachyodes are clustered together with full or strong support (PP = 1, BS = 98). A close relationship between Absala and Actenochroma was also identified for the first time. The remaining Geometrinae are clustered in a clade (PP = 0.97, BS = 62) embracing seven tribes and two unassigned genera: Chlorodontopera Warren, Aracimini, Neohipparchini, Nemoriini + Synchlorini + Comibaenini, Iotaphora Warren, Timandromorphini and Geometrini. The monophyly of Neohipparchini is well supported in both analyses (PP = 1, BS = 83). The tribe is redefined to accommodate Chlororithra Butler in addition to Neohipparchus Inoue and Chloroglyphica Warren. Aracimini is fully supported (PP = 1, BS = 100) as a monophyletic clade consisting of Paramaxates Warren, Dooabia Warren and Aracima Butler, with Aracima embedded within Dooabia. In the analyses excluding 28S, the position of Aracimini is exchanged with that of Neohipparchini (Supporting Information, Fig. S1). The tribes Nemoriini, Synchlorini and Comibaenini are clustered in one clade with strong support (PP = 0.98, BS = 99) but with the relationship among them was unresolved. The current concept of Nemoriini is polyphyletic, as Pyrochlora Warren is sister to Comibaenini in all trees. The monophyly of Comibaenini is well supported (PP = 1, BS = 88). The sister relationship between Timandromorphini and Geometrini is moderately supported (PP = 0.95, BS = 88), and the monophyly of both tribes is strongly to fully supported. In the tribe Geometrini, the sister relationship between Chlorozancla Prout and Mixochlora Warren is strongly supported (PP = 0.95, BS = 96). Members of Geometra and Tanaorhinus Butler are clustered in one clade with full support (BS = 100, PP = 1.00) and these genera are confirmed to be polyphyletic groups. DISCUSSION This study covers all tribes of the Geometrinae, except the North American tribe Dichordophorini Ferguson, which includes only one genus, Dichordophora Prout, making this study a comprehensive phylogenetic analysis to date of Geometrinae at the tribal level. Though 17 (18 in total) currently recognized tribes were included in this analysis, our sampling was mainly restricted to the Palaearctic and Oriental regions; the data are, therefore, not sufficient to elaborate the whole evolutionary story of Geometrinae. The genus Eumelea Duncan was transferred from Oenochrominae s.l. to Desmobathrinae by Holloway (1996), whilst the author pointed out that Eumelea lacks the definitive features of the desmobathrines. Beljaev (2008) considered Eumelea be a member of Geometrinae on the basis of the skeleto-muscular structure of the male genitalia, and pointed out that it may occupy a basal position in Geometrinae. In the same study, Beljaev doubted the desmobathrine position of the genus Celerena Walker (not sampled in the present study) and thought it a possible geometrine member. Although the affinity between Eumelea and Geometrinae is not directly supported in this study, the former is clustered with members of Desmobathrinae and Oenochrominae with poor support, so the possibility of Eumelea belonging to Geometrinae and occupying a basal position is not excluded. The multi-gene phylogeny determined in this study validates the monophyly of the subfamily Geometrinae and recovers 12 tribes (Dichordophorini not sampled), two of which are proposed as new. The tribes are Ornithospilini trib. nov., Agathiini trib. nov., Dysphaniini, Pseudoterpnini, Neohipparchini, Aracimini, Nemoriini, Synchlorini, Comibaenini, Timandromorphini, Geometrini and Hemitheini on a very broad concept embracing nine subtribes. Only three tribes (Dysphaniini, Comibaenini and Timandromorphini) are totally concordant with the previous morphology-based concepts of tribes recognized by Holloway (1996, as subtribes), Hausmann (1996) and Forum Herbulot (2007), and five tribes (Aracimini, Neohipparchini, Nemoriini, Synchlorini and Geometrini) are in rough agreement with them. Resolution of the inter-tribal relationships within Geometrinae remains limited, probably due to the limited sampling of taxa and molecular markers and sampling bias towards the Palaearctic and Oriental regions. The tribe Ornithospilini is the most basal taxon, followed by Agathiini. The sister relationship between Hemitheini and all the remaining geometrine groups is fully supported in Bayesian analyses and only weakly supported in ML analyses. In the clade composed of Chlorodontopera, Aracimini, Neohipparchini, Nemoriini + Synchlorini + Comibaenini, Iotaphora, Timandromorphini and Geometrini, Chlorodontopera and Neohipparchini are the most basal taxa, the close relationship among Nemoriini, Synchlorini and Comibaenini is strongly supported, and the close relationship between Timandromorphini and Geometrini is moderately supported. Holloway (1996) described the typical ovipositor lobes of Geometrinae (different from those of Dysphaniini) as follows: the distal margin of the ovipositor lobes recedes obliquely ventrally, and the setae are placed irregularly on papillate projections. He also noted that there are exceptions in the Geometrini, Timandromorphini, Paramaxates and Neohipparchini. Combined with the present tree (Fig. 2), there is one possible trend: the ovipositor lobes are inclined to be more sclerotized, smoother and slenderer in more evolved groups (e.g. Geometrini, Neohipparchini and Paramaxates). The modification of the ovipositor lobes may be related to oviposition preferences and larval host plants. Because the phylogenetic relationships among the tribes were not totally resolved, this hypothesis requires further testing with studies that clarify the phylogeny in Geometrinae by including more taxa and more genes. The following sections will describe the tribal classification of the Geometrinae, including the morphological characters and a short review of the main taxonomic histories of the respective groups, and the credible phylogenetic relationships inferred from the phylogenetic trees. Unless major changes occurred in one tribe, the differential features of the tribes will not be repeated. Ornithospilini Ban & Han trib. nov. Type genus: Ornithospila Warren, 1894 (Holloway, 1996: plate 7, figs 217–225 and 315–316; Han & Xue, 2011a: figs 20–22 of plate 18, figs 342–344, 661–663 and 865–866). Differential features: The wings of the members of Ornithospilini are bright green. The hind tibia of the male is not dilated. The veins Sc+R1 are close to the cell at one point, then separate rapidly on the hindwing; CuA1 and M3 are separate, and vein 3A is absent. Sternite 3 of the male abdomen lacks setal patches. The socii of the male genitalia are developed and are almost the same length as the uncus as in Hemitheini but sometimes with a basal process. The signum of the female genitalia, if present, is elongate, ovate and scobinate (Holloway, 1996). Ornithospilini is proposed as a new, currently monobasic tribe that is mainly distributed in the Oriental region. In this study, the Ornithospilini exemplars (two different species of Ornithospila) form a distinct group that occupies a basal position in Geometrinae. Prout (1912) placed Ornithospila in Group IV of the Old World genera and mentioned that it probably derived from Hipparchus (Geometra), but he also stated that the venation and genitalia of the type species agree better with Prasinocyma Warren and the Iodis group (Jodis). Later, Prout (1920–41) suggested that some species of Ornithospila are somewhat analogous to Aporandria in size, shape and coloration. Although Hausmann (1996) placed Ornithospila in Geometrini, he also referred to features that differentiate it from Geometrini, such as the presence of an uncus and the shorter and slightly sclerotized socii. Holloway (1996) considered Ornithospila as set apart from the rest of the Geometrinae by the condition of the female signum, which is elongate, ovate and scobinate. This opinion is supported here, as Ornithospila is positioned at the base of Geometrinae, and the relationship to Aporandria and Geometrini is not supported. Agathiini Ban & Han trib. nov. Type genus: Agathia Guenée, 1858 (Holloway, 1996: plates 7, 8 and 10, figs 194–211, 213–216, 239, 243; Han & Xue, 2011a: figs 22–28 of plate 19, figs 1–8 of plate 20, figs 371–385, 690–704 and 884–893). Differential features: Wings are bright green. The antennae are filiform in both males and females. The hind tibia of the male is dilated, with hair-pencil. The forewing usually possesses distinctive medial and terminal bands and a series of patches. Veins M3 and CuA1 are connate at the cell on the hindwing, and 3A is present. Sternite 3 of the male abdomen usually has a pair of setal patches. The two branches of the socii are close to each other and are fused at the base, resembling those of Pseudoterpna, Dooabia and Louisproutia Wehrli. The costa of the valva is ornamented with a dorsal process. In the female genitalia, the corpus bursae usually has a bicornute signum. Agathiini is established here as a new tribe, tentatively including only the genus, Agathia, represented by three species, including the type species of the genus Hypagathia Inoue (synonym of Agathia), Agathia carissima Butler. Agathia is a large genus, including 77 species worldwide (Scoble, 1999; Scoble & Hausmann, 2007) and is widely distributed in Southeast Asia, Australia and Africa. Inoue (1961), Viidalepp (1981), Hausmann (1996) and Beljaev (2016) placed Agathia in Pseudoterpnini (or Terpnini) mainly based on morphological studies. Stekolnikov & Kuznetzov (1981) suggested that it belongs to Ochrognesiini (Nemoriini) on the basis of the functional morphology (muscles) of the male genitalia. Holloway (1996) did not place it into any tribe and stated that it is unwise to erect a new tribe without a well-understood classification of Geometrinae in its entirety. In this study, species of Agathia form a distinct group that branched off after Ornithospilini and are placed in a more basal position, unlike the results of Sihvonen et al. (2011), in which Agathia is positioned at the base of the second major lineage with very weak support. The combination of the bright green wing colour, the structure of the socii and the presence of a dorsal ornament of the valva distinguish Agathiini from other known tribes. Hemitheini The concept of Hemitheini recognized here is broader than that of Holloway (1996) due to the inclusion of several additional tribes: Rhomboristini, Lophochoristini, Heliotheini and Microloxiini (= Hierochthoniini). For this study, the main characters of Hemitheini are: the male antennae are usually bipectinate; the moths are mainly bluish, emerald green or greyish green in colour; the outer margin of the hindwing bears a tail process in many genera; veins M3 and CuA1 of the hindwing are usually stalked (separate or connate in Rhomboristiti genera); most genera have a frenulum, but some do not (such as Berta, Comostola Meyrick, Hemistola Warren, Jodis, Thalera Hübner and Eucrostes Hübner); and the socii and uncus are similar in length and are usually closely adpressed (a strong uncus with weak socii in Rhomboristiti genera). Holloway (1996) stated that the larvae are usually slender and the resting posture is stick-like. The concept of Hemitheini has long been controversial and the internal structure has not been resolved, though some researchers suggested a close relationship among some groups. Viidalepp (1996) indicated a close relationship between Thalerini and Hemistolini, Jodini and Hemitheini by including Hemistola in Thalerini and genera of Jodini in Hemitheini, respectively. Hausmann (1996) noted that Thalerini, Hemistolini, Comostolini, Jodini, Hemitheini and Microloxiini are linked by various genera. For example, he stated that the venation of Rhomboristini corresponds to that of Jodini and Comostolini, some features of Comostolini resemble those of Hemistolini, Jodini has a relationship to Hemitheini and Thalerini is close to Hemitheini. Holloway (1996) introduced a wide concept of Hemitheini, embracing Thalerini, Comostolini, Hemistolini, Jodini and Thalassodini. He also synonymized Lophochoristini with Rhomboristini. Pitkin (1996) still treated Lophochoristini as a valid tribe. Beljaev (2007) stated that the transtilla of the type genus of Hemitheini is quite different from that of the other genera, which is similar to that in Jodini, Microloxiini and Hemistolini (sensuInoue, 1961 and Hausmann, 2001). He also indicated that Thalerini are probably subordinate to Hemitheini Bruand, 1946. The Hemitheini concept in Beljaev (2016) is wider, embracing Hemitheini Bruand, Comostolini, Jodini, Hemistolini, Thalassodini, Rhomboristini, Thalerini, Lophochoristini and Microloxiini (also Hierochthoniini). In this analysis, the broad concept of Hemitheini is fully supported and the monophyletic Hemitheini embrace almost all tribes mentioned in Beljaev (2016); the concept of Hemitheini by Beljaev is accepted here by the addition of Heliotheini (Petovia Walker). As Hemitheini is extremely large, some previous tribes are treated as subtribes, with subtribes equal to previous tribes. After the branching off of the genera Rhomborista Warren (Rhomboristiti) and Petovia (Heliotheiti), three well-supported subclades are recognized within Hemitheini: Hemistoliti + Comostoliti, Hemitheiti + Microloxiiti, and Joditi + Aporandria + Thalassoditi. Rhomboristiti The subtribe Rhomboristiti (as Rhomboristini) was established by Inoue (1961) as embracing three Indo-Australian genera, Rhomborista, Spaniocentra Prout and Rhombocentra Holloway, and was treated as a valid tribe by Holloway (1996). Holloway (1996) suggested the synonymy of Lophochoristiti and Heliotheiti with Rhomboristiti for three tribes sharing similar male genitalia with features such as a strong uncus with weak socii, a strong gnathos and often a doubled harpe-like process in the centre of the valva. Hausmann (1996) indicated that the hindwing venation of Rhomboristiti corresponds well with that of Comostola (Comostoliti) and Berta (Joditi). In this study, close relationships between Rhomboristiti, Lophochoristiti and Heliotheiti or between Rhomboristiti and Comostoliti were not supported; instead, Rhomboristiti constitutes a basal clade within Hemitheini with full support, implying its isolated position in Hemitheini. Hemistoliti + Comostoliti Hemistoliti and Comostoliti were both erected by Inoue (1961) as tribes. Hausmann (1996) summarized the differential features of these two groups, mentioned that some features of Comostoliti (e.g. the male genitalia) are reminiscent of Hemistoliti and stated that there is a close relationship between Comostoliti and Joditi. As in Sihvonen et al. (2011), the close relationship between Comostoliti and Hemistoliti, represented by the type genus of each, is fully supported here, validating the statement by Hausmann (1996). However, the monophyly of Hemistoliti is not supported, as Hemistola tenuilinea Alphéraky is sister to parts of Hemistoliti and Comostoliti. Therefore, we suggest that Comostoliti is a possible synonym of Hemistoliti and that further research, including more genera of Hemistoliti and Comostoliti, is needed. In this analysis, the close relationship between Comostoliti and Joditi is not directly supported, and the synonymization between Hemistoliti and Thalassoditi presented by Hausmann et al. (2016b) is not directly supported because the phylogeny of Hemitheini is not fully resolved. Hemitheiti + Microloxiiti The subtribe Hemitheiti (i.e Hemitheini s.s.), embracing 18 genera (Inoue, 1961; Ferguson, 1969, 1985; Hausmann, 1996; Pitkin, 1996; Viidalepp, 1996), is mainly characterized by the male genitalia, in which the uncus is slender, rod-like and pointed or tapered, and the socii are usually similar to the uncus in shape and size (Pitkin, 1996). In this study, Microloxiini, Hemitheini s.s. and Thalerini listed in Forum Herbulot (2007) are grouped in a clade with good support. The phylogenetic relationship within this clade is well resolved in Bayesian analyses, with the genus Episothalma Swinhoe at the most basal position. Microloxia Warren is sister to Pamphlebia Warren and then clusters with Hemithea Duponchel, Hethemia Ferguson falls within Thalera, and Chlorochlamys Hulst is clustered with Chloropteryx Hulst first and then grouped with Chlorissa Stephens. The type genus of the subtribe Thaleriti, Thalera, was placed in Hemitheini by Inoue (1961). Subsequently, Herbulot (1963) established Thaleriti (as Thalerini) based on Thalera. Hausmann (1996) stated that Hemitheiti is rather closely related to Thaleriti based on genitalic morphology. In this study, Thaleriti [including the type species of Thalera, Thalera fimbrialis (Scopoli)] are embedded in Hemitheiti [including the type species of Hemithea, Hemithea aestivaria (Hübner)]. Based on the similarities in the male genitalia of the Thaleriti and Hemitheiti, such as the similar shape and size of the uncus and the socii (Han & Xue, 2011a: figs 225, 353), Thaleriti (syn. nov.) can be synonymized with Hemitheiti. Accordingly, several other genera of Thaleriti, recognized by Hausmann (1996, 2001) (Culpinia Prout, Bustilloxia Expósito, Dyschloropsis Warren, Heteroculpinia Hausmann, Dolosis Prout and Kuchleria Hausmann), should be transferred into Hemitheiti. The subtribe Microloxiiti (as Microloxiini) was established by Hausmann (1996) and includes 11 genera. Externally, these genera share stalked M3 and CuA1 of the hindwing, and the presence of socii and uncus of similar lengths as the Hemitheiti. In this analysis, though Microloxia ruficornis Warren is embedded in Hemitheiti, it is not the type species and, therefore, does not necessarily represent the whole of Microloxia or even Microloxiiti. We, therefore, hesitate to synonymize Microloxiiti with Hemitheiti; the relationship between Microloxiiti and Hemitheiti needs further study with more taxa. The monotypic genus Hethemia, with Hethemia pistasciaria (Guenée) as the type species, is found in North America. In this study, Hethemia falls within Thalera, forms a monophyletic clade with Thalera fimbrialis (= type species of Thalera, T. thymiaria (Linnaeus)) and is, therefore, synonymized with Thalera (= Hethemiasyn. nov.). Pistasciaria is transferred to Thalera as Thalera pistasciariacomb. nov. This synonymy is also supported by morphological characters: the venation (Ferguson, 1969: pl. 5, fig. 5; Han & Xue, 2011a: fig. 63) of both genera is almost identical, except that M3 and CuA1 are stalked in Hethemia and sometimes CuA1 also diverges from the lower angle of the cell in Thalera. In the male genitalia, the two genera possess similar uncus, socii, gnathos and aedeagus (Ferguson, 1969: pl. 29, figs 1 and 2; reference to Han & Xue 2011a, related figures). Joditi + Aporandria + Thalassoditi The grouping of the Joditi, Aporandria and Thalassoditi is well supported in this study. The subtribe Joditi (as Jodini) was established by Inoue (1961) and was treated as a provisional tribe, including four Palaearctic and Indo-Pacific genera (Jodis, Berta, Gelasma and Thalerura Swinhoe, the latter two genera as synonyms of Maxates) by Hausmann (1996). Viidalepp (1996) and Holloway (1996) included Joditi in the wider concept of Hemitheini. Han & Xue (2011a) followed this definition, which is also supported in this molecular study. The species of Maxates number over 100 and were separated in Gelasma Warren, Maxates and Thalerura (Prout, 1912, 1920–41) until Holloway (1996) synonymized Gelasma and Thalerura with Maxates and summarized the most distinctive feature of Maxates as the possession of a strong hindwing tail and a ventral flap on the valva. When Prout (1934–38) described Ecchloropsis, he made a comparison with Hemistola and Dyschloropsis but did not mention Gelasma and Maxates, perhaps because he did not examine the male genitalia. Han & Xue (2011a) summarized the diagnostic characters of Ecchloropsis and Maxates and listed the differences between them. Although they noted that Ecchloropsis has a ventral flap in the valva similar to that found in typical Maxates, the authors did not synonymize the two, given that Ecchloropsis lacks a frenulum, whereas almost all species of Maxates have one. In this analysis, the genus Maxates is found to be polyphyletic, as Maxates acutissima perplexata and M. grandificaria are sister to Ecchloropsis with full support, whereas another three species, M. sp.1, M. sp.2 and M. thetydaria, are grouped as sister to Berta and Jodis. The genus Berta is also found to be paraphyletic, since two species of Jodis are nested within Berta species (including the type species B. chrysolineata Walker). Further research, including the type species of Maxates and Jodis and a greater number of other species, is needed to resolve the phylogenetic relationship among these four genera, the monophyly of the Joditi and the monophyly of Maxates and Berta. The subtribe Thalassoditi (as Thalassodini) was also erected by Inoue (1961) with the inclusion of the genus Thalassodes Guenée, from which three genera (Orothalassodes Holloway, Pelagodes Holloway and Remiformvalva Inoue) were split and erected by Holloway (1996) and Inoue (2006), mainly based on the structures of the male genitalia and the eighth segment. Hausmann (1996) summarized the differential features of Thalassoditi as follows: cell of hindwing very short, discocellular vein oblique and lacking abdominal crests. Hausmann et al. (2016b) synonymized Thalassoditi with Hemistoliti because they share many morphological characters. However, the monophyly of Thalassoditi is fully supported in the present study, with Thalassodes at the basal position of the clade. The genera Prasinocyma and Albinospila Holloway are closely allied to Orothalassodes (Holloway, 1996), and they are expected to be clustered with Orothalassodes if they are sampled. Hausmann et al. (2016a) suggested that the current generic combinations within the large Thalassodes complex (Holloway, 1996) need to be revised. Further research is needed to explore the internal structure of the Thalassoditi by including more genera, such as Prasinocyma and Albinospila. Aporandria was placed in Hemistoliti by Hausmann (1996). He also stated that the external appearance of Aporandria resembles some genera of Geometrini but differs from the latter with respect to the tympanum and venation. In this study, the genus Aporandria is grouped with Thalassoditi with good support. The close relationship between Aporandria and Thalassoditi was first found in this study. However, we hesitate to place Aporandria in Thalassoditi due to its distinct wing patterns. Genera in Thalassoditi, together with Aporandria, are sister to part of Joditi and fall within Joditi. We suspect that the subtribe Thalassoditi may be a synonym of Joditi and that Aporandria also belongs to Joditi, but additional data are needed to validate this hypothesis. Lophochoristiti and Heliotheiti Ferguson (1969) erected the tribe Lophochoristini by including the genera Lophochorista Warren and Eueana Prout. Cook (1993) gave a detailed revision of the neotropical genus Oospila Warren, defined this monophyletic group by the presence of an anellar complex and suggested that Oospila and Lophochorista may be sister taxa. Pitkin (1996) added Anomphax Warren, Telotheta Warren and Oospila to the tribe Lophochoristini. Heliotheini, a tribe erected based on Heliothea Boisduval and another Afrotropical genus, Petovia, was described as a subfamily, but its rank was challenged by Vives Moreno (1994), Müller (1996) and Viidalepp (1996). Later, it was subordinated under Geometrinae by Holloway (1996) and Hausmann (1996). Holloway (1996) suggested Lophochoristini and Heliotheini as junior synonyms of Rhomboristini on the basis of their similar genitalic features. In this study, both Oospila and Petovia are grouped in the tribe Hemitheini, with their positions not resolved. Although Oospila is not the type genus of Lophochoristini, it shares some features with Lophochorista, such as a similar wing pattern, bearing abdominal tufts and possessing a medio-ventral sclerite in the valva (Pitkin, 1996). In addition, Pitkin (1996) pointed out that the ventral sclerite on the valva of the Lophochoristini also occurred in the Rhomboristini and Chlorissa (Hemitheini), which implied a relationship with Hemitheini. Beljaev (2016) also included Lophochoristini in his broad concept of Hemitheini. Thus, it is reasonable to treat Lophochoristini as a subtribe of Hemitheini. However, the position of the tribe Heliotheini is in doubt, as it has some unique features within Geometrinae, such as the shape of the ansa in the tympanal organ, the yellow wing colour and some unusual larval features (Hausmann, 2001). Considering that Heliotheini has similar genitalic features with Hemistoliti (Hausmann, 2001: fig. 11; Han & Xue, 2009: figs 58–61), and Petovia is clustered in Hemitheini in this study, though not as type genus, we tentatively retain Heliotheini as a subtribe. Further study, including Lophochorista and Heliothea, is needed to resolve the phylogenetic position of the Lophochoristiti and Heliotheiti. Dysphaniini + Xenozancla + Pseudoterpnini s.s. In this study, the grouping of Dysphaniini, Xenozancla and Pseudoterpnini s.s. is fully supported in Bayesian analyses but only weakly supported in ML analyses, with Dysphaniini constituting a sister-group of Xenozancla + Pseudoterpnini. The Dysphaniini currently includes only two known genera, Dysphania Hübner and Cusuma Moore, which have been regarded as a natural group. Warren (1895) treated the Dysphaniini as the subfamily Dysphaniinae. Prout (1912) put Dysphania and Cusuma into Group III of Old World genera. Both treatments reflect the distinctive characters that these genera possess. Holloway (1996) presented the unique features of Dysphaniini (the presence of a forewing fovea in both sexes, ansa hammer-headed and lacking a central expansion) in detail and treated it as a sister-group to the rest of Geometrinae. Our result is almost concordant with Sihvonen et al. (2011), in that we did not find support for a division between Dysphaniini and the remaining Geometrinae. The difference from Sihvonen et al. (2011) is that the sister relationship between Dysphaniini and Pseudoterpnini is not supported. Instead, Xenozancla is clustered with Pseudoterpnini. Xenozancla is a small Asian genus that includes only one species. It has not been placed into any known tribes because its combined external and male genitalic features (small size, concavity of forewing distal margin under apex, the coexistence of a bifid uncus and socii, simple valva and long saccus) do not agree with those of known tribes (Han & Xue, 2011a). The present position of Xenozancla is doubtful, given its morphology. Xenozancla is morphologically similar to some species of Pelagodes in Thalassoditi, as the socii of the male genitalia are attached to the base of the gnathos (Han & Xue, 2011a: fig. 390; Han & Xue, 2011b: figs 33–34.). Prout (1912) mentioned its affinity with the African genus Bathycolpodes Prout; both genera have an anteriorly excavated distal margin of the forewing and almost identical wing patterns. In Xenozancla, the excavation on the hindwing is shallower than in Bathycolpodes. Pitkin et al. (2007) provided a comprehensive morphological review of the tribe Pseudoterpnini, in which 34 genera were recognized, covering most genera in the Pseudoterpninae (Warren, 1893, 1894), Groups I and II (Prout, 1912), Terpnini (Inoue, 1961), Archaeobalbini (Viidalepp, 1981), Pingasini (Heppner & Inoue, 1992), Pseudoterpnini (Hausmann, 1996, 2001) and Pseudoterpniti (Holloway, 1996). They suggested that Pseudoterpnini was likely monophyletic, although no single defining character was found. Hausmann (1996, 2001) stated that some features of Holoterpna Püngeler and Aplasta Hübner were anomalous within Pseudoterpnini, the systematic position of Aplasta being particularly isolated. When Holloway (1996) summarized the diagnosis of Pseudoterpnini, he also mentioned that the strong black discal dots and broad black bands on the underside, characteristic of most genera in this broad concept, are absent from Pseudoterpna (though present in Pingasa). Pitkin et al. (2007) also referred to the fact that the type genus Pseudoterpna and several apparently related genera (Aplasta, Holoterpna, Mictoschema Prout and Mimandria Warren) are anomalous in comparison with the rest of the tribe. All these statements imply that the monophyly of Pseudoterpnini is in doubt. In this study, it is surprising that most Oriental and Palaearctic Pseudoterpnini genera in Pitkin et al. (2007), such as Herochroma, Metallolophia, Actenochroma, Absala, Metaterpna, Psilotagma, Limbatochlamys, Dindica, Dindicodes, Lophophelma and Pachyodes, are not clustered with the type genus of Pseudoterpnini, Pseudoterpna. This result differs from other research, such as Sihvonen et al. (2011), in which only two genera and two species of Pseudoterpnini, Pseudoterpna coronillaria (Hübner) and Crypsiphona ocultaria (Donovan), were sampled. This result probably further proves that the monophyly of the tribe Pseudoterpnini is problematic. We tentatively treat the concept of Pseudoterpnini of Pitkin et al. (2007) as Pseudoterpnini s.l. and genera centred around Pseudoterpna as Pseudoterpnini s.s. Prout (1912–16) stated that the larva of Pingasa seems to be allied with Pseudoterpna and that the latter is probably descended from the former. In this study, Pseudoterpna and Pingasa form a monophyletic clade representing Pseudoterpnini s.s. with full support, validating the close relationship mentioned by Prout. These genera also share a similar wing pattern (distinctive transverse lines) and male genitalia (e.g. bifid socii) with Epipristis Meyrick, Mictoschema, Mimandria, Hypodoxa Prout and Pullichroma Holloway. However, to determine which genera belong to Pseudoterpnini s.s., a more extensive phylogenetic study including all the related genera in Pseudoterpnini s.l. and not only Oriental genera, as in this study, is needed. Pachyodes-complex in Pseudoterpnini s.l. In this study, many of the genera previously included within Pseudoterpnini in Pitkin et al. (2007) form a separate clade: Herochroma, Metallolophia, Actenochroma, Absala, Metaterpna, Limbatochlamys, Psilotagma, Dindica, Dindicodes, Lophophelma and Pachyodes. Although these genera are always clustered together and branch after the clade composed of Dysphaniini + Xenozancla + Pseudoterpnini s.s., the support value is weak. They are also difficult to deliminate from Pseudoterpnini s.s. morphologically, as sharing many features, including: fairly large moth with a robust build, wings undersides usually with strong terminal bands; the socii/uncus complex often present; and valvae often divided into two parts (a costal lobe and a sacculus) (Pitkin et al., 2007). Further research tends to separate Pseudoterpnini s.s. and these genera and studies, including more taxa, are needed. We tentatively treat these genera as a generic group, Pachyodes-complex, in Pseudoterpnini s.l. In the Pachyodes-complex, Herochroma and Metallolophia are the two most basal genera. The close relationship between the genera Limbatochlamys and Psilotagma is fully supported and was first discovered in this study. Although these genera are very different externally, the male genitalia of both have a slender uncus and socii, and the female genitalia of both possess a short ductus bursae and a large concave corpus bursae (Han & Xue 2011a: fig. 110–112, 143, 733, 734 and 755). Sphagnodela Warren (not sampled in this study) probably belongs to this group, based on its similar uncus and socii. Dindica, Dindicodes, Lophophelma and Pachyodes form a monophyletic group within the Pachyodes-complex. This relationship was first found in this study. These genera are mainly characterized by the presence of a bifid uncus and usually a divided valva in the male genitalia. The sister relationship between Absala and Actenochroma was also established here. It is possible that the monotypic genera Pachista and Calleremites Warren (not sampled in this study) also belong to this generic group, as Calleremites shares the presence of both uncus and socii with Actenochroma, Limbatochlamys, Metaterpna and Psilotagma, and Pachista shares divided costal and saccular lobes with Pachyodes, Metallolophia, Dindica and Dindicodes. The monophyly of most genera is fully supported, except for that of Lophophelma, which is paraphyletic, as two species of Pachyodes (type species not sampled) are nested within Lophophelma. The male genitalia of Lophophelma vary between species and are quite different from those of Pachyodes, which are characterized by a valva divided into two large lobes of similar length or with the costal lobe a little shorter. Further study, including the type species of both genera and more species, is needed to resolve the monophyly of Lophophelma and its relationship with Pachyodes. Chlorodontopera Warren The genus Chlorodontopera is characterized by the following characters: both fore- and hindwings have large, rounded discal spots, which are larger on the hindwing; a dull reddish-brown patch is present between the discal spot and the costa on the hindwing; in the male genitalia, the socii are stout and setose and the lateral arms of the gnathos are developed, not joined; sternite 3 of the male has setal patches; and veins M3 and CuA1 are unstalked on the hindwing. Inoue (1961) suggested that Chlorodontopera is more or less related to Aracima, but he hesitated to place it in the tribe Aracimini. Chlorodontopera was placed in Nemoriini by Hausmann (1996) and in Aracimini by Holloway (1996), followed by Han & Xue (2011a). Prout (1920–41) referred to the similar morphological characters of Chlorodontopera and Euxena Warren. Later, Holloway (1996) compared Chlorodontopera and Euxena, showing that both genera have similar wing patterns but different genitalia. In this study, Chlorodontopera is sister to the clade including Neohipparchini, Aracimini, Nemoriini, Synchlorini, Comibaenini, Timandromorphini and Geometrini. Chlorodontopera is not related to Aracimini and, therefore, can be excluded from that tribe. Given isolated position, the designation of a new tribe, perhaps including the genus Euxena, is probably appropriate. Further study is needed to confirm a close relationship between these two genera. Neohipparchini Inoue (1961) established Neohipparchus, into which he placed three species from Prout’s section C of Hipparchus. He placed the genus into a new tribe, Neohipparchini, separating it from Geometrini. Species of Chloroglyphica were placed in section D of Hipparchus (Prout, 1920–41). Hausmann (1996) synonymized Neohipparchini with Geometrini and stated that the ansa of the tympanal organ in Neohipparchus and Chlororithra shares a similar structure with that of Tanaorhinus. Holloway (1996) treated Neohipparchini (as Neohipparchiti) as a separate tribe, mentioning that Neohipparchus shares similar venation and facies with Geometrini. Han & Xue (2011a) placed both Neohipparchus and Chloroglyphica in Geometrini, without placing Chlororithra in any known tribe. Our results support Neohipparchus + Chloroglyphica + Chlororithra comprising Neohipparchini, whereas a close relationship between Neohipparchini and Geometrini is not supported. Although the two species of Chlororithra are externally different from Neohipparchus and Chloroglyphica, considering the similar ansa structure mentioned by Hausmann, and that Chlororithra shares the presence of both uncus and socii with some species of Neohipparchus, it is better to put Chlororithra in Neohipparchini. Hausmann (1996) implied a possible homology between Neohipparchus and Iotaphora based on the presence of a stout external spine on the aedeagus. Members of Iotaphora are characterized by short radial lines outside the postmedial line on both the fore- and hindwings. The male genitalia of Iotaphora are also similar to those of Chlororithra, as they possess a similarly developed uncus and socii. Hausmann (1996) placed this genus in Geometrini together with Chlororithra. Beljaev (2016) put Iotaphora in Pseudoterpnini. Han & Xue (2011a) did not place Iotaphora into any known tribe. In this analysis, a close relationship between Iotaphora and Neohipparchus is not supported, and the position of Iotaphora is not resolved. Aracimini Inoue (1961) erected the tribe Aracimini, including only Aracima. Holloway (1996) placed another four genera, Paramaxates, Dooabia, Euxena and Chlorodontopera, in Aracimini, but he also noted the differences among them and suggested that these four genera are probably best placed in the vicinity of Geometrini, this was also mentioned in Hausmann (1996). Hausmann (1996) placed Dooabia in Pseudoterpnini together with Agathia because the genitalia of Dooabia are close to those of Agathia. In this study, the monophyly of Aracimini, represented by Paramaxates, Dooabia and Aracima, is fully supported. Aracima serrata Wileman is embedded in Dooabia and forms a monophyletic clade with the type species of Dooabia, D. viridata, with strong support. It is possible that Aracima serrata should be placed in Dooabia, but the male genitalia of D. puncticostata Prout are very different from those of D. viridata (Moore), as they lack a developed costal projection at the base of the valva. Thus, a new genus may need to be erected for this species. If the isolation of D. puncticostata from Dooabia were proven, A. serrata would no longer be combined into Dooabia. The relationship between A. serrata and A. muscosa Butler (type species of Aracima, not sampled) is still pendent, as the male genitalia of the former is unknown and their wing patterns and female genitalia show great differences. Further morphological research based on type species and additional species of both genera is needed. The close relationship between the Aracimini and Timandromorphini proposed in Sihvonen et al. (2011) is not supported in this study. Nemoriini + Synchlorini + Comibaenini Nemoriini (as Nemoriinae in Gumppenberg, 1887) is a New World tribe including many genera, with Ochrognesiini as a representative in the Indo-Australian tropics. The tribe Ochrognesiini was established by Inoue (1961) to include the two genera Chloromachia Warren and Ochrognesia Warren, both of which were synonymized with Eucyclodes Warren, together with six other genera by Holloway (1996). Accordingly, Ochrognesiini was synonymized with Nemoriini. The diagnostic features of Nemoriini were summarized and commented on by Pitkin (1996), Hausmann (1996) and Holloway (1996). Most recently, Viidalepp (2017) recognized 25 genera in Nemoriini and summarized three main features: the rod-shaped uncus of the male genitalia, the specific shape of the eighth abdominal sternite of the male abdomen and larvae with unclothed chalazae. Ferguson (1969) first erected Synchlorini and placed the genera Synchlora Guenée, Merochlora Prout (= Synchlora), Cheteoscelis Prout (= Synchlora) in it. Synchlorini is characterized by male genitalia in which the uncus is reduced and the socii are rigidly sclerotized, tapered and pointed (Pitkin, 1996). The tribe Comibaenini is a small-sized group in the Geometrinae and was first established by Inoue (1961), including the genera Comibaena Hübner (Chlorochromodes Warren and Comostolodes Warren as synonyms, and Colutoceras Warren as a subgenus) and Thetidia Boisduval. Hausmann (1996) added two new genera, Microbaena Hausmann and Proteuchloris Hausmann, and suggested that the tribe is monophyletic. Holloway (1996) recognized Comibaenini (as subtribe Comibaeniti) as a discrete group. He included the genera Comibaena, Argyrocosma Turner, Comostolodes (with Chlorochromodes and Hercoloxia as synonyms of Comostolodes) and Thetidia, and added a new genus, Protuliocnemis Holloway. Han, Galsworthy & Xue (2012) reviewed Comibaenini worldwide, embracing eight genera: Comibaena, Microbaena, Thetidia, Proteuchloris, Linguisaccus Han et al., Chlorochromodes, Argyrocosma and Protuliocnemis. The most distinctive feature of Comibaenini is the bifid vinculum of the male genitalia. This study sampled five known genera of Comibaenini and the monophyly of Comibaenini is well supported. Within the tribe, Protuliocnemis + Argyrographa are sister to Linguisaccus + (Comibaena + Thetidia). Comibaena and Thetidia are closely related, and Comibaena is paraphyletic, in that Th. chlorophyllaria (Hedemann) and Th. albocostaria (Bremer) are nested within Comibaena, indicating that these two species may be transferred to Comibaena. Han et al. (2012) discussed the similarity among some species of Comibaena (C. hypolampes Prout, C. cenocraspis Prout, C. latilinea Prout and C. swanni Prout) and Thetidia, stating that the frenulum is present in Comibaena species but absent in Thetidia. Prout (1932: 20) regarded the absence or presence of a frenulum in the male as an important character at the level of genus and above. However, Pitkin (1996) stated that both states can occur within a genus, giving as examples Synchlora, Oospila, Chloractis Warren and Phrudocentra Warren. Therefore, it is possible to include Thetidia in Comibaena. Given the morphological diversity of Comibaena members, it is also possible that it needs to be split into different genera. Previous studies have shown a close relationship among Nemoriini, Synchlorini and Comibaenini. Ferguson (1985) stated that Synchlorini have much more in common with Nemoriini, and he would have included the Synchlorini in Nemoriini, were it not for differences in genitalia, venation and larval behaviour. In contrast, Pitkin (1993) stated that the genital differences between Synchlorini and Nemoriini appear insufficient to justify separating tribal status, and deferred formal synonymy due to a lack of information on the early stages of some other important genera, such as Lissochlora Warren and Chavarriella Pitkin. Later, Pitkin (1996) mentioned that some genera in Nemoriini share a similar valva structure with Synchlora (Synchlorini) and Chlorissa (Hemitheini), and continued using Synchlorini, adding Xenopepla Warren to it. Holloway (1996) stated that Synchlorini are probably related to Comibaenini, based on the larval habit of attaching debris and some aspects of genitalic structure. In summary, these three tribes are closely related, as shown by their similar larval behaviour and some genitalic features. In this analysis, Nemoriini, Synchlorini and Comibaenini form a monophyletic clade with strong support. The tribe Synchlorini is clustered with Nemoria Hübner with full support, and Comibaenini is recovered as sister to Pyrochlora with moderate support. A similar result was found by Sihvonen et al. (2011), unsurprisingly, as the data for Nemoriini (Nemoria, Pyrochlora) and Synchlorini (Synchlora) used in the current study were mainly obtained from their research. The monophyly of Nemoriini is not supported by the present concept, under which it would be a monophyletic group with the inclusion of Synchlorini and Comibaenini. Considering that only five species in three genera of Nemoriini are included in our analysis, and there are more than 130 species in Nemoria alone, we defer a decision on this synonymy at present. Further analysis, including additional taxa, is needed to determine the relationship among these tribes and the position of Pyrochlora. Timandromorphini Inoue (1961) erected Timandromorphini based on a single genus, Timandromorpha Inoue. The diagnostic characters were summarized in Inoue (1961), Hausmann (1996), Holloway (1996) and Han & Xue (2011a). Holloway (1996) stated that the Timandromorphini share a modified eighth segment of the male abdomen with the Aracimini and referred to the fact that the ovipositor lobes of the female genitalia are intermediate between the typical type of Geometrinae (oblique and papillate) and the modified type of Geometrini (more sclerotized, smoother and slenderer). Although in Sihvonen et al. (2011), Timandromorpha is a sister to Aracimini, in this study, Timandromorphini is the sister-group to Geometrini, indicating a close relationship to the latter. Geometrini Geometra, the type genus of this tribe, its subfamily and family, and its junior synonym, Hipparchus (both with papilionaria as type species), have been used in the past to describe a number of species that were later split amongst several sections or subgenera on the basis of wing shape and features of the palpus and antenna by Prout (1912, 1920–41). Most subgenera were later synonymized with Geometra, with the exception of Neohipparchus and Chloroglyphica, which were placed in Sections C and D of Hipparchus in Prout (1920–41). Prout (1912–16, 1920–41) stated that Tanaorhinus is scarcely more than a subgenus of Hipparchus (Geometra), with a more or less strongly falcate apex. Section C of Tanaorhinus (as Timandromorpha), Geometra smaragdus (Butler) and G. sinoisaria Oberthür are to some extent intermediate. The species of section B of Tanaorhinus belong to Mixochlora. Prout’s statements and treatment indicated a close relationship among Geometra, Tanaorhinus, Mixochlora, Neohipparchus, Chloroglyphica and Timandromorpha. Inoue (1961) included Geometra, Tanaorhinus and Mixochlora in Geometrini for the Japanese fauna based on the absence of abdominal crests, the separated CuA1 and M3, and the structure of the male genitalia. Holloway (1996) followed Inoue’s tribes, emphasizing the distinctive ovipositor lobes of the Geometrini, which are smoother, more sclerotized and more elongated than those of other tribes. He also noted that Timandromorphini, Neohipparchini and Aracimini are perhaps related to Geometrini. Hausmann (1996) provided a wider concept of Geometrini, including Paramaxates (Aracimini), Neohipparchus (Neohipparchini), Chlororithra, Iotaphora, Ornithospila, Sphagnodela, Mixochlora and Tanaorhinus in addition to the type genus Geometra, and synonymized Neohipparchini with Geometrini. Han & Xue (2011a) first placed Chlorozancla into Geometrini, due to the similar wing shape and male genitalia, but they also noted that a developed, collar-like colliculum in the female genitalia is absent in Chlorozancla but present in Geometra, Tanaorhinus and Mixochlora. In the present concept of Geometrini, Mixochlora and Chlorozancla constitute a monophyletic clade, which is sister to the clade embracing Geometra and Tanaorhinus. Han, Galsworthy & Xue (2009) stated that the monophyly of Geometra is highly questionable and that a full phylogenetic revision would probably entail splitting the genus. Those authors also split Geometra into two species-groups (smaragdus group and papilionaria group) based on the male genitalia, with three species, glaucaria Ménétriés, rana (Oberthür) and sigaria (Oberthür), not placed in any group. The authors mentioned that on the basis of the male genitalia, some species in Tanaorhinus centred around kina Swinhoe are similar to the smaragdus group of Geometra, whereas another group centred around Tanaorhinus rafflesii (Moore) is similar to the papilionaria group. This opinion was validated in this study, in which Tanaorhinus kina is clustered with Geometra fragilis (Oberthür), G. sinoisaria and G. smaragdus (smaragdus-group of Geometra) with full support and Tanaorhinus reciprocata confuciaria (Walker) (type species of Tanaorhinus), T. viridiluteata (Walker) and T. luteivirgatus Yazaki & Wang are clustered with most species of the papilionaria group with full support. Although not all species of Geometra and Tanaorhinus were sampled, we propose, on the basis of the combination of morphological characters and molecular analysis, that T. kina, G. fragilis, G. sinoisaria, G. smaragdus and most likely G. burmensis and T. tibeta Chu (Han et al., 2009: fig. 2: L–O; Han & Xue, 2011a: fig. 161; Orhant, 2014: photograph 6) should be placed in a separate genus. The genus Loxochila Butler stat. rev., which was established based on Tanaorhinus smaragdus Butler, was treated as a subgenus of Hipparchus by Prout (1912, 1920–41) but as a valid genus by Fletcher (1979) and is listed as a synonym of Geometra by Scoble (1999). Here, we revive its generic status and transfer the species mentioned above to it as L. smaragdus stat. rev., L. kinacomb. nov., L. fragiliscomb. nov., L. sinoisariacomb. nov., L. burmensiscomb. nov. and L. tibetacomb. nov. We also tentatively speculate that Tanaorhinus reciprocata (Walker), T. viridiluteata and perhaps T. celebensis Yazaki, T. dohertyi Prout, T. rafflesii, T. unipuncta Warren, T. waterstradti Prout, T. philippinensis Yazaki and T. luteivirgatus should be combined into Geometra. However, further molecular studies, including additional taxa, are needed to confirm this hypothesis. SUPPORTING INFORMATION Additional Supporting Information may be found in the online version of this article at the publisher’s web-site: Table S1. List of specimens and GenBank accession numbers. Table S2. Primers and annealing temperatures used for PCR and cycle sequencing. Table S3. Parameters and partitions assigned according to PARTITIONFINDER 1.1.1. Figure S1. Phylogenetic tree of Geometrinae from the ML analysis excluding the 28S gene fragment. [Version of Record, published online 15 May 2018; http://zoobank.org/urn:lsid:zoobank.org:pub:D2792250- B5CA-4917-A2EA-EBCBE1B42E70] ACKNOWLEDGEMENTS We are grateful to all collectors whose contributions made our work possible. We thank Professor Aibing Zhang (Capital Normal University, Beijing, China) for kindly providing the DNA of Pamphlebia rubrolimbraria, and thank Professor Jaan Viidalepp (Estonian University of Life Sciences, Estonia) for sending us valuable literature. We thank Dr Chaodong Zhu (Institute of Zoology, Chinese Academy of Sciences, Beijing, China) for providing valuable suggestions on selecting genes. We sincerely appreciate Dr Axel Hausmann (Zoologische Staatssammlung München, Munich, Germany) and two anonymous referees for the valuable comments to the manuscript. We are grateful for Sir Anthony Galsworthy (The Natural History Museum, London, UK) for correcting the English. This work was supported by the National Science Foundation of China (No. 31672331, 31372176, 31702041) and the Ministry of Science and Technology of China (No. 2015FY210300). REFERENCES Abraham D , Ryrholm N , Wittzell H , Holloway JD , Scoble MJ , Löfstedt C . 2001 . Molecular phylogeny of the subfamilies in Geometridae (Geometroidea: Lepidoptera) . Molecular Phylogenetics and Evolution 20 : 65 – 77 . Google Scholar CrossRef Search ADS Beljaev EA . 2007 . Taxonomic changes in the emerald moths (Lepidoptera: Geometridae, Geometrinae) of East Asia, with notes on the systematics and phylogeny of Hemitheini . Zootaxa 1584 : 55 – 68 . Beljaev EA . 2008 . Phylogenetic relationships of the family Geometridae and its subfamilies (Lepidoptera) . Meetings in Memory of N. A. Cholodkovsky . Iss. 60 . St. Petersburg ; 1 – 283 . [in Russian with English abstract.] . Beljaev EA . 2016 . Sem. Geometridae – Pyadenitzi [Fam. Geometridae – Geometer moth] . In: Lelei AS , ed. Annotated catalogue of the insects of Russian Far East, Vol. II. Lepidoptera . Vladivostok, Russia Dalnauka , 518 – 666 . Belshaw R , Quicke DLJ . 1997 . A molecular phylogeny of the Aphidiinae (Hymenoptera, Braconidae) . Molecular Phylogenetics and Evolution 7 : 281 – 293 . Google Scholar CrossRef Search ADS Canfield MR , Greene E , Moreau CS , Chen N , Pierce NE . 2008 . Exploring phenotypic plasticity and biogeography in emerald moths: a phylogeny of the genus Nemoria (Lepidoptera: Geometridae) . Molecular Phylogenetics and Evolution 49 : 477 – 487 . Google Scholar CrossRef Search ADS Cheng R , Jiang N , Xue DY , Li XX , Ban XS , Han HX . 2016 . The evolutionary history of Biston suppressaria (Guenée) (Lepidoptera: Geometridae) related to complex topography and geological history . Systematic Entomology 41 : 732 – 743 . Google Scholar CrossRef Search ADS Cook MA . 1993 . The systematics of Emerald Moths (Geometridae, Geometrinae): wing pigments, tympanal organs and a revision of the neotropical genus Oospila Warren . Unpublished D. Phil. Thesis, Oxford University . Cook MA , Harwood LM , Scoble MJ , McGavin GC . 1994 . The chemistry and systematic importance of the green wing pigment in emerald moths (Lepidoptera: Geometridae, Geometrinae) . Biolchemical Systematics and Ecology 22 : 43 – 51 . Google Scholar CrossRef Search ADS Cummins CA , McInerney JO . 2011 . A method for inferring the rate of evolution of homologous characters that can potentially improve phylogenetic inference, resolve deep divergence and correct systematic biases . Systematic Biology 60 : 833 – 844 . Google Scholar CrossRef Search ADS Ferguson DC . 1969 . A revision of the moths of the subfamily Geometridae of America, north of Mexico (Insecta, Lepidoptera) . Bulletin of the Peabody Museum of Natural History 29 : 1 – 251 . Ferguson DC . 1985 . Geometroidea, geometridae (part): subfamily geometrinae . In: Ferguson DC , Lawrence LH , Paige EM , Dominick RB , eds. The moths of America North of Mexico (Lepidoptera). Fascicle 18.1 . Washington, DC : Wedge Entomological Research Foundation , 1 – 131 . Fletcher DS . 1979 . Geometroidea . In: Nye IWB , ed. The generic names of moths of the World , Vol. 3 . London : British Museum (Natural History) ; 1 – 243 . Folmer O , Black M , Hoeh W , Lutz R , Vrijenhoek R . 1994 . DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates . Molecular Marine Biology and Biotechnology 3 : 294 – 299 . Forbes WTM . 1948 . Lepidoptera of New York and neighboring states. II . Memoirs of the Cornell University Agricultural Experiment Station 274 : 1 – 263 . Forum Herbulot . 2007 . The Forum Herbulot World List of Family Group Names in Geometridae [WWW document] . Available at: http://www.herbulot.de/famgroup.htm [last accessed on 16 March 2017 ]. Gumppenberg CF. von . 1887 . Systema Geometrarum zonae temperatioris septentrionalis [part 1] . Nova Acta Academiae Caesareae Leopoldino Carolinae germanicae naturae curiosorum 49 : 233 – 400 . Gutell RR . 1996 . Comparative sequence analysis and the structure of 16S and 23S rRNA . In: Dahlberg AE , Zimmerman EA , eds. Ribosomal RNA structure, evolution, processing and function in protein synthesis . Boca Raton, FL : CRC Press , 111 – 129 . Hampson GF . 1895 . The fauna of British India, including Ceylon and Burma (Moths) . 3 : 1 – 546 . London : Taylor and Francis . Han HX . 2005 . A study on the systematics of Geometrinae from China (Lepidoptera: Geometridae) . A dissertation submitted for the degree of Doctor of Philosophy, Institute of Zoology, Chinese Academy of Sciences . Han HX , Xue DY . 2009 . Taxonomic review of Hemistola Warren, 1893 from China, with descriptions of seven new species (Lepidoptera: Geometridae, Geometrinae) . Entomological Science 12 : 382 – 410 . Google Scholar CrossRef Search ADS Han HX , Xue DY . 2011a . Fauna sinica (Insecta vol. 54, Lepidoptera, Geometridae, Geometrinae) . Beijing : Science Press [in Chinese with English abstract]. Han HX , Xue DY . 2011b . Thalassodes and related taxa of emerald moths in China (Geometridae, Geometrinae) . Zootaxa 3019 : 26 – 50 . Han HX , Galsworthy A , Xue DY . 2009 . A survey of the genus Geometra Linnaeus (Lepidoptera, Geometridae, Geometrinae) . Journal of Natural History 43 : 885 – 922 . Google Scholar CrossRef Search ADS Han HX , Galsworthy AC , Xue DY . 2012 . The Comibaenini of China (Geometridae: Geometrinae), with a review of the tribe . Zoological Journal of the Linnean Society 165 : 723 – 772 . Google Scholar CrossRef Search ADS Hausmann A . 1996 . The morphology of the geometrid moths of the Levant and neighbouring countries . Nota Lepidopterologica 19 : 3 – 90 . Hausmann A . 2001 . Introduction. Archiearinae, Orthostixinae, Desmobathrinae, Alsophilinae, Geometrinae . In: Hausmann A , ed. The geometrid moths of Europe, Vol. 1 . Stenstrup : Apollo Books , 1 – 282 . Hausmann A , Miller SE , Holloway JD , deWaard JR , Pollock D , Prosser SWJ , Hebert PDN . 2016a . Calibrating the taxonomy of a megadiverse insect family: 3000 DNA barcodes from geometrid type specimens (Lepidoptera, Geometridae) . Genome 59 : 671 – 683 . Google Scholar CrossRef Search ADS Hausmann A , Parisi F , Sciarretta A . 2014 . The geometrid moths of Ethiopia I: tribes Pseudoterpnini and Comibaenini (Lepidoptera: Geometridae, Geometrinae) . Zootaxa 3768 : 460 – 468 . Google Scholar CrossRef Search ADS Hausmann A , Sciarretta A , Parisi F . 2016b . The Geometrinae of Ethiopia II: tribus Hemistolini, genus Prasinocyma (Lepidoptera: Geometridae, Geometrinae) . Zootaxa 4065 : 1 – 63 . Google Scholar CrossRef Search ADS Hedtke SM , Townsend TM , Hillis DM . 2006 . Resolution of phylogenetic conflict in large data sets by increased taxon sampling . Systematic Biology 55 : 522 – 529 . Google Scholar CrossRef Search ADS Heppner JB , Inoue H . 1992 . Lepidoptera of Taiwan. Volume 1, part 2: Checklist . Gainsville, Florida : Association for Tropical Lepidoptera and Scientific Publishers . Herbulot C . 1963 . Mise a jour de la liste des Geometridae de France . Alexanor 3 : 17 – 24 . Holloway JD . 1996 . The moths of Borneo: family Geometridae, subfamilies Oenochrominae, Desmobathrinae and Geometrinae . The Malayan Nature Journal 49 : 147 – 326 . Holloway JD . 1997 . The moths of Borneo: family Geometridae, subfamilies Sterrhinae and Larentiinae . The Malayan Nature Journal 51 : 1 – 241 . Holloway JD . 2011 . The moths of Borneo: families Phaudidae, Himantopteridae and Zygaenidae; revised and annotated checklist . The Malayan Nature Journal 63 : 1 – 548 . Inoue H . 1961 . Lepidoptera: Geometridae . Insecta Japonica 4 : 1 – 106 , Tokyo : Hokuryukan . Inoue H . 2006 . Thalassodes-group of emerald moths from Sulawesi and the Philippine Islands (Geometridae, Geometrinae) . Tinea 19 : 214 – 243 . Jiang N , Li XX , Hausmann A , Cheng R , Xue DY , Han HX . 2017 . A molecular phylogeny of the Palaearctic and Oriental members of the tribe Boarmiini (Lepidoptera: Geometridae: Ennominae) . Invertebrate Systematics 31 : 427 – 441 . Google Scholar CrossRef Search ADS Katoh K , Toh H . 2008 . Recent developments in the MAFFT multiple sequence alignment program . Briefings in Bioinformatics 9 : 286 – 298 . Google Scholar CrossRef Search ADS Lalitha S . 2000 . Primer premier 5 . Biotech Software & Internet Report 1 : 270 – 272 . Google Scholar CrossRef Search ADS Lanfear R , Calcott B , Ho SYW , Guindon S . 2012 . PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses . Molecular Biology and Evolution 29 : 1695 – 1701 Google Scholar CrossRef Search ADS Lederer J . 1853 . Versuch die europäischen Lepidopteren in möglichst natürliche Reihenfolge zu stellen, nebst Bemerkungen zu einigen Familien und Arten . Verhandlungen der Zoologisch-Botanischen Gesellschaft in Wien 3 : 165 – 270 . Marvaldi AE , Duckett CN , Kjer KM , Gillespie JJ . 2009 . Structural alignment of 18S and 28S rDNA sequences provides insights into phylogeny of Phytophaga (Coleoptera: Curculionoidea and Chrysomeloidea) . Zoologica Scripta 38 : 63 – 77 . Google Scholar CrossRef Search ADS McGuffin WC . 1988 . Guide to the Geometridae of Canada (Lepidoptera). 3, 4, and 5. Subfamilies Archiearinae, Oenochrominae, and Geometrinae . Memoirs of the Entomological Society of Canada 145 : 1 – 56 . McQuillan PB , Edwards ED . 1996 . Geometridae . In: Nielsen ES , Edwards ED , Rangsi TV , eds. Checklist of the Lepidoptera of Australia. Monographs on Australian Lepidoptera, Vol. 4 . Melbourne : CSIRO , 200 – 228 . Mengual X , Ståhls G , Rojo S . 2015 . Phylogenetic relationships and taxonomic ranking of pipizine flower flies (Diptera: Syrphidae) with implications for the evolution of aphidophagy . Cladistics 31 : 491 – 508 . Google Scholar CrossRef Search ADS Meyrick E . 1892 . On the classification of the Geometrina of the European fauna . Transactions of the Royal Entomological Society of London 1892 : 53 – 140 . Miller MA , Pfeiffer W , Schwartz T . 2010 . Creating the CIPRES Science Gateway for inference of large phylogenetic trees . In: Proceedings of the Gateway Computing Environments Workshop (GCE) . New Orleans, LA : IEEE , 1 – 8 . Müller B . 1996 . Geometridae . In: Karsholt O , Razowski J , eds. The Lepidoptera of Europe, a distributional checklist . Stenstrup : Apollo Books , 218 – 249 . Mutanen M , Wahlberg N , Kaila L . 2010 . Comprehensive gene and taxon coverage elucidates radiation patterns in moths and butterflies . Proceedings of the Royal Society B 277 : 2839 – 2848 . Google Scholar CrossRef Search ADS Orhant G . 2014 . Contribution à la connaissance du genre Tanaorhinus description d’une nouvelle espèce des Moluques Découverte et description du male de Tanaorhinus tibeta CHU, 1982 (Lepidoptera, Geometridae, Geometrinae) . Bulletin de la Société Entomologique de Mulhouse 70 : 59 – 64 . Õunap E , Viidalepp J , Saarma U . 2008 . Systematic position of Lythriini revised: transferred from Larentiinae to Sterrhinae (Lepidoptera, Geometridae) . Zoologica Scripta 37 : 405 – 413 . Google Scholar CrossRef Search ADS Õunap E , Javois J , Viidalepp J , Tammaru T . 2011 . Phylogenetic relationships of selected European Ennominae (Lepidoptera: Geometridae) . European Journal of Entomology 108 : 267 – 273 . Google Scholar CrossRef Search ADS Õunap E , Viidalepp J , Truuverk A . 2016 . Phylogeny of the subfamily Larentiinae (Lepidoptera: Geometridae): integrating molecular data and traditional classifications . Systematic Entomology 41 : 824 – 843 . Google Scholar CrossRef Search ADS Pitkin LM . 1993 . Neotropical emerald moths of the genera Nemoria, Lissochlora and Chavarriella, with particular reference to the species of Costa Rica (Lepidoptera: Geometridae, Geometrinae) . Bulletin of the Natural History Museum, London (Entomology) 62 : 39 – 159 . Pitkin LM . 1996 . Neotropical emerald moths: a review of the genera (Lepidoptera: Geometridae, Geometrinae) . Zoological Journal of the Linnean Society 118 : 309 – 440 . Google Scholar CrossRef Search ADS Pitkin LM , Han HX , James S . 2007 . Moths of the tribe Pseudoterpnini (Geometridae: Geometrinae): a review of the genera . Zoological Journal of the Linnean Society 150 : 343 – 412 . Google Scholar CrossRef Search ADS Posada D , Buckley T . 2004 . Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests . Systematic Biology 53 : 793 – 808 . Google Scholar CrossRef Search ADS Prout LB . 1912 . Lepidoptera Heterocera, fam. Geometridae, subfam. Hemitheinae . In: Wytsman P , ed. Genera insectorum , 129 . Bruxelles : Verteneuil & Desmet . Prout LB . 1912–16 . The Palaearctic Geometrae . In: Seitz A , ed. The macrolepidoptera of the world4 . Stuttgart : Verlag A. Kernen . Prout LB . 1920–41 . The Indoaustralian Geometridae . In: Seitz A , ed. The macrolepidoptera of the world 12 . Stuttgart : Verlag A. Kernen . Prout LB . 1934–38 . The Palaearctic Geometrae, 3. Subfam. Hemitheinae . In: Seitz A , ed. The macrolepidoptera of the world 4 (Suppl.) . Stuttgart : Verlag A. Kernen . Rota J , Wahlberg N . 2012 . Exploration of data partitioning in an eight-gene data set: phylogeny of metalmark moths (Lepidoptera, Choreutidae) . Zoologica Scripta 41 : 536 – 546 . Google Scholar CrossRef Search ADS Schnare MN , Damberger SH , Gray MW , Gutell RR . 1996 . Comprehensive comparison of structural cahracteristics in eukaryotic sytoplasmatic large subunit (23S-like) ribosomal RNA . Journal of Molecular Evolution 256 : 701 – 719 . Scoble MJ , ed. 1999 . Geometrid moths of the world: a catalogue (Lepidoptera, Geometridae) . Collingwood : CSIRO Publishing . Scoble MJ , Hausmann A. (updated 2007 ). Online list of valid and available names of the Geometridae of the world . Available at: http://www.lepbarcoding.org/geometridae/ species_checklists.php (last accessed 9 March 2017) . Sihvonen P , Mutanen M , Kaila L , Brehm G , Hausmann A , Staude HS . 2011 . Comprehensive molecular sampling yields a robust phylogeny for Geometrid moths (Lepidoptera: Geometridae) . PLoS One 6 : e20356 . Google Scholar CrossRef Search ADS Sihvonen P , Staude HS , Mutanen M . 2015 . Systematic position of the enigmatic African cycad moths: an integrative approach to a nearly century old problem (Lepidoptera: Geometridae, Diptychini) . Systematic Entomology 40 : 606 – 627 . Google Scholar CrossRef Search ADS Snäll N , Tammaru T , Wahlberg N , Viidalepp J , Ruohomäki K , Savontaus ML , Huoponen K . 2007 . Phylogenetic relationships of the tribe Operophterini (Lepidoptera, Geometridae): a case study of the evolution of female flightlessness . Biological Journal of the Linnean Society 92 : 241 – 252 . Google Scholar CrossRef Search ADS Stamatakis A , Hoover P , Rougemont J . 2008 . A rapid Bootstrap algorithm for the RAxML web-servers . Systematic Biology 75 : 758 – 771 . Google Scholar CrossRef Search ADS Stekolnikov AA , Kuznetzov VI . 1981 . Functional morphology of the male genitalia and notes on the system of the subfamily Geometrinae (Lepidoptera, Geometridae) . Entomological Review, Washington 60 : 37 – 54 . Strutzenberger P , Brehm G , Bodner F , Fiedler K . 2010 . Molecular phylogeny of Eois (Lepidoptera, Geometridae): evolution of wing patterns and host plant use in a species rich group of Neotropical moths . Zoologica Scripta 39 : 603 – 620 . Google Scholar CrossRef Search ADS Tamura K , Stecher G , Peterson D , Filipski A , Kumar S . 2013 . MEGA6: molecular evolutionary genetics analysis version 6.0 . Molecular Biology and Evolution 30 : 2725 – 2729 . Google Scholar CrossRef Search ADS Viidalepp J . 1981 . On the suprageneric systematics of Geometridae subfamily (Lepidoptera: Geometridae) [In Russian]. Horae Societatis Entomologicae Unionis Soveticae 63 : 90 – 95 . Viidalepp J . 1996 . Checklist of the Geometridae (Lepidoptera) of the former U.S.S.R . Stenstrup: Apollo Books . Viidalepp J . 2017 . A morphology based key to the genera of the tribe Nemoriini (Lepidoptera: Geometridae, Geometrinae) . Zootaxa 4236 : 521 – 532 . Google Scholar CrossRef Search ADS Vives Moreno A . 1994 . Catálogo sistemático y sinonímico de los Lepidópteros de la Peninsula Ibérica y Baleares (Insecta: Lepidoptera, II) . Pesca y Alimentacion, Madrid : Ministerio de Agricultura , 775 . Wahlberg N , Wheat CW . 2008 . Genomic outposts serve the phylogenomic pioneers: designing novel nuclear markers for genomic DNA extractions of Lepidoptera . Systematic Biology 57 : 231 – 242 . Google Scholar CrossRef Search ADS Wahlberg N , Snäll N , Viidalepp J , Ruohomäki K , Tammaru T . 2010 . The evolution of female flightlessness among Ennominae of the Holarctic forest zone (Lepidoptera, Geometridae) . Molecular Phylogenetics and Evolution 55 : 929 – 938 . Google Scholar CrossRef Search ADS Warren W . 1893 . On new genera and species of moths of the family Geometridae from India, in the collection of H. J. Elwes . Proceedings of the Zoological Society of London 1893 : 341 – 434 . Warren W . 1894 . New genera and species of Geometridae . Novitates Zoologicae 1 : 366 – 466 . Google Scholar CrossRef Search ADS Warren W . 1895 . New species and genera of Geometridae in the Tring Museum . Novitates Zoologicae 2 : 82 – 159 . Young C . 2006 . Molecular relationships of the Australian Ennominae (Lepidoptera: Geometridae) and implications for the phylogeny of the Geometridae from molecular and morphological data . Zootaxa 1264 : 1 – 147 . Yamamoto S , Sota T . 2007 . Phylogeny of the Geometridae and the evolution of winter moths inferred from a simultaneous analysis of mitochondrial and nuclear genes . Molecular Phylogenetics and Evolution 44 : 711 – 723 . Google Scholar CrossRef Search ADS © 2018 The Linnean Society of London, Zoological Journal of the Linnean Society This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Zoological Journal of the Linnean Society Oxford University Press

Tribal classification and phylogeny of Geometrinae (Lepidoptera: Geometridae) inferred from seven gene regions

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© 2018 The Linnean Society of London, Zoological Journal of the Linnean Society
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Abstract

Abstract Despite recent progress in the molecular systematics of Geometridae, phylogenetic relationships within the subfamily 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 classification 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. © 2018 The Linnean Society of London, Biological Journal of the Linnean Society, 2018, XX, 000–000 Insecta, molecular phylogeny, new taxa, revision INTRODUCTION Geometridae is one of the three most species-rich families of Lepidoptera, with approximately 23000 described species (Scoble, 1999; Scoble & Hausmann, 2007). Caterpillars of this family are known as loopers or inchworms because of their looping gait, due to a reduced number of abdominal prolegs. Geometridae has long attracted the interest of dedicated researchers at leading institutions around the world, and much progress has been made towards a better understanding of geometrid taxonomy and systematics (Pitkin, Han & James, 2007). The subfamily Geometrinae, commonly known as emerald moths, is the third largest subfamily in Geometridae, with more than 2500 described species in 268 genera worldwide (Scoble & Hausmann, 2007). Geometrinae is particularly diverse in tropical areas, and the caterpillars mainly feed on various trees and shrubs (Pitkin, 1996). Holloway (1996) and Pitkin (1996) summarized the main defining characters of Geometrinae, among which the predominance of green pigment (geoverdin) is synapomorphic with Geometrinae (Cook et al., 1994) and the shape of the ansa of the tympanal organ supports the monophyly of Geometrinae (Hausmann, 2001). The other characters are: wings are mostly green in colour, the frenulum tends to be reduced, the third sternite of the male often possesses a pair of setal patches, the socii of the male genitalia are usually well developed, the vinculum is distally cruciform in structure, the sclerotization of the aedeagus is usually reduced to a ventral strip along its length, and the female genitalia have oblique and papillate ovipositor lobes and a bicornute signum. Both Hausmann (2001) and Han & Xue (2011a) mentioned venation characters: forewing usually without an areole, hindwing with vein M2 close to M1 and far from M3. Beljaev (2008) summarized 12 apomorphies of Geometrinae by adding the results of his study of the skeleto-muscular system of the male genitalia. Since very early studies, the subfamily Geometrinae has been considered a natural entity; it was treated as Group I in Lederer (1853), as Geometridae in Meyrick (1892), as Geometrinae in Hampson (1895) and as Hemitheinae in Prout (1912, 1912–16, 1920–41). The monophyly of Geometrinae is also well supported by later molecular studies, such as those of Yamamoto & Sota (2007) and Sihvonen et al. (2011). Holloway (1997) provided the first tentative phylogeny for Geometridae, which was established mostly based on characters of the adult male and female abdomen, and showed a sister relationship between Geometrinae and Desmobathrinae. Yamamoto & Sota (2007) found that Geometrinae was a sister-group to Oenochrominae. In the molecular phylogenetic analysis of Sihvonen et al. (2011), Oenochrominae s.s. or Oenochrominae s.s. + Desmobathrinae was considered a sister-group to Geometrinae with weak support. Considerable progress has been made in systematics within Geometrinae. The major global taxonomic revision of Geometrinae was that of Prout (1912, 1934–38). Subsequently, many regional works on Geometrinae have been produced: Forbes (1948), Ferguson (1969, 1985) and McGuffin (1988) studied the Geometrinae of North America, Inoue (1961) reviewed the Japanese Geometrinae, Pitkin (1996) researched the neotropical Geometrinae, Holloway (1996) reviewed the Bornean Geometrinae, Hausmann (1996, 2001) investigated Geometrinae from the Levant and neighbouring countries and Europe, McQuillan & Edwards (1996) studied Australian Geometrinae, Viidalepp (1996) produced a checklist of Geometridae from the USSR and erected a new tribe, Hierochthoniini, Han & Xue (2011a) studied Chinese representatives, Hausmann, Parisi & Sciarretta (2014) and Hausmann, Sciarretta & Parisi (2016b) reviewed the Ethiopian Geometrinae (Parts I and II) and Beljaev (2016) published a catalogue of Geometrinae in the insects of the Russian Far East. Almost all of these researchers allocated genera of Geometrinae to tribes or groups. However, due to the lack of a global review, there is no consensus regarding the systematic placement of tribes and groups within Geometrinae and no clear understanding of the relationships between the tribes. Within Geometrinae, Holloway (1996) divided the subfamily into two tribes: Dysphaniini and Geometrini. The latter included almost all the geometrine species and almost all the known tribes as subtribes. Later, Holloway (2011) separated the tribe Pseudoterpnini from Geometrini. Pitkin (1996), Hausmann (1996) and Han & Xue (2011a) raised Holloway’s subtribes to the tribal level. Hausmann (1996) recognized 15 tribes and Forum Herbulot (2007) recognized 18 tribes for Geometrinae on a global basis. However, some tribal concepts remain controversial. For example, Holloway (1996) favoured a wide concept of Hemitheini embracing Thalerini, Comostolini, Hemistolini, Jodini and Thalassodini, whereas these taxa were treated as valid tribes by Hausmann (1996, 2001). Later, Thalassodini were synonymized with Hemistolini in Hausmann et al. (2016b). Beljaev (2016) proposed a much wider concept of Hemitheini by adding Rhomboristini (also Lophochoristini) and Microloxiini (also Hierochthoniini). The most likely reason for these controversies is that these systematic concepts were mainly drawn from morphological overviews and not based on phylogenetic analysis, although they sometimes utilized phylogenetic hints. The first morphology-based topology of Geometrinae was presented by Viidalepp (1981), who used various calculations to divide 26 genera into ten tribes based on 12 multi-state characters, erected the tribe Archaeobalbini and placed Pseudoterpnini sensuHerbulot, 1963 under Terpnini sensuInoue, 1961 as a subtribe. Stekolnikov & Kuznetzov (1981) presented two supertribes, Geometridii and Comibaenidii, based on the functional morphology of the male genitalia of ten geometrid species; the former included Geometrini, Ochrognesiini, Hemitheini and Hemistolini, and the latter included only Comibaenini. Cook (1993) conducted the first cladistic analysis based on 45 geometrine genera and 24 multistate characters. Although he stated that his dataset was insufficient to resolve the phylogeny of Geometrinae, the topology still showed that many known tribes (such as Thalassodini, Hemitheini, Thalerini, Jodini, Hemistolini, Comostolini, Synchlorini and Nemoriini) were grouped in one superclade, which somewhat supports some of the morphological results mentioned above. Han (2005) conducted a preliminary cladistic analysis of the tribe Geometrini, based on 71 morphological characters, and found that the monophyly of Geometra Linnaeus was doubtful, since the species were clustered in several different clades, and the phylogenetic relationships among genera were unclear. The rapid development of DNA sequencing techniques has accelerated the molecular phylogenetic analysis of Geometridae (Abraham et al., 2001; Young, 2006; Snäll et al., 2007; Yamamoto & Sota, 2007; Õunap, Viidalepp & Saarma, 2008; Strutzenberger et al., 2010; Wahlberg et al., 2010; Õunap et al., 2011; Sihvonen et al., 2011; Õunap, Viidalepp & Truuverk, 2016; Sihvonen, Staude & Mutanen, 2015). The most comprehensive taxon sampling at the tribal level was achieved by Sihvonen et al. (2011): 16 of 18 geometrine tribes sensuForum Herbulot (2007) and three genera of unknown affiliation were sampled, and a preliminary molecular phylogeny of Geometrinae was established on a global scale. Although the study included most tribes of Geometrinae, only one species was sampled for each of 11 tribes and a total of only 27 geometrine species in 25 genera representing Geometrinae were included. In addition, as the authors stated, the bootstrap values of most nodes were very low and most of the phylogenetic relationships in Geometrinae, with the exception of the position of the Dysphaniini, were not discussed. The relationships among the tribes of Geometrinae remain largely unexplored. This study aims to further investigate the phylogenetic relationships within Geometrinae at the tribal level, to test the monophyletic hypotheses of tribes, to revise the existing tribal classification within the subfamily and to revise the tribe Geometrini, which is mainly based on Palaearctic and Oriental genera, to cover almost all known tribes (except Dichordophorini) using one mitochondrial gene (COI) and six nuclear genes (EF-1α, CAD, GAPDH, RPS5, MDH and 28S). The results of this study will shed light on the tribal classification of the genera in Geometrinae, improve our understanding of the phylogenetic relationships within the subfamily at the global scale and provide a phylogenetic framework for studying the evolutionary history of Geometrinae. MATERIAL AND METHODS Taxon sampling A total of 116 species belonging to 56 genera representing 17 currently recognized Geometrinae tribes (with only one monobasic tribe, Dichordophorini, not sampled) were included in this study (Fig. 1). At least two species in each tribe, except Lophochoristini, were sampled to weaken the possible effects of long-branch attraction (Hedtke, Townsend & Hillis, 2006). These samples included 22 species of 19 genera downloaded from NCBI (https://www.ncbi.nlm.nih.gov/) that were sequenced by Canfield et al. (2008), Wahlberg et al. (2010), Mutanen, Wahlberg & Kaila (2010) and Sihvonen et al. (2011). We adopted 12 exemplars representing the other six subfamilies (Sterrhinae, Larentiinae, Archiearinae, Ennominae, Oenochrominae and Desmobathrinae) of Geometridae as outgroups. A list of taxa with the collecting localities, voucher codes and GenBank accession numbers is provided in the Supporting Information (Table S1). Some specimens are unidentified morphologically and molecularly on BOLD SYSTEMS due to insufficient taxonomy and constitute potential new species. A formal description of new species is, however, beyond the scope of this study. Figure 1. View largeDownload slide Representatives of the tribes of Geometrinae, sampled in the present study. A, Ornithospilini, Ornithospila esmeralda (Hampson); B, Agathiini, Agathia arcuata Moore; C–H, Hemitheini; C, Rhomboristiti, Rhomborista monosticta (Wehrli); D, Hemistoliti, Hemistola isommata Prout; E, Comostoliti, Comostola virago Prout; F, Hemitheiti, Hemithea aestivaria (Hübner); G, Joditi, Jodis irregularis (Warren); H, Thalassoditi, Thalassodes immissaria Walker; I, Xenozancla versicolor Warren; J, Dysphaniini, Dysphania militaris (Linnaeus); K, Pseudoterpnini, Pingasa rufofasciata Moore; L, Pseudoterpnini, Pachyodes novata Han & Xue; M, Chlorodontopera discospilata (Moore); N, Neohipparchini, Neohipparchus vallata (Butler); O, Aracimini, Aracima serrata Wileman; P, Nemoriini, Eucyclodes pastor Butler; Q, Comibaenini, Comibaena biplaga Walker; R, Iotaphora admirabilis (Oberthür); S, Timandromorphini, Timandromorpha discolor (Warren); T, Geometrini, Geometra papilionaria (Linnaeus); U, Geometrini, Tanaorhinus viridiluteata (Walker). Scale bar = 1 cm. Figure 1. View largeDownload slide Representatives of the tribes of Geometrinae, sampled in the present study. A, Ornithospilini, Ornithospila esmeralda (Hampson); B, Agathiini, Agathia arcuata Moore; C–H, Hemitheini; C, Rhomboristiti, Rhomborista monosticta (Wehrli); D, Hemistoliti, Hemistola isommata Prout; E, Comostoliti, Comostola virago Prout; F, Hemitheiti, Hemithea aestivaria (Hübner); G, Joditi, Jodis irregularis (Warren); H, Thalassoditi, Thalassodes immissaria Walker; I, Xenozancla versicolor Warren; J, Dysphaniini, Dysphania militaris (Linnaeus); K, Pseudoterpnini, Pingasa rufofasciata Moore; L, Pseudoterpnini, Pachyodes novata Han & Xue; M, Chlorodontopera discospilata (Moore); N, Neohipparchini, Neohipparchus vallata (Butler); O, Aracimini, Aracima serrata Wileman; P, Nemoriini, Eucyclodes pastor Butler; Q, Comibaenini, Comibaena biplaga Walker; R, Iotaphora admirabilis (Oberthür); S, Timandromorphini, Timandromorpha discolor (Warren); T, Geometrini, Geometra papilionaria (Linnaeus); U, Geometrini, Tanaorhinus viridiluteata (Walker). Scale bar = 1 cm. DNA extraction, amplification and sequencing We extracted total genomic DNA from adult unilateral legs that had been dried or freshly preserved in anhydrous ethanol using the DNeasy Blood and Tissue Kit (Qiagen, Beijing, China) following the protocol suggested by the manufacturer. In total, fragments of one mitochondrial protein-coding gene (COI), five nuclear protein-coding genes (EF-1α, CAD, GAPDH, RPS5 and MDH) and one nuclear rRNA gene (28S) were sequenced. These molecular markers have been widely used in reconstructing the phylogenies of different families of Lepidoptera (e.g. Wahlberg & Wheat, 2008; Rota & Wahlberg, 2012), especially Geometridae (e.g. Yamamoto & Sota, 2007; Wahlberg et al., 2010; Sihvonen et al., 2011). Several pairs of new primers were designed by PRIMER PREMIER 5.0 (Lalitha, 2000) based on sequences that were previously obtained using universal primers. The primer sequences and the annealing temperatures used for polymerase chain reactions (PCRs) are provided in the Supporting Information (Table S2), mainly from Folmer et al. (1994), Belshaw & Quicke (1997), Wahlberg & Wheat (2008) and our previous works (Cheng et al., 2016; Jiang et al., 2017). PCR was performed in a total volume of 25 μL; the reaction contained 12.5 μL of PCR 2×TSINGKETM Master Mix (TSINGKE, Beijing, China), 0.5 μL of each primer, 1 μL of the extracted DNA and 10.5 μL of ultrapure water. The cycling parameters were: a 5-min denaturing step at 95 °C followed by 30–40 cycles of 30 s at 94 °C, 30 s at a primer-specific annealing temperature, extension at 72 °C for 30 s to 1 min and final extension at 72 °C for 10 min. A 7-μL PCR mixture was examined on a 1.0% agarose gel to determine the quality and quantity of the PCR products before the sequencing reaction was performed. The remaining PCR product was sequenced using the same primers on an ABI PRISM 3730xl automated sequencer at BGI (Beijing Genomics Institute, China). Phylogenetic analyses The phylogenetic analyses were conducted both with, and excluding, the 28S rRNA gene fragment. The alignment of the 28S fragment is problematic due to the coexistence of a highly conserved core structure and highly variable regions (Gutell, 1996; Schnare et al., 1996; Marvaldi et al., 2009), and there is no consensus on how to use this gene fragment (Young, 2006; Mengual, Ståhls & Rojo, 2015; Õunap et al., 2016). In this study, all the 28S gene loci, after alignment by MAFFT, were used for phylogenetic analyses. Partial DNA sequences were downloaded from GenBank, due to the lack of samples. All sequences were manually edited using the SEQMAN module of the LASERGENE software package (DNASTAR, Madison, WI). Sequences of protein-coding genes were aligned using CLUSTALW as implemented in MEGA 6.0 (Tamura et al., 2013), and 28S rRNA segments D1 and D2 were concatenated and aligned in MAFFT v.6 (Katoh & Toh, 2008). Neighbour-joining trees for each gene were constructed using MEGA 6.0 to check the validity of each gene of every sample. Problematic sequences were re-analysed or removed from subsequent analyses. We obtained 153 samples yielding an assembly of 5805 bp of nucleotide data. A partition strategy based on the actual evolution rate of nucleotide data has been widely used in recent phylogenetic analyses (Õunap et al., 2016; Jiang et al., 2017). Rota & Wahlberg (2012) showed its advantages over partitioning by genes or codon positions in Lepidoptera. We partitioned the nucleotide dataset by the actual rate of evolution in the following analyses; the related substitution models are shown in the Supporting Information (Table S3). We used TIGER v.1.02 (Cummins & McInerney, 2011) to separate slowly evolving characters, which was expected to be more reliable for inferring deep divergences, from rapidly evolving characters, with the total bin number parameter set to 50. PARTITIONFINDER 1.1.1 (Lanfear et al., 2012) was used to select the most effective partitioning scheme according to the Bayesian information criterion (BIC) (Posada & Buckley, 2004) and to determine the best phylogenetic models for each dataset using the bins defined by TIGER. For the maximum likelihood (ML) analyses, PARTITIONFINDER was run with models = raxml and search = greedy options, whereas in the Bayesian analyses, models = mrbayes and search = greedy options were performed. The ML analyses were implemented in RAxML v.7.7.1 on the RAxML webserver (http://phylobench.vital-it.ch/raxml-bb/index.php) (Stamatakis et al., 2008) under the GTR+Gamma model for the final best-scoring ML tree. Bayesian phylogenetic reconstructions were generated using MRBAYES v.3.2 (Huelsenbeck & Ronquist 2001) on the CIPRES Science Gateway v. 3.1 (Miller, Pfeiffer & Schwartz, 2010), with the appropriate models and substitution rates. Four simultaneous Markov chains (one cold and three heated) were run for 10000 million generations until the split frequencies were below 0.01, sampling trees every 1000 generations and discarding 25% of the trees as burn-in. The software TRACER v.1.6 (Rambaut et al., 2014) was used both to estimate the sample sizes of the parameters in the Bayesian analyses and to check for the convergences or otherwise of the parallel MCMC runs. RESULTS The analyses conducted in this study are based on the sequence data from one mitochondrial gene region (1371 bp of COI), six nuclear gene regions (955 bp of EF-1α, 847 bp of CAD, 706 bp of GAPDH, 602 bp of RPS5, 474 bp of MDH and 850 bp of 28S rRNA). The final aligned data matrix contained 5805 nucleotide sites. The robustness of clades found is presented as posterior probabilities (PP, for the Bayesian analysis) or bootstrap values (BS, for the ML analysis). The two phylogenetic analyses (ML and Bayesian) of the combined datasets of seven gene regions yield almost identical topologies (Fig. 2). The analyses excluding 28S also yielded very similar topologies (Supporting Information, Fig. S1) except for several small differences in the terminal branches. Figure 2. View largeDownload slide View largeDownload slide Maximum likelihood phylogeny of the subfamily Geometrinae. Bootstrap support values from the ML analysis and posterior probabilities from Bayesian analysis indicated at the nodes as BS/PP. Figure 2. View largeDownload slide View largeDownload slide Maximum likelihood phylogeny of the subfamily Geometrinae. Bootstrap support values from the ML analysis and posterior probabilities from Bayesian analysis indicated at the nodes as BS/PP. The monophyly of Geometrinae is strongly supported in two phylogenetic analyses (PP = 1, BS = 100) in relation to the genera included in this study. Close to the root of Geometrinae, two genera, Ornithospila Warren and Agathia Guenée, branch off the main lineage, one after the other, with strong support. The tribes Rhomboristini, Heliotheini, Hemistolini, Comostolini, Hemitheini, Microloxiini, Thalerini, Lophochoristini, Jodini, Thalassodini and one unassigned genus Aporandria Warren are clustered in a clade with full support (PP = 1, BS = 100). In this clade, the tribe Rhomboristini is at the most basal position with very strong support (PP = 1, BS = 99). Three well-supported subclades within this clade are recognized: (1) Hemistolini and Comostolini constitute a monophyletic subclade with full support (PP = 1, BS = 100); (2) the monophyly of the subclade composed of Hemitheini, Microloxiini and Thalerini is well supported (PP = 1, BS = 94) – in this subclade, Thalerini is embedded in Hemitheini; (3) Jodini and Thalassodini, together with Aporandria, form a monophyletic clade (PP = 0.93, BS = 92) in which the monophyly of Thalassodini is fully supported, the sister relationship between Thalassodini and Aporandria is strongly supported and the monophyly of Jodini is not supported because Thalassodini + Aporandria form a sister-group to part of Jodini and are nested in Jodini. The genus Maxates Moore is shown as a non-monophyletic assemblage in which M. grandificaria Graeser and M. acutissima perplexata Prout cluster with Ecchloropsis Prout, and M. thetydaria Guenée, M. sp.1 and M. sp.2 cluster with Berta Walker and Jodis Hübner. The concept of Pseudoterpnini in Pitkin et al. (2007) is revealed to be polyphyletic. Pseudoterpna Hübner and Pingasa Moore form a monophyletic group with full support (PP = 1, BS = 100), and group with Dysphaniini with full support in Bayesian analyses but weak support in ML analyses (PP = 1, BS = 47), after clustering with Xenozancla Warren. However, many other genera (Herochroma Swinhoe, Metallolophia Warren, Absala Swinhoe, Actenochroma Warren, Metaterpna Yazaki, Limbatochlamys Rothschild, Psilotagma Warren, Dindica Moore, Dindicodes Prout, Lophophelma Prout and Pachyodes Guenée) are clustered in a separate clade with moderate support in Bayesian analyses (PP = 0.97) and weak support (BS = 57) in ML analyses. In this clade, the sister relationship between Limbatochlamys and Psilotagma is fully supported (PP = 1, BS = 100) and was first found in this study. The genera Dindica, Dindicodes, Lophophelma and Pachyodes are clustered together with full or strong support (PP = 1, BS = 98). A close relationship between Absala and Actenochroma was also identified for the first time. The remaining Geometrinae are clustered in a clade (PP = 0.97, BS = 62) embracing seven tribes and two unassigned genera: Chlorodontopera Warren, Aracimini, Neohipparchini, Nemoriini + Synchlorini + Comibaenini, Iotaphora Warren, Timandromorphini and Geometrini. The monophyly of Neohipparchini is well supported in both analyses (PP = 1, BS = 83). The tribe is redefined to accommodate Chlororithra Butler in addition to Neohipparchus Inoue and Chloroglyphica Warren. Aracimini is fully supported (PP = 1, BS = 100) as a monophyletic clade consisting of Paramaxates Warren, Dooabia Warren and Aracima Butler, with Aracima embedded within Dooabia. In the analyses excluding 28S, the position of Aracimini is exchanged with that of Neohipparchini (Supporting Information, Fig. S1). The tribes Nemoriini, Synchlorini and Comibaenini are clustered in one clade with strong support (PP = 0.98, BS = 99) but with the relationship among them was unresolved. The current concept of Nemoriini is polyphyletic, as Pyrochlora Warren is sister to Comibaenini in all trees. The monophyly of Comibaenini is well supported (PP = 1, BS = 88). The sister relationship between Timandromorphini and Geometrini is moderately supported (PP = 0.95, BS = 88), and the monophyly of both tribes is strongly to fully supported. In the tribe Geometrini, the sister relationship between Chlorozancla Prout and Mixochlora Warren is strongly supported (PP = 0.95, BS = 96). Members of Geometra and Tanaorhinus Butler are clustered in one clade with full support (BS = 100, PP = 1.00) and these genera are confirmed to be polyphyletic groups. DISCUSSION This study covers all tribes of the Geometrinae, except the North American tribe Dichordophorini Ferguson, which includes only one genus, Dichordophora Prout, making this study a comprehensive phylogenetic analysis to date of Geometrinae at the tribal level. Though 17 (18 in total) currently recognized tribes were included in this analysis, our sampling was mainly restricted to the Palaearctic and Oriental regions; the data are, therefore, not sufficient to elaborate the whole evolutionary story of Geometrinae. The genus Eumelea Duncan was transferred from Oenochrominae s.l. to Desmobathrinae by Holloway (1996), whilst the author pointed out that Eumelea lacks the definitive features of the desmobathrines. Beljaev (2008) considered Eumelea be a member of Geometrinae on the basis of the skeleto-muscular structure of the male genitalia, and pointed out that it may occupy a basal position in Geometrinae. In the same study, Beljaev doubted the desmobathrine position of the genus Celerena Walker (not sampled in the present study) and thought it a possible geometrine member. Although the affinity between Eumelea and Geometrinae is not directly supported in this study, the former is clustered with members of Desmobathrinae and Oenochrominae with poor support, so the possibility of Eumelea belonging to Geometrinae and occupying a basal position is not excluded. The multi-gene phylogeny determined in this study validates the monophyly of the subfamily Geometrinae and recovers 12 tribes (Dichordophorini not sampled), two of which are proposed as new. The tribes are Ornithospilini trib. nov., Agathiini trib. nov., Dysphaniini, Pseudoterpnini, Neohipparchini, Aracimini, Nemoriini, Synchlorini, Comibaenini, Timandromorphini, Geometrini and Hemitheini on a very broad concept embracing nine subtribes. Only three tribes (Dysphaniini, Comibaenini and Timandromorphini) are totally concordant with the previous morphology-based concepts of tribes recognized by Holloway (1996, as subtribes), Hausmann (1996) and Forum Herbulot (2007), and five tribes (Aracimini, Neohipparchini, Nemoriini, Synchlorini and Geometrini) are in rough agreement with them. Resolution of the inter-tribal relationships within Geometrinae remains limited, probably due to the limited sampling of taxa and molecular markers and sampling bias towards the Palaearctic and Oriental regions. The tribe Ornithospilini is the most basal taxon, followed by Agathiini. The sister relationship between Hemitheini and all the remaining geometrine groups is fully supported in Bayesian analyses and only weakly supported in ML analyses. In the clade composed of Chlorodontopera, Aracimini, Neohipparchini, Nemoriini + Synchlorini + Comibaenini, Iotaphora, Timandromorphini and Geometrini, Chlorodontopera and Neohipparchini are the most basal taxa, the close relationship among Nemoriini, Synchlorini and Comibaenini is strongly supported, and the close relationship between Timandromorphini and Geometrini is moderately supported. Holloway (1996) described the typical ovipositor lobes of Geometrinae (different from those of Dysphaniini) as follows: the distal margin of the ovipositor lobes recedes obliquely ventrally, and the setae are placed irregularly on papillate projections. He also noted that there are exceptions in the Geometrini, Timandromorphini, Paramaxates and Neohipparchini. Combined with the present tree (Fig. 2), there is one possible trend: the ovipositor lobes are inclined to be more sclerotized, smoother and slenderer in more evolved groups (e.g. Geometrini, Neohipparchini and Paramaxates). The modification of the ovipositor lobes may be related to oviposition preferences and larval host plants. Because the phylogenetic relationships among the tribes were not totally resolved, this hypothesis requires further testing with studies that clarify the phylogeny in Geometrinae by including more taxa and more genes. The following sections will describe the tribal classification of the Geometrinae, including the morphological characters and a short review of the main taxonomic histories of the respective groups, and the credible phylogenetic relationships inferred from the phylogenetic trees. Unless major changes occurred in one tribe, the differential features of the tribes will not be repeated. Ornithospilini Ban & Han trib. nov. Type genus: Ornithospila Warren, 1894 (Holloway, 1996: plate 7, figs 217–225 and 315–316; Han & Xue, 2011a: figs 20–22 of plate 18, figs 342–344, 661–663 and 865–866). Differential features: The wings of the members of Ornithospilini are bright green. The hind tibia of the male is not dilated. The veins Sc+R1 are close to the cell at one point, then separate rapidly on the hindwing; CuA1 and M3 are separate, and vein 3A is absent. Sternite 3 of the male abdomen lacks setal patches. The socii of the male genitalia are developed and are almost the same length as the uncus as in Hemitheini but sometimes with a basal process. The signum of the female genitalia, if present, is elongate, ovate and scobinate (Holloway, 1996). Ornithospilini is proposed as a new, currently monobasic tribe that is mainly distributed in the Oriental region. In this study, the Ornithospilini exemplars (two different species of Ornithospila) form a distinct group that occupies a basal position in Geometrinae. Prout (1912) placed Ornithospila in Group IV of the Old World genera and mentioned that it probably derived from Hipparchus (Geometra), but he also stated that the venation and genitalia of the type species agree better with Prasinocyma Warren and the Iodis group (Jodis). Later, Prout (1920–41) suggested that some species of Ornithospila are somewhat analogous to Aporandria in size, shape and coloration. Although Hausmann (1996) placed Ornithospila in Geometrini, he also referred to features that differentiate it from Geometrini, such as the presence of an uncus and the shorter and slightly sclerotized socii. Holloway (1996) considered Ornithospila as set apart from the rest of the Geometrinae by the condition of the female signum, which is elongate, ovate and scobinate. This opinion is supported here, as Ornithospila is positioned at the base of Geometrinae, and the relationship to Aporandria and Geometrini is not supported. Agathiini Ban & Han trib. nov. Type genus: Agathia Guenée, 1858 (Holloway, 1996: plates 7, 8 and 10, figs 194–211, 213–216, 239, 243; Han & Xue, 2011a: figs 22–28 of plate 19, figs 1–8 of plate 20, figs 371–385, 690–704 and 884–893). Differential features: Wings are bright green. The antennae are filiform in both males and females. The hind tibia of the male is dilated, with hair-pencil. The forewing usually possesses distinctive medial and terminal bands and a series of patches. Veins M3 and CuA1 are connate at the cell on the hindwing, and 3A is present. Sternite 3 of the male abdomen usually has a pair of setal patches. The two branches of the socii are close to each other and are fused at the base, resembling those of Pseudoterpna, Dooabia and Louisproutia Wehrli. The costa of the valva is ornamented with a dorsal process. In the female genitalia, the corpus bursae usually has a bicornute signum. Agathiini is established here as a new tribe, tentatively including only the genus, Agathia, represented by three species, including the type species of the genus Hypagathia Inoue (synonym of Agathia), Agathia carissima Butler. Agathia is a large genus, including 77 species worldwide (Scoble, 1999; Scoble & Hausmann, 2007) and is widely distributed in Southeast Asia, Australia and Africa. Inoue (1961), Viidalepp (1981), Hausmann (1996) and Beljaev (2016) placed Agathia in Pseudoterpnini (or Terpnini) mainly based on morphological studies. Stekolnikov & Kuznetzov (1981) suggested that it belongs to Ochrognesiini (Nemoriini) on the basis of the functional morphology (muscles) of the male genitalia. Holloway (1996) did not place it into any tribe and stated that it is unwise to erect a new tribe without a well-understood classification of Geometrinae in its entirety. In this study, species of Agathia form a distinct group that branched off after Ornithospilini and are placed in a more basal position, unlike the results of Sihvonen et al. (2011), in which Agathia is positioned at the base of the second major lineage with very weak support. The combination of the bright green wing colour, the structure of the socii and the presence of a dorsal ornament of the valva distinguish Agathiini from other known tribes. Hemitheini The concept of Hemitheini recognized here is broader than that of Holloway (1996) due to the inclusion of several additional tribes: Rhomboristini, Lophochoristini, Heliotheini and Microloxiini (= Hierochthoniini). For this study, the main characters of Hemitheini are: the male antennae are usually bipectinate; the moths are mainly bluish, emerald green or greyish green in colour; the outer margin of the hindwing bears a tail process in many genera; veins M3 and CuA1 of the hindwing are usually stalked (separate or connate in Rhomboristiti genera); most genera have a frenulum, but some do not (such as Berta, Comostola Meyrick, Hemistola Warren, Jodis, Thalera Hübner and Eucrostes Hübner); and the socii and uncus are similar in length and are usually closely adpressed (a strong uncus with weak socii in Rhomboristiti genera). Holloway (1996) stated that the larvae are usually slender and the resting posture is stick-like. The concept of Hemitheini has long been controversial and the internal structure has not been resolved, though some researchers suggested a close relationship among some groups. Viidalepp (1996) indicated a close relationship between Thalerini and Hemistolini, Jodini and Hemitheini by including Hemistola in Thalerini and genera of Jodini in Hemitheini, respectively. Hausmann (1996) noted that Thalerini, Hemistolini, Comostolini, Jodini, Hemitheini and Microloxiini are linked by various genera. For example, he stated that the venation of Rhomboristini corresponds to that of Jodini and Comostolini, some features of Comostolini resemble those of Hemistolini, Jodini has a relationship to Hemitheini and Thalerini is close to Hemitheini. Holloway (1996) introduced a wide concept of Hemitheini, embracing Thalerini, Comostolini, Hemistolini, Jodini and Thalassodini. He also synonymized Lophochoristini with Rhomboristini. Pitkin (1996) still treated Lophochoristini as a valid tribe. Beljaev (2007) stated that the transtilla of the type genus of Hemitheini is quite different from that of the other genera, which is similar to that in Jodini, Microloxiini and Hemistolini (sensuInoue, 1961 and Hausmann, 2001). He also indicated that Thalerini are probably subordinate to Hemitheini Bruand, 1946. The Hemitheini concept in Beljaev (2016) is wider, embracing Hemitheini Bruand, Comostolini, Jodini, Hemistolini, Thalassodini, Rhomboristini, Thalerini, Lophochoristini and Microloxiini (also Hierochthoniini). In this analysis, the broad concept of Hemitheini is fully supported and the monophyletic Hemitheini embrace almost all tribes mentioned in Beljaev (2016); the concept of Hemitheini by Beljaev is accepted here by the addition of Heliotheini (Petovia Walker). As Hemitheini is extremely large, some previous tribes are treated as subtribes, with subtribes equal to previous tribes. After the branching off of the genera Rhomborista Warren (Rhomboristiti) and Petovia (Heliotheiti), three well-supported subclades are recognized within Hemitheini: Hemistoliti + Comostoliti, Hemitheiti + Microloxiiti, and Joditi + Aporandria + Thalassoditi. Rhomboristiti The subtribe Rhomboristiti (as Rhomboristini) was established by Inoue (1961) as embracing three Indo-Australian genera, Rhomborista, Spaniocentra Prout and Rhombocentra Holloway, and was treated as a valid tribe by Holloway (1996). Holloway (1996) suggested the synonymy of Lophochoristiti and Heliotheiti with Rhomboristiti for three tribes sharing similar male genitalia with features such as a strong uncus with weak socii, a strong gnathos and often a doubled harpe-like process in the centre of the valva. Hausmann (1996) indicated that the hindwing venation of Rhomboristiti corresponds well with that of Comostola (Comostoliti) and Berta (Joditi). In this study, close relationships between Rhomboristiti, Lophochoristiti and Heliotheiti or between Rhomboristiti and Comostoliti were not supported; instead, Rhomboristiti constitutes a basal clade within Hemitheini with full support, implying its isolated position in Hemitheini. Hemistoliti + Comostoliti Hemistoliti and Comostoliti were both erected by Inoue (1961) as tribes. Hausmann (1996) summarized the differential features of these two groups, mentioned that some features of Comostoliti (e.g. the male genitalia) are reminiscent of Hemistoliti and stated that there is a close relationship between Comostoliti and Joditi. As in Sihvonen et al. (2011), the close relationship between Comostoliti and Hemistoliti, represented by the type genus of each, is fully supported here, validating the statement by Hausmann (1996). However, the monophyly of Hemistoliti is not supported, as Hemistola tenuilinea Alphéraky is sister to parts of Hemistoliti and Comostoliti. Therefore, we suggest that Comostoliti is a possible synonym of Hemistoliti and that further research, including more genera of Hemistoliti and Comostoliti, is needed. In this analysis, the close relationship between Comostoliti and Joditi is not directly supported, and the synonymization between Hemistoliti and Thalassoditi presented by Hausmann et al. (2016b) is not directly supported because the phylogeny of Hemitheini is not fully resolved. Hemitheiti + Microloxiiti The subtribe Hemitheiti (i.e Hemitheini s.s.), embracing 18 genera (Inoue, 1961; Ferguson, 1969, 1985; Hausmann, 1996; Pitkin, 1996; Viidalepp, 1996), is mainly characterized by the male genitalia, in which the uncus is slender, rod-like and pointed or tapered, and the socii are usually similar to the uncus in shape and size (Pitkin, 1996). In this study, Microloxiini, Hemitheini s.s. and Thalerini listed in Forum Herbulot (2007) are grouped in a clade with good support. The phylogenetic relationship within this clade is well resolved in Bayesian analyses, with the genus Episothalma Swinhoe at the most basal position. Microloxia Warren is sister to Pamphlebia Warren and then clusters with Hemithea Duponchel, Hethemia Ferguson falls within Thalera, and Chlorochlamys Hulst is clustered with Chloropteryx Hulst first and then grouped with Chlorissa Stephens. The type genus of the subtribe Thaleriti, Thalera, was placed in Hemitheini by Inoue (1961). Subsequently, Herbulot (1963) established Thaleriti (as Thalerini) based on Thalera. Hausmann (1996) stated that Hemitheiti is rather closely related to Thaleriti based on genitalic morphology. In this study, Thaleriti [including the type species of Thalera, Thalera fimbrialis (Scopoli)] are embedded in Hemitheiti [including the type species of Hemithea, Hemithea aestivaria (Hübner)]. Based on the similarities in the male genitalia of the Thaleriti and Hemitheiti, such as the similar shape and size of the uncus and the socii (Han & Xue, 2011a: figs 225, 353), Thaleriti (syn. nov.) can be synonymized with Hemitheiti. Accordingly, several other genera of Thaleriti, recognized by Hausmann (1996, 2001) (Culpinia Prout, Bustilloxia Expósito, Dyschloropsis Warren, Heteroculpinia Hausmann, Dolosis Prout and Kuchleria Hausmann), should be transferred into Hemitheiti. The subtribe Microloxiiti (as Microloxiini) was established by Hausmann (1996) and includes 11 genera. Externally, these genera share stalked M3 and CuA1 of the hindwing, and the presence of socii and uncus of similar lengths as the Hemitheiti. In this analysis, though Microloxia ruficornis Warren is embedded in Hemitheiti, it is not the type species and, therefore, does not necessarily represent the whole of Microloxia or even Microloxiiti. We, therefore, hesitate to synonymize Microloxiiti with Hemitheiti; the relationship between Microloxiiti and Hemitheiti needs further study with more taxa. The monotypic genus Hethemia, with Hethemia pistasciaria (Guenée) as the type species, is found in North America. In this study, Hethemia falls within Thalera, forms a monophyletic clade with Thalera fimbrialis (= type species of Thalera, T. thymiaria (Linnaeus)) and is, therefore, synonymized with Thalera (= Hethemiasyn. nov.). Pistasciaria is transferred to Thalera as Thalera pistasciariacomb. nov. This synonymy is also supported by morphological characters: the venation (Ferguson, 1969: pl. 5, fig. 5; Han & Xue, 2011a: fig. 63) of both genera is almost identical, except that M3 and CuA1 are stalked in Hethemia and sometimes CuA1 also diverges from the lower angle of the cell in Thalera. In the male genitalia, the two genera possess similar uncus, socii, gnathos and aedeagus (Ferguson, 1969: pl. 29, figs 1 and 2; reference to Han & Xue 2011a, related figures). Joditi + Aporandria + Thalassoditi The grouping of the Joditi, Aporandria and Thalassoditi is well supported in this study. The subtribe Joditi (as Jodini) was established by Inoue (1961) and was treated as a provisional tribe, including four Palaearctic and Indo-Pacific genera (Jodis, Berta, Gelasma and Thalerura Swinhoe, the latter two genera as synonyms of Maxates) by Hausmann (1996). Viidalepp (1996) and Holloway (1996) included Joditi in the wider concept of Hemitheini. Han & Xue (2011a) followed this definition, which is also supported in this molecular study. The species of Maxates number over 100 and were separated in Gelasma Warren, Maxates and Thalerura (Prout, 1912, 1920–41) until Holloway (1996) synonymized Gelasma and Thalerura with Maxates and summarized the most distinctive feature of Maxates as the possession of a strong hindwing tail and a ventral flap on the valva. When Prout (1934–38) described Ecchloropsis, he made a comparison with Hemistola and Dyschloropsis but did not mention Gelasma and Maxates, perhaps because he did not examine the male genitalia. Han & Xue (2011a) summarized the diagnostic characters of Ecchloropsis and Maxates and listed the differences between them. Although they noted that Ecchloropsis has a ventral flap in the valva similar to that found in typical Maxates, the authors did not synonymize the two, given that Ecchloropsis lacks a frenulum, whereas almost all species of Maxates have one. In this analysis, the genus Maxates is found to be polyphyletic, as Maxates acutissima perplexata and M. grandificaria are sister to Ecchloropsis with full support, whereas another three species, M. sp.1, M. sp.2 and M. thetydaria, are grouped as sister to Berta and Jodis. The genus Berta is also found to be paraphyletic, since two species of Jodis are nested within Berta species (including the type species B. chrysolineata Walker). Further research, including the type species of Maxates and Jodis and a greater number of other species, is needed to resolve the phylogenetic relationship among these four genera, the monophyly of the Joditi and the monophyly of Maxates and Berta. The subtribe Thalassoditi (as Thalassodini) was also erected by Inoue (1961) with the inclusion of the genus Thalassodes Guenée, from which three genera (Orothalassodes Holloway, Pelagodes Holloway and Remiformvalva Inoue) were split and erected by Holloway (1996) and Inoue (2006), mainly based on the structures of the male genitalia and the eighth segment. Hausmann (1996) summarized the differential features of Thalassoditi as follows: cell of hindwing very short, discocellular vein oblique and lacking abdominal crests. Hausmann et al. (2016b) synonymized Thalassoditi with Hemistoliti because they share many morphological characters. However, the monophyly of Thalassoditi is fully supported in the present study, with Thalassodes at the basal position of the clade. The genera Prasinocyma and Albinospila Holloway are closely allied to Orothalassodes (Holloway, 1996), and they are expected to be clustered with Orothalassodes if they are sampled. Hausmann et al. (2016a) suggested that the current generic combinations within the large Thalassodes complex (Holloway, 1996) need to be revised. Further research is needed to explore the internal structure of the Thalassoditi by including more genera, such as Prasinocyma and Albinospila. Aporandria was placed in Hemistoliti by Hausmann (1996). He also stated that the external appearance of Aporandria resembles some genera of Geometrini but differs from the latter with respect to the tympanum and venation. In this study, the genus Aporandria is grouped with Thalassoditi with good support. The close relationship between Aporandria and Thalassoditi was first found in this study. However, we hesitate to place Aporandria in Thalassoditi due to its distinct wing patterns. Genera in Thalassoditi, together with Aporandria, are sister to part of Joditi and fall within Joditi. We suspect that the subtribe Thalassoditi may be a synonym of Joditi and that Aporandria also belongs to Joditi, but additional data are needed to validate this hypothesis. Lophochoristiti and Heliotheiti Ferguson (1969) erected the tribe Lophochoristini by including the genera Lophochorista Warren and Eueana Prout. Cook (1993) gave a detailed revision of the neotropical genus Oospila Warren, defined this monophyletic group by the presence of an anellar complex and suggested that Oospila and Lophochorista may be sister taxa. Pitkin (1996) added Anomphax Warren, Telotheta Warren and Oospila to the tribe Lophochoristini. Heliotheini, a tribe erected based on Heliothea Boisduval and another Afrotropical genus, Petovia, was described as a subfamily, but its rank was challenged by Vives Moreno (1994), Müller (1996) and Viidalepp (1996). Later, it was subordinated under Geometrinae by Holloway (1996) and Hausmann (1996). Holloway (1996) suggested Lophochoristini and Heliotheini as junior synonyms of Rhomboristini on the basis of their similar genitalic features. In this study, both Oospila and Petovia are grouped in the tribe Hemitheini, with their positions not resolved. Although Oospila is not the type genus of Lophochoristini, it shares some features with Lophochorista, such as a similar wing pattern, bearing abdominal tufts and possessing a medio-ventral sclerite in the valva (Pitkin, 1996). In addition, Pitkin (1996) pointed out that the ventral sclerite on the valva of the Lophochoristini also occurred in the Rhomboristini and Chlorissa (Hemitheini), which implied a relationship with Hemitheini. Beljaev (2016) also included Lophochoristini in his broad concept of Hemitheini. Thus, it is reasonable to treat Lophochoristini as a subtribe of Hemitheini. However, the position of the tribe Heliotheini is in doubt, as it has some unique features within Geometrinae, such as the shape of the ansa in the tympanal organ, the yellow wing colour and some unusual larval features (Hausmann, 2001). Considering that Heliotheini has similar genitalic features with Hemistoliti (Hausmann, 2001: fig. 11; Han & Xue, 2009: figs 58–61), and Petovia is clustered in Hemitheini in this study, though not as type genus, we tentatively retain Heliotheini as a subtribe. Further study, including Lophochorista and Heliothea, is needed to resolve the phylogenetic position of the Lophochoristiti and Heliotheiti. Dysphaniini + Xenozancla + Pseudoterpnini s.s. In this study, the grouping of Dysphaniini, Xenozancla and Pseudoterpnini s.s. is fully supported in Bayesian analyses but only weakly supported in ML analyses, with Dysphaniini constituting a sister-group of Xenozancla + Pseudoterpnini. The Dysphaniini currently includes only two known genera, Dysphania Hübner and Cusuma Moore, which have been regarded as a natural group. Warren (1895) treated the Dysphaniini as the subfamily Dysphaniinae. Prout (1912) put Dysphania and Cusuma into Group III of Old World genera. Both treatments reflect the distinctive characters that these genera possess. Holloway (1996) presented the unique features of Dysphaniini (the presence of a forewing fovea in both sexes, ansa hammer-headed and lacking a central expansion) in detail and treated it as a sister-group to the rest of Geometrinae. Our result is almost concordant with Sihvonen et al. (2011), in that we did not find support for a division between Dysphaniini and the remaining Geometrinae. The difference from Sihvonen et al. (2011) is that the sister relationship between Dysphaniini and Pseudoterpnini is not supported. Instead, Xenozancla is clustered with Pseudoterpnini. Xenozancla is a small Asian genus that includes only one species. It has not been placed into any known tribes because its combined external and male genitalic features (small size, concavity of forewing distal margin under apex, the coexistence of a bifid uncus and socii, simple valva and long saccus) do not agree with those of known tribes (Han & Xue, 2011a). The present position of Xenozancla is doubtful, given its morphology. Xenozancla is morphologically similar to some species of Pelagodes in Thalassoditi, as the socii of the male genitalia are attached to the base of the gnathos (Han & Xue, 2011a: fig. 390; Han & Xue, 2011b: figs 33–34.). Prout (1912) mentioned its affinity with the African genus Bathycolpodes Prout; both genera have an anteriorly excavated distal margin of the forewing and almost identical wing patterns. In Xenozancla, the excavation on the hindwing is shallower than in Bathycolpodes. Pitkin et al. (2007) provided a comprehensive morphological review of the tribe Pseudoterpnini, in which 34 genera were recognized, covering most genera in the Pseudoterpninae (Warren, 1893, 1894), Groups I and II (Prout, 1912), Terpnini (Inoue, 1961), Archaeobalbini (Viidalepp, 1981), Pingasini (Heppner & Inoue, 1992), Pseudoterpnini (Hausmann, 1996, 2001) and Pseudoterpniti (Holloway, 1996). They suggested that Pseudoterpnini was likely monophyletic, although no single defining character was found. Hausmann (1996, 2001) stated that some features of Holoterpna Püngeler and Aplasta Hübner were anomalous within Pseudoterpnini, the systematic position of Aplasta being particularly isolated. When Holloway (1996) summarized the diagnosis of Pseudoterpnini, he also mentioned that the strong black discal dots and broad black bands on the underside, characteristic of most genera in this broad concept, are absent from Pseudoterpna (though present in Pingasa). Pitkin et al. (2007) also referred to the fact that the type genus Pseudoterpna and several apparently related genera (Aplasta, Holoterpna, Mictoschema Prout and Mimandria Warren) are anomalous in comparison with the rest of the tribe. All these statements imply that the monophyly of Pseudoterpnini is in doubt. In this study, it is surprising that most Oriental and Palaearctic Pseudoterpnini genera in Pitkin et al. (2007), such as Herochroma, Metallolophia, Actenochroma, Absala, Metaterpna, Psilotagma, Limbatochlamys, Dindica, Dindicodes, Lophophelma and Pachyodes, are not clustered with the type genus of Pseudoterpnini, Pseudoterpna. This result differs from other research, such as Sihvonen et al. (2011), in which only two genera and two species of Pseudoterpnini, Pseudoterpna coronillaria (Hübner) and Crypsiphona ocultaria (Donovan), were sampled. This result probably further proves that the monophyly of the tribe Pseudoterpnini is problematic. We tentatively treat the concept of Pseudoterpnini of Pitkin et al. (2007) as Pseudoterpnini s.l. and genera centred around Pseudoterpna as Pseudoterpnini s.s. Prout (1912–16) stated that the larva of Pingasa seems to be allied with Pseudoterpna and that the latter is probably descended from the former. In this study, Pseudoterpna and Pingasa form a monophyletic clade representing Pseudoterpnini s.s. with full support, validating the close relationship mentioned by Prout. These genera also share a similar wing pattern (distinctive transverse lines) and male genitalia (e.g. bifid socii) with Epipristis Meyrick, Mictoschema, Mimandria, Hypodoxa Prout and Pullichroma Holloway. However, to determine which genera belong to Pseudoterpnini s.s., a more extensive phylogenetic study including all the related genera in Pseudoterpnini s.l. and not only Oriental genera, as in this study, is needed. Pachyodes-complex in Pseudoterpnini s.l. In this study, many of the genera previously included within Pseudoterpnini in Pitkin et al. (2007) form a separate clade: Herochroma, Metallolophia, Actenochroma, Absala, Metaterpna, Limbatochlamys, Psilotagma, Dindica, Dindicodes, Lophophelma and Pachyodes. Although these genera are always clustered together and branch after the clade composed of Dysphaniini + Xenozancla + Pseudoterpnini s.s., the support value is weak. They are also difficult to deliminate from Pseudoterpnini s.s. morphologically, as sharing many features, including: fairly large moth with a robust build, wings undersides usually with strong terminal bands; the socii/uncus complex often present; and valvae often divided into two parts (a costal lobe and a sacculus) (Pitkin et al., 2007). Further research tends to separate Pseudoterpnini s.s. and these genera and studies, including more taxa, are needed. We tentatively treat these genera as a generic group, Pachyodes-complex, in Pseudoterpnini s.l. In the Pachyodes-complex, Herochroma and Metallolophia are the two most basal genera. The close relationship between the genera Limbatochlamys and Psilotagma is fully supported and was first discovered in this study. Although these genera are very different externally, the male genitalia of both have a slender uncus and socii, and the female genitalia of both possess a short ductus bursae and a large concave corpus bursae (Han & Xue 2011a: fig. 110–112, 143, 733, 734 and 755). Sphagnodela Warren (not sampled in this study) probably belongs to this group, based on its similar uncus and socii. Dindica, Dindicodes, Lophophelma and Pachyodes form a monophyletic group within the Pachyodes-complex. This relationship was first found in this study. These genera are mainly characterized by the presence of a bifid uncus and usually a divided valva in the male genitalia. The sister relationship between Absala and Actenochroma was also established here. It is possible that the monotypic genera Pachista and Calleremites Warren (not sampled in this study) also belong to this generic group, as Calleremites shares the presence of both uncus and socii with Actenochroma, Limbatochlamys, Metaterpna and Psilotagma, and Pachista shares divided costal and saccular lobes with Pachyodes, Metallolophia, Dindica and Dindicodes. The monophyly of most genera is fully supported, except for that of Lophophelma, which is paraphyletic, as two species of Pachyodes (type species not sampled) are nested within Lophophelma. The male genitalia of Lophophelma vary between species and are quite different from those of Pachyodes, which are characterized by a valva divided into two large lobes of similar length or with the costal lobe a little shorter. Further study, including the type species of both genera and more species, is needed to resolve the monophyly of Lophophelma and its relationship with Pachyodes. Chlorodontopera Warren The genus Chlorodontopera is characterized by the following characters: both fore- and hindwings have large, rounded discal spots, which are larger on the hindwing; a dull reddish-brown patch is present between the discal spot and the costa on the hindwing; in the male genitalia, the socii are stout and setose and the lateral arms of the gnathos are developed, not joined; sternite 3 of the male has setal patches; and veins M3 and CuA1 are unstalked on the hindwing. Inoue (1961) suggested that Chlorodontopera is more or less related to Aracima, but he hesitated to place it in the tribe Aracimini. Chlorodontopera was placed in Nemoriini by Hausmann (1996) and in Aracimini by Holloway (1996), followed by Han & Xue (2011a). Prout (1920–41) referred to the similar morphological characters of Chlorodontopera and Euxena Warren. Later, Holloway (1996) compared Chlorodontopera and Euxena, showing that both genera have similar wing patterns but different genitalia. In this study, Chlorodontopera is sister to the clade including Neohipparchini, Aracimini, Nemoriini, Synchlorini, Comibaenini, Timandromorphini and Geometrini. Chlorodontopera is not related to Aracimini and, therefore, can be excluded from that tribe. Given isolated position, the designation of a new tribe, perhaps including the genus Euxena, is probably appropriate. Further study is needed to confirm a close relationship between these two genera. Neohipparchini Inoue (1961) established Neohipparchus, into which he placed three species from Prout’s section C of Hipparchus. He placed the genus into a new tribe, Neohipparchini, separating it from Geometrini. Species of Chloroglyphica were placed in section D of Hipparchus (Prout, 1920–41). Hausmann (1996) synonymized Neohipparchini with Geometrini and stated that the ansa of the tympanal organ in Neohipparchus and Chlororithra shares a similar structure with that of Tanaorhinus. Holloway (1996) treated Neohipparchini (as Neohipparchiti) as a separate tribe, mentioning that Neohipparchus shares similar venation and facies with Geometrini. Han & Xue (2011a) placed both Neohipparchus and Chloroglyphica in Geometrini, without placing Chlororithra in any known tribe. Our results support Neohipparchus + Chloroglyphica + Chlororithra comprising Neohipparchini, whereas a close relationship between Neohipparchini and Geometrini is not supported. Although the two species of Chlororithra are externally different from Neohipparchus and Chloroglyphica, considering the similar ansa structure mentioned by Hausmann, and that Chlororithra shares the presence of both uncus and socii with some species of Neohipparchus, it is better to put Chlororithra in Neohipparchini. Hausmann (1996) implied a possible homology between Neohipparchus and Iotaphora based on the presence of a stout external spine on the aedeagus. Members of Iotaphora are characterized by short radial lines outside the postmedial line on both the fore- and hindwings. The male genitalia of Iotaphora are also similar to those of Chlororithra, as they possess a similarly developed uncus and socii. Hausmann (1996) placed this genus in Geometrini together with Chlororithra. Beljaev (2016) put Iotaphora in Pseudoterpnini. Han & Xue (2011a) did not place Iotaphora into any known tribe. In this analysis, a close relationship between Iotaphora and Neohipparchus is not supported, and the position of Iotaphora is not resolved. Aracimini Inoue (1961) erected the tribe Aracimini, including only Aracima. Holloway (1996) placed another four genera, Paramaxates, Dooabia, Euxena and Chlorodontopera, in Aracimini, but he also noted the differences among them and suggested that these four genera are probably best placed in the vicinity of Geometrini, this was also mentioned in Hausmann (1996). Hausmann (1996) placed Dooabia in Pseudoterpnini together with Agathia because the genitalia of Dooabia are close to those of Agathia. In this study, the monophyly of Aracimini, represented by Paramaxates, Dooabia and Aracima, is fully supported. Aracima serrata Wileman is embedded in Dooabia and forms a monophyletic clade with the type species of Dooabia, D. viridata, with strong support. It is possible that Aracima serrata should be placed in Dooabia, but the male genitalia of D. puncticostata Prout are very different from those of D. viridata (Moore), as they lack a developed costal projection at the base of the valva. Thus, a new genus may need to be erected for this species. If the isolation of D. puncticostata from Dooabia were proven, A. serrata would no longer be combined into Dooabia. The relationship between A. serrata and A. muscosa Butler (type species of Aracima, not sampled) is still pendent, as the male genitalia of the former is unknown and their wing patterns and female genitalia show great differences. Further morphological research based on type species and additional species of both genera is needed. The close relationship between the Aracimini and Timandromorphini proposed in Sihvonen et al. (2011) is not supported in this study. Nemoriini + Synchlorini + Comibaenini Nemoriini (as Nemoriinae in Gumppenberg, 1887) is a New World tribe including many genera, with Ochrognesiini as a representative in the Indo-Australian tropics. The tribe Ochrognesiini was established by Inoue (1961) to include the two genera Chloromachia Warren and Ochrognesia Warren, both of which were synonymized with Eucyclodes Warren, together with six other genera by Holloway (1996). Accordingly, Ochrognesiini was synonymized with Nemoriini. The diagnostic features of Nemoriini were summarized and commented on by Pitkin (1996), Hausmann (1996) and Holloway (1996). Most recently, Viidalepp (2017) recognized 25 genera in Nemoriini and summarized three main features: the rod-shaped uncus of the male genitalia, the specific shape of the eighth abdominal sternite of the male abdomen and larvae with unclothed chalazae. Ferguson (1969) first erected Synchlorini and placed the genera Synchlora Guenée, Merochlora Prout (= Synchlora), Cheteoscelis Prout (= Synchlora) in it. Synchlorini is characterized by male genitalia in which the uncus is reduced and the socii are rigidly sclerotized, tapered and pointed (Pitkin, 1996). The tribe Comibaenini is a small-sized group in the Geometrinae and was first established by Inoue (1961), including the genera Comibaena Hübner (Chlorochromodes Warren and Comostolodes Warren as synonyms, and Colutoceras Warren as a subgenus) and Thetidia Boisduval. Hausmann (1996) added two new genera, Microbaena Hausmann and Proteuchloris Hausmann, and suggested that the tribe is monophyletic. Holloway (1996) recognized Comibaenini (as subtribe Comibaeniti) as a discrete group. He included the genera Comibaena, Argyrocosma Turner, Comostolodes (with Chlorochromodes and Hercoloxia as synonyms of Comostolodes) and Thetidia, and added a new genus, Protuliocnemis Holloway. Han, Galsworthy & Xue (2012) reviewed Comibaenini worldwide, embracing eight genera: Comibaena, Microbaena, Thetidia, Proteuchloris, Linguisaccus Han et al., Chlorochromodes, Argyrocosma and Protuliocnemis. The most distinctive feature of Comibaenini is the bifid vinculum of the male genitalia. This study sampled five known genera of Comibaenini and the monophyly of Comibaenini is well supported. Within the tribe, Protuliocnemis + Argyrographa are sister to Linguisaccus + (Comibaena + Thetidia). Comibaena and Thetidia are closely related, and Comibaena is paraphyletic, in that Th. chlorophyllaria (Hedemann) and Th. albocostaria (Bremer) are nested within Comibaena, indicating that these two species may be transferred to Comibaena. Han et al. (2012) discussed the similarity among some species of Comibaena (C. hypolampes Prout, C. cenocraspis Prout, C. latilinea Prout and C. swanni Prout) and Thetidia, stating that the frenulum is present in Comibaena species but absent in Thetidia. Prout (1932: 20) regarded the absence or presence of a frenulum in the male as an important character at the level of genus and above. However, Pitkin (1996) stated that both states can occur within a genus, giving as examples Synchlora, Oospila, Chloractis Warren and Phrudocentra Warren. Therefore, it is possible to include Thetidia in Comibaena. Given the morphological diversity of Comibaena members, it is also possible that it needs to be split into different genera. Previous studies have shown a close relationship among Nemoriini, Synchlorini and Comibaenini. Ferguson (1985) stated that Synchlorini have much more in common with Nemoriini, and he would have included the Synchlorini in Nemoriini, were it not for differences in genitalia, venation and larval behaviour. In contrast, Pitkin (1993) stated that the genital differences between Synchlorini and Nemoriini appear insufficient to justify separating tribal status, and deferred formal synonymy due to a lack of information on the early stages of some other important genera, such as Lissochlora Warren and Chavarriella Pitkin. Later, Pitkin (1996) mentioned that some genera in Nemoriini share a similar valva structure with Synchlora (Synchlorini) and Chlorissa (Hemitheini), and continued using Synchlorini, adding Xenopepla Warren to it. Holloway (1996) stated that Synchlorini are probably related to Comibaenini, based on the larval habit of attaching debris and some aspects of genitalic structure. In summary, these three tribes are closely related, as shown by their similar larval behaviour and some genitalic features. In this analysis, Nemoriini, Synchlorini and Comibaenini form a monophyletic clade with strong support. The tribe Synchlorini is clustered with Nemoria Hübner with full support, and Comibaenini is recovered as sister to Pyrochlora with moderate support. A similar result was found by Sihvonen et al. (2011), unsurprisingly, as the data for Nemoriini (Nemoria, Pyrochlora) and Synchlorini (Synchlora) used in the current study were mainly obtained from their research. The monophyly of Nemoriini is not supported by the present concept, under which it would be a monophyletic group with the inclusion of Synchlorini and Comibaenini. Considering that only five species in three genera of Nemoriini are included in our analysis, and there are more than 130 species in Nemoria alone, we defer a decision on this synonymy at present. Further analysis, including additional taxa, is needed to determine the relationship among these tribes and the position of Pyrochlora. Timandromorphini Inoue (1961) erected Timandromorphini based on a single genus, Timandromorpha Inoue. The diagnostic characters were summarized in Inoue (1961), Hausmann (1996), Holloway (1996) and Han & Xue (2011a). Holloway (1996) stated that the Timandromorphini share a modified eighth segment of the male abdomen with the Aracimini and referred to the fact that the ovipositor lobes of the female genitalia are intermediate between the typical type of Geometrinae (oblique and papillate) and the modified type of Geometrini (more sclerotized, smoother and slenderer). Although in Sihvonen et al. (2011), Timandromorpha is a sister to Aracimini, in this study, Timandromorphini is the sister-group to Geometrini, indicating a close relationship to the latter. Geometrini Geometra, the type genus of this tribe, its subfamily and family, and its junior synonym, Hipparchus (both with papilionaria as type species), have been used in the past to describe a number of species that were later split amongst several sections or subgenera on the basis of wing shape and features of the palpus and antenna by Prout (1912, 1920–41). Most subgenera were later synonymized with Geometra, with the exception of Neohipparchus and Chloroglyphica, which were placed in Sections C and D of Hipparchus in Prout (1920–41). Prout (1912–16, 1920–41) stated that Tanaorhinus is scarcely more than a subgenus of Hipparchus (Geometra), with a more or less strongly falcate apex. Section C of Tanaorhinus (as Timandromorpha), Geometra smaragdus (Butler) and G. sinoisaria Oberthür are to some extent intermediate. The species of section B of Tanaorhinus belong to Mixochlora. Prout’s statements and treatment indicated a close relationship among Geometra, Tanaorhinus, Mixochlora, Neohipparchus, Chloroglyphica and Timandromorpha. Inoue (1961) included Geometra, Tanaorhinus and Mixochlora in Geometrini for the Japanese fauna based on the absence of abdominal crests, the separated CuA1 and M3, and the structure of the male genitalia. Holloway (1996) followed Inoue’s tribes, emphasizing the distinctive ovipositor lobes of the Geometrini, which are smoother, more sclerotized and more elongated than those of other tribes. He also noted that Timandromorphini, Neohipparchini and Aracimini are perhaps related to Geometrini. Hausmann (1996) provided a wider concept of Geometrini, including Paramaxates (Aracimini), Neohipparchus (Neohipparchini), Chlororithra, Iotaphora, Ornithospila, Sphagnodela, Mixochlora and Tanaorhinus in addition to the type genus Geometra, and synonymized Neohipparchini with Geometrini. Han & Xue (2011a) first placed Chlorozancla into Geometrini, due to the similar wing shape and male genitalia, but they also noted that a developed, collar-like colliculum in the female genitalia is absent in Chlorozancla but present in Geometra, Tanaorhinus and Mixochlora. In the present concept of Geometrini, Mixochlora and Chlorozancla constitute a monophyletic clade, which is sister to the clade embracing Geometra and Tanaorhinus. Han, Galsworthy & Xue (2009) stated that the monophyly of Geometra is highly questionable and that a full phylogenetic revision would probably entail splitting the genus. Those authors also split Geometra into two species-groups (smaragdus group and papilionaria group) based on the male genitalia, with three species, glaucaria Ménétriés, rana (Oberthür) and sigaria (Oberthür), not placed in any group. The authors mentioned that on the basis of the male genitalia, some species in Tanaorhinus centred around kina Swinhoe are similar to the smaragdus group of Geometra, whereas another group centred around Tanaorhinus rafflesii (Moore) is similar to the papilionaria group. This opinion was validated in this study, in which Tanaorhinus kina is clustered with Geometra fragilis (Oberthür), G. sinoisaria and G. smaragdus (smaragdus-group of Geometra) with full support and Tanaorhinus reciprocata confuciaria (Walker) (type species of Tanaorhinus), T. viridiluteata (Walker) and T. luteivirgatus Yazaki & Wang are clustered with most species of the papilionaria group with full support. Although not all species of Geometra and Tanaorhinus were sampled, we propose, on the basis of the combination of morphological characters and molecular analysis, that T. kina, G. fragilis, G. sinoisaria, G. smaragdus and most likely G. burmensis and T. tibeta Chu (Han et al., 2009: fig. 2: L–O; Han & Xue, 2011a: fig. 161; Orhant, 2014: photograph 6) should be placed in a separate genus. The genus Loxochila Butler stat. rev., which was established based on Tanaorhinus smaragdus Butler, was treated as a subgenus of Hipparchus by Prout (1912, 1920–41) but as a valid genus by Fletcher (1979) and is listed as a synonym of Geometra by Scoble (1999). Here, we revive its generic status and transfer the species mentioned above to it as L. smaragdus stat. rev., L. kinacomb. nov., L. fragiliscomb. nov., L. sinoisariacomb. nov., L. burmensiscomb. nov. and L. tibetacomb. nov. We also tentatively speculate that Tanaorhinus reciprocata (Walker), T. viridiluteata and perhaps T. celebensis Yazaki, T. dohertyi Prout, T. rafflesii, T. unipuncta Warren, T. waterstradti Prout, T. philippinensis Yazaki and T. luteivirgatus should be combined into Geometra. However, further molecular studies, including additional taxa, are needed to confirm this hypothesis. SUPPORTING INFORMATION Additional Supporting Information may be found in the online version of this article at the publisher’s web-site: Table S1. List of specimens and GenBank accession numbers. Table S2. Primers and annealing temperatures used for PCR and cycle sequencing. Table S3. Parameters and partitions assigned according to PARTITIONFINDER 1.1.1. Figure S1. Phylogenetic tree of Geometrinae from the ML analysis excluding the 28S gene fragment. [Version of Record, published online 15 May 2018; http://zoobank.org/urn:lsid:zoobank.org:pub:D2792250- B5CA-4917-A2EA-EBCBE1B42E70] ACKNOWLEDGEMENTS We are grateful to all collectors whose contributions made our work possible. We thank Professor Aibing Zhang (Capital Normal University, Beijing, China) for kindly providing the DNA of Pamphlebia rubrolimbraria, and thank Professor Jaan Viidalepp (Estonian University of Life Sciences, Estonia) for sending us valuable literature. We thank Dr Chaodong Zhu (Institute of Zoology, Chinese Academy of Sciences, Beijing, China) for providing valuable suggestions on selecting genes. We sincerely appreciate Dr Axel Hausmann (Zoologische Staatssammlung München, Munich, Germany) and two anonymous referees for the valuable comments to the manuscript. We are grateful for Sir Anthony Galsworthy (The Natural History Museum, London, UK) for correcting the English. This work was supported by the National Science Foundation of China (No. 31672331, 31372176, 31702041) and the Ministry of Science and Technology of China (No. 2015FY210300). REFERENCES Abraham D , Ryrholm N , Wittzell H , Holloway JD , Scoble MJ , Löfstedt C . 2001 . Molecular phylogeny of the subfamilies in Geometridae (Geometroidea: Lepidoptera) . Molecular Phylogenetics and Evolution 20 : 65 – 77 . Google Scholar CrossRef Search ADS Beljaev EA . 2007 . Taxonomic changes in the emerald moths (Lepidoptera: Geometridae, Geometrinae) of East Asia, with notes on the systematics and phylogeny of Hemitheini . Zootaxa 1584 : 55 – 68 . Beljaev EA . 2008 . Phylogenetic relationships of the family Geometridae and its subfamilies (Lepidoptera) . Meetings in Memory of N. A. Cholodkovsky . Iss. 60 . St. Petersburg ; 1 – 283 . [in Russian with English abstract.] . Beljaev EA . 2016 . Sem. Geometridae – Pyadenitzi [Fam. Geometridae – Geometer moth] . In: Lelei AS , ed. Annotated catalogue of the insects of Russian Far East, Vol. II. Lepidoptera . Vladivostok, Russia Dalnauka , 518 – 666 . Belshaw R , Quicke DLJ . 1997 . A molecular phylogeny of the Aphidiinae (Hymenoptera, Braconidae) . Molecular Phylogenetics and Evolution 7 : 281 – 293 . Google Scholar CrossRef Search ADS Canfield MR , Greene E , Moreau CS , Chen N , Pierce NE . 2008 . Exploring phenotypic plasticity and biogeography in emerald moths: a phylogeny of the genus Nemoria (Lepidoptera: Geometridae) . Molecular Phylogenetics and Evolution 49 : 477 – 487 . Google Scholar CrossRef Search ADS Cheng R , Jiang N , Xue DY , Li XX , Ban XS , Han HX . 2016 . The evolutionary history of Biston suppressaria (Guenée) (Lepidoptera: Geometridae) related to complex topography and geological history . Systematic Entomology 41 : 732 – 743 . Google Scholar CrossRef Search ADS Cook MA . 1993 . The systematics of Emerald Moths (Geometridae, Geometrinae): wing pigments, tympanal organs and a revision of the neotropical genus Oospila Warren . Unpublished D. Phil. Thesis, Oxford University . Cook MA , Harwood LM , Scoble MJ , McGavin GC . 1994 . The chemistry and systematic importance of the green wing pigment in emerald moths (Lepidoptera: Geometridae, Geometrinae) . Biolchemical Systematics and Ecology 22 : 43 – 51 . Google Scholar CrossRef Search ADS Cummins CA , McInerney JO . 2011 . A method for inferring the rate of evolution of homologous characters that can potentially improve phylogenetic inference, resolve deep divergence and correct systematic biases . Systematic Biology 60 : 833 – 844 . Google Scholar CrossRef Search ADS Ferguson DC . 1969 . A revision of the moths of the subfamily Geometridae of America, north of Mexico (Insecta, Lepidoptera) . Bulletin of the Peabody Museum of Natural History 29 : 1 – 251 . Ferguson DC . 1985 . Geometroidea, geometridae (part): subfamily geometrinae . In: Ferguson DC , Lawrence LH , Paige EM , Dominick RB , eds. The moths of America North of Mexico (Lepidoptera). Fascicle 18.1 . Washington, DC : Wedge Entomological Research Foundation , 1 – 131 . Fletcher DS . 1979 . Geometroidea . In: Nye IWB , ed. The generic names of moths of the World , Vol. 3 . London : British Museum (Natural History) ; 1 – 243 . Folmer O , Black M , Hoeh W , Lutz R , Vrijenhoek R . 1994 . DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates . Molecular Marine Biology and Biotechnology 3 : 294 – 299 . Forbes WTM . 1948 . Lepidoptera of New York and neighboring states. II . Memoirs of the Cornell University Agricultural Experiment Station 274 : 1 – 263 . Forum Herbulot . 2007 . The Forum Herbulot World List of Family Group Names in Geometridae [WWW document] . Available at: http://www.herbulot.de/famgroup.htm [last accessed on 16 March 2017 ]. Gumppenberg CF. von . 1887 . Systema Geometrarum zonae temperatioris septentrionalis [part 1] . Nova Acta Academiae Caesareae Leopoldino Carolinae germanicae naturae curiosorum 49 : 233 – 400 . Gutell RR . 1996 . Comparative sequence analysis and the structure of 16S and 23S rRNA . In: Dahlberg AE , Zimmerman EA , eds. Ribosomal RNA structure, evolution, processing and function in protein synthesis . Boca Raton, FL : CRC Press , 111 – 129 . Hampson GF . 1895 . The fauna of British India, including Ceylon and Burma (Moths) . 3 : 1 – 546 . London : Taylor and Francis . Han HX . 2005 . A study on the systematics of Geometrinae from China (Lepidoptera: Geometridae) . A dissertation submitted for the degree of Doctor of Philosophy, Institute of Zoology, Chinese Academy of Sciences . Han HX , Xue DY . 2009 . Taxonomic review of Hemistola Warren, 1893 from China, with descriptions of seven new species (Lepidoptera: Geometridae, Geometrinae) . Entomological Science 12 : 382 – 410 . Google Scholar CrossRef Search ADS Han HX , Xue DY . 2011a . Fauna sinica (Insecta vol. 54, Lepidoptera, Geometridae, Geometrinae) . Beijing : Science Press [in Chinese with English abstract]. Han HX , Xue DY . 2011b . Thalassodes and related taxa of emerald moths in China (Geometridae, Geometrinae) . Zootaxa 3019 : 26 – 50 . Han HX , Galsworthy A , Xue DY . 2009 . A survey of the genus Geometra Linnaeus (Lepidoptera, Geometridae, Geometrinae) . Journal of Natural History 43 : 885 – 922 . Google Scholar CrossRef Search ADS Han HX , Galsworthy AC , Xue DY . 2012 . The Comibaenini of China (Geometridae: Geometrinae), with a review of the tribe . Zoological Journal of the Linnean Society 165 : 723 – 772 . Google Scholar CrossRef Search ADS Hausmann A . 1996 . The morphology of the geometrid moths of the Levant and neighbouring countries . Nota Lepidopterologica 19 : 3 – 90 . Hausmann A . 2001 . Introduction. Archiearinae, Orthostixinae, Desmobathrinae, Alsophilinae, Geometrinae . In: Hausmann A , ed. The geometrid moths of Europe, Vol. 1 . Stenstrup : Apollo Books , 1 – 282 . Hausmann A , Miller SE , Holloway JD , deWaard JR , Pollock D , Prosser SWJ , Hebert PDN . 2016a . Calibrating the taxonomy of a megadiverse insect family: 3000 DNA barcodes from geometrid type specimens (Lepidoptera, Geometridae) . Genome 59 : 671 – 683 . Google Scholar CrossRef Search ADS Hausmann A , Parisi F , Sciarretta A . 2014 . The geometrid moths of Ethiopia I: tribes Pseudoterpnini and Comibaenini (Lepidoptera: Geometridae, Geometrinae) . Zootaxa 3768 : 460 – 468 . Google Scholar CrossRef Search ADS Hausmann A , Sciarretta A , Parisi F . 2016b . The Geometrinae of Ethiopia II: tribus Hemistolini, genus Prasinocyma (Lepidoptera: Geometridae, Geometrinae) . Zootaxa 4065 : 1 – 63 . Google Scholar CrossRef Search ADS Hedtke SM , Townsend TM , Hillis DM . 2006 . Resolution of phylogenetic conflict in large data sets by increased taxon sampling . Systematic Biology 55 : 522 – 529 . Google Scholar CrossRef Search ADS Heppner JB , Inoue H . 1992 . Lepidoptera of Taiwan. Volume 1, part 2: Checklist . Gainsville, Florida : Association for Tropical Lepidoptera and Scientific Publishers . Herbulot C . 1963 . Mise a jour de la liste des Geometridae de France . Alexanor 3 : 17 – 24 . Holloway JD . 1996 . The moths of Borneo: family Geometridae, subfamilies Oenochrominae, Desmobathrinae and Geometrinae . The Malayan Nature Journal 49 : 147 – 326 . Holloway JD . 1997 . The moths of Borneo: family Geometridae, subfamilies Sterrhinae and Larentiinae . The Malayan Nature Journal 51 : 1 – 241 . Holloway JD . 2011 . The moths of Borneo: families Phaudidae, Himantopteridae and Zygaenidae; revised and annotated checklist . The Malayan Nature Journal 63 : 1 – 548 . Inoue H . 1961 . Lepidoptera: Geometridae . Insecta Japonica 4 : 1 – 106 , Tokyo : Hokuryukan . Inoue H . 2006 . Thalassodes-group of emerald moths from Sulawesi and the Philippine Islands (Geometridae, Geometrinae) . Tinea 19 : 214 – 243 . Jiang N , Li XX , Hausmann A , Cheng R , Xue DY , Han HX . 2017 . A molecular phylogeny of the Palaearctic and Oriental members of the tribe Boarmiini (Lepidoptera: Geometridae: Ennominae) . Invertebrate Systematics 31 : 427 – 441 . Google Scholar CrossRef Search ADS Katoh K , Toh H . 2008 . Recent developments in the MAFFT multiple sequence alignment program . Briefings in Bioinformatics 9 : 286 – 298 . Google Scholar CrossRef Search ADS Lalitha S . 2000 . Primer premier 5 . Biotech Software & Internet Report 1 : 270 – 272 . Google Scholar CrossRef Search ADS Lanfear R , Calcott B , Ho SYW , Guindon S . 2012 . PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses . Molecular Biology and Evolution 29 : 1695 – 1701 Google Scholar CrossRef Search ADS Lederer J . 1853 . Versuch die europäischen Lepidopteren in möglichst natürliche Reihenfolge zu stellen, nebst Bemerkungen zu einigen Familien und Arten . Verhandlungen der Zoologisch-Botanischen Gesellschaft in Wien 3 : 165 – 270 . Marvaldi AE , Duckett CN , Kjer KM , Gillespie JJ . 2009 . Structural alignment of 18S and 28S rDNA sequences provides insights into phylogeny of Phytophaga (Coleoptera: Curculionoidea and Chrysomeloidea) . Zoologica Scripta 38 : 63 – 77 . Google Scholar CrossRef Search ADS McGuffin WC . 1988 . Guide to the Geometridae of Canada (Lepidoptera). 3, 4, and 5. Subfamilies Archiearinae, Oenochrominae, and Geometrinae . Memoirs of the Entomological Society of Canada 145 : 1 – 56 . McQuillan PB , Edwards ED . 1996 . Geometridae . In: Nielsen ES , Edwards ED , Rangsi TV , eds. Checklist of the Lepidoptera of Australia. Monographs on Australian Lepidoptera, Vol. 4 . Melbourne : CSIRO , 200 – 228 . Mengual X , Ståhls G , Rojo S . 2015 . Phylogenetic relationships and taxonomic ranking of pipizine flower flies (Diptera: Syrphidae) with implications for the evolution of aphidophagy . Cladistics 31 : 491 – 508 . Google Scholar CrossRef Search ADS Meyrick E . 1892 . On the classification of the Geometrina of the European fauna . Transactions of the Royal Entomological Society of London 1892 : 53 – 140 . Miller MA , Pfeiffer W , Schwartz T . 2010 . Creating the CIPRES Science Gateway for inference of large phylogenetic trees . In: Proceedings of the Gateway Computing Environments Workshop (GCE) . New Orleans, LA : IEEE , 1 – 8 . Müller B . 1996 . Geometridae . In: Karsholt O , Razowski J , eds. The Lepidoptera of Europe, a distributional checklist . Stenstrup : Apollo Books , 218 – 249 . Mutanen M , Wahlberg N , Kaila L . 2010 . Comprehensive gene and taxon coverage elucidates radiation patterns in moths and butterflies . Proceedings of the Royal Society B 277 : 2839 – 2848 . Google Scholar CrossRef Search ADS Orhant G . 2014 . Contribution à la connaissance du genre Tanaorhinus description d’une nouvelle espèce des Moluques Découverte et description du male de Tanaorhinus tibeta CHU, 1982 (Lepidoptera, Geometridae, Geometrinae) . Bulletin de la Société Entomologique de Mulhouse 70 : 59 – 64 . Õunap E , Viidalepp J , Saarma U . 2008 . Systematic position of Lythriini revised: transferred from Larentiinae to Sterrhinae (Lepidoptera, Geometridae) . Zoologica Scripta 37 : 405 – 413 . Google Scholar CrossRef Search ADS Õunap E , Javois J , Viidalepp J , Tammaru T . 2011 . Phylogenetic relationships of selected European Ennominae (Lepidoptera: Geometridae) . European Journal of Entomology 108 : 267 – 273 . Google Scholar CrossRef Search ADS Õunap E , Viidalepp J , Truuverk A . 2016 . Phylogeny of the subfamily Larentiinae (Lepidoptera: Geometridae): integrating molecular data and traditional classifications . Systematic Entomology 41 : 824 – 843 . Google Scholar CrossRef Search ADS Pitkin LM . 1993 . Neotropical emerald moths of the genera Nemoria, Lissochlora and Chavarriella, with particular reference to the species of Costa Rica (Lepidoptera: Geometridae, Geometrinae) . Bulletin of the Natural History Museum, London (Entomology) 62 : 39 – 159 . Pitkin LM . 1996 . Neotropical emerald moths: a review of the genera (Lepidoptera: Geometridae, Geometrinae) . Zoological Journal of the Linnean Society 118 : 309 – 440 . Google Scholar CrossRef Search ADS Pitkin LM , Han HX , James S . 2007 . Moths of the tribe Pseudoterpnini (Geometridae: Geometrinae): a review of the genera . Zoological Journal of the Linnean Society 150 : 343 – 412 . Google Scholar CrossRef Search ADS Posada D , Buckley T . 2004 . Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests . Systematic Biology 53 : 793 – 808 . Google Scholar CrossRef Search ADS Prout LB . 1912 . Lepidoptera Heterocera, fam. Geometridae, subfam. Hemitheinae . In: Wytsman P , ed. Genera insectorum , 129 . Bruxelles : Verteneuil & Desmet . Prout LB . 1912–16 . The Palaearctic Geometrae . In: Seitz A , ed. The macrolepidoptera of the world4 . Stuttgart : Verlag A. Kernen . Prout LB . 1920–41 . The Indoaustralian Geometridae . In: Seitz A , ed. The macrolepidoptera of the world 12 . Stuttgart : Verlag A. Kernen . Prout LB . 1934–38 . The Palaearctic Geometrae, 3. Subfam. Hemitheinae . In: Seitz A , ed. The macrolepidoptera of the world 4 (Suppl.) . Stuttgart : Verlag A. Kernen . Rota J , Wahlberg N . 2012 . Exploration of data partitioning in an eight-gene data set: phylogeny of metalmark moths (Lepidoptera, Choreutidae) . Zoologica Scripta 41 : 536 – 546 . Google Scholar CrossRef Search ADS Schnare MN , Damberger SH , Gray MW , Gutell RR . 1996 . Comprehensive comparison of structural cahracteristics in eukaryotic sytoplasmatic large subunit (23S-like) ribosomal RNA . Journal of Molecular Evolution 256 : 701 – 719 . Scoble MJ , ed. 1999 . Geometrid moths of the world: a catalogue (Lepidoptera, Geometridae) . Collingwood : CSIRO Publishing . Scoble MJ , Hausmann A. (updated 2007 ). Online list of valid and available names of the Geometridae of the world . Available at: http://www.lepbarcoding.org/geometridae/ species_checklists.php (last accessed 9 March 2017) . Sihvonen P , Mutanen M , Kaila L , Brehm G , Hausmann A , Staude HS . 2011 . Comprehensive molecular sampling yields a robust phylogeny for Geometrid moths (Lepidoptera: Geometridae) . PLoS One 6 : e20356 . Google Scholar CrossRef Search ADS Sihvonen P , Staude HS , Mutanen M . 2015 . Systematic position of the enigmatic African cycad moths: an integrative approach to a nearly century old problem (Lepidoptera: Geometridae, Diptychini) . Systematic Entomology 40 : 606 – 627 . Google Scholar CrossRef Search ADS Snäll N , Tammaru T , Wahlberg N , Viidalepp J , Ruohomäki K , Savontaus ML , Huoponen K . 2007 . Phylogenetic relationships of the tribe Operophterini (Lepidoptera, Geometridae): a case study of the evolution of female flightlessness . Biological Journal of the Linnean Society 92 : 241 – 252 . Google Scholar CrossRef Search ADS Stamatakis A , Hoover P , Rougemont J . 2008 . A rapid Bootstrap algorithm for the RAxML web-servers . Systematic Biology 75 : 758 – 771 . Google Scholar CrossRef Search ADS Stekolnikov AA , Kuznetzov VI . 1981 . Functional morphology of the male genitalia and notes on the system of the subfamily Geometrinae (Lepidoptera, Geometridae) . Entomological Review, Washington 60 : 37 – 54 . Strutzenberger P , Brehm G , Bodner F , Fiedler K . 2010 . Molecular phylogeny of Eois (Lepidoptera, Geometridae): evolution of wing patterns and host plant use in a species rich group of Neotropical moths . Zoologica Scripta 39 : 603 – 620 . Google Scholar CrossRef Search ADS Tamura K , Stecher G , Peterson D , Filipski A , Kumar S . 2013 . MEGA6: molecular evolutionary genetics analysis version 6.0 . Molecular Biology and Evolution 30 : 2725 – 2729 . Google Scholar CrossRef Search ADS Viidalepp J . 1981 . On the suprageneric systematics of Geometridae subfamily (Lepidoptera: Geometridae) [In Russian]. Horae Societatis Entomologicae Unionis Soveticae 63 : 90 – 95 . Viidalepp J . 1996 . Checklist of the Geometridae (Lepidoptera) of the former U.S.S.R . Stenstrup: Apollo Books . Viidalepp J . 2017 . A morphology based key to the genera of the tribe Nemoriini (Lepidoptera: Geometridae, Geometrinae) . Zootaxa 4236 : 521 – 532 . Google Scholar CrossRef Search ADS Vives Moreno A . 1994 . Catálogo sistemático y sinonímico de los Lepidópteros de la Peninsula Ibérica y Baleares (Insecta: Lepidoptera, II) . Pesca y Alimentacion, Madrid : Ministerio de Agricultura , 775 . Wahlberg N , Wheat CW . 2008 . Genomic outposts serve the phylogenomic pioneers: designing novel nuclear markers for genomic DNA extractions of Lepidoptera . Systematic Biology 57 : 231 – 242 . Google Scholar CrossRef Search ADS Wahlberg N , Snäll N , Viidalepp J , Ruohomäki K , Tammaru T . 2010 . The evolution of female flightlessness among Ennominae of the Holarctic forest zone (Lepidoptera, Geometridae) . Molecular Phylogenetics and Evolution 55 : 929 – 938 . Google Scholar CrossRef Search ADS Warren W . 1893 . On new genera and species of moths of the family Geometridae from India, in the collection of H. J. Elwes . Proceedings of the Zoological Society of London 1893 : 341 – 434 . Warren W . 1894 . New genera and species of Geometridae . Novitates Zoologicae 1 : 366 – 466 . Google Scholar CrossRef Search ADS Warren W . 1895 . New species and genera of Geometridae in the Tring Museum . Novitates Zoologicae 2 : 82 – 159 . Young C . 2006 . Molecular relationships of the Australian Ennominae (Lepidoptera: Geometridae) and implications for the phylogeny of the Geometridae from molecular and morphological data . Zootaxa 1264 : 1 – 147 . Yamamoto S , Sota T . 2007 . Phylogeny of the Geometridae and the evolution of winter moths inferred from a simultaneous analysis of mitochondrial and nuclear genes . Molecular Phylogenetics and Evolution 44 : 711 – 723 . Google Scholar CrossRef Search ADS © 2018 The Linnean Society of London, Zoological Journal of the Linnean Society This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

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Published: May 15, 2018

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