Tribal Classification and Phylogeny of Geometrinae (Lepidoptera

Zoological Journal of the Linnean Society, 2018, 184, 653–672. With 2 figures.

Tribal classification and phylogeny of Geometrinae Downloaded from https://academic.oup.com/zoolinnean/article-abstract/184/3/653/4996193 by Institute of Zoology, CAS user on 05 November 2018 (Lepidoptera: Geometridae) inferred from seven gene regions

XIAOSHUANG BAN1,2,†, NAN JIANG1,†, RUI CHENG1,†, DAYONG XUE1 AND HONGXIANG HAN1,*

1Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, No. 1 Beichen West Road, Chaoyang District, Beijing 100101, China 2University of Chinese Academy of Sciences, 19A Yuquan Road, Shijingshan District, Beijing 100049, China

Received 30 September 2017; revised 18 January 2018; accepted for publication 27 February 2018

Despite recent progress in the molecular systematics of Geometridae, phylogenetic relationships within the 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.

ADDITIONAL KEYWORDS: Insecta – molecular phylogeny – new taxa – revision.

INTRODUCTION The subfamily Geometrinae, commonly known as emerald moths, is the third largest subfamily in Geometridae is one of the three most species-rich fami- Geometridae, with more than 2500 described spe- lies of Lepidoptera, with approximately 23 000 described cies in 268 genera worldwide (Scoble & Hausmann, species (Scoble, 1999; Scoble & Hausmann, 2007). 2007). Geometrinae is particularly diverse in trop- Caterpillars of this family are known as loopers or inch- ical areas, and the caterpillars mainly feed on various worms because of their looping gait, due to a reduced trees and shrubs (Pitkin, 1996). Holloway (1996) and number of abdominal prolegs. Geometridae has long Pitkin (1996) summarized the main defining charac- attracted the interest of dedicated researchers at leading ters of Geometrinae, among which the predominance institutions around the world, and much progress has of green pigment (geoverdin) is synapomorphic with been made towards a better understanding of geometrid Geometrinae (Cook et al., 1994) and the shape of the taxonomy and systematics (Pitkin, Han & James, 2007). ansa of the tympanal organ supports the monophyly of Geometrinae (Hausmann, 2001). The other characters *Corresponding author. E-mail: [email protected] are: wings are mostly green in colour, the frenulum †Xiaoshuang Ban, Nan Jiang and Rui Cheng contributed equally to the present paper. tends to be reduced, the third sternite of the male often [Version of Record, published online 15 May 2018; possesses a pair of setal patches, the socii of the male http://zoobank.org/urn:lsid:zoobank.org:pub:D2792250- genitalia are usually well developed, the vinculum is B5CA-4917-A2EA-EBCBE1B42E70] distally cruciform in structure, the sclerotization of the

© 2018 The Linnean Society of London, Zoological Journal of the Linnean Society, 2018, 184, 653–672 653 654 X. BAN ET AL. aedeagus is usually reduced to a ventral strip along Geometrini. Pitkin (1996), Hausmann (1996) and Han its length, and the female genitalia have oblique and & Xue (2011a) raised Holloway’s subtribes to the tribal papillate ovipositor lobes and a bicornute signum. level. Hausmann (1996) recognized 15 tribes and Forum Both Hausmann (2001) and Han & Xue (2011a) men- Herbulot (2007) recognized 18 tribes for Geometrinae on tioned venation characters: forewing usually without a global basis. However, some tribal concepts remain con- Downloaded from https://academic.oup.com/zoolinnean/article-abstract/184/3/653/4996193 by Institute of Zoology, CAS user on 05 November 2018 an areole, hindwing with vein M2 close to M1 and far troversial. For example, Holloway (1996) favoured a wide from M3. Beljaev (2008) summarized 12 apomorphies concept of Hemitheini embracing Thalerini, Comostolini, of Geometrinae by adding the results of his study of Hemistolini, Jodini and Thalassodini, whereas these taxa the skeleto-muscular system of the male genitalia. were treated as valid tribes by Hausmann (1996, 2001). Since very early studies, the subfamily Geometrinae Later, Thalassodini were synonymized with Hemistolini in has been considered a natural entity; it was treated as Hausmann et al. (2016b). Beljaev (2016) proposed a much Group I in Lederer (1853), as Geometridae in Meyrick wider concept of Hemitheini by adding Rhomboristini (also (1892), as Geometrinae in Hampson (1895) and as Lophochoristini) and Microloxiini (also Hierochthoniini). Hemitheinae in Prout (1912, 1912–16, 1920–41). The The most likely reason for these controversies is that these monophyly of Geometrinae is also well supported by systematic concepts were mainly drawn from morpho- later molecular studies, such as those of Yamamoto & logical overviews and not based on phylogenetic analysis, Sota (2007) and Sihvonen et al. (2011). Holloway (1997) although they sometimes utilized phylogenetic hints. provided the first tentative phylogeny for Geometridae, The first morphology-based topology of Geometrinae which was established mostly based on characters of the was presented by Viidalepp (1981), who used vari- adult male and female abdomen, and showed a sister ous calculations to divide 26 genera into ten tribes relationship between Geometrinae and Desmobathrinae. based on 12 multi-state characters, erected the tribe Yamamoto & Sota (2007) found that Geometrinae was a Archaeobalbini and placed Pseudoterpnini sensu sister-group to Oenochrominae. In the molecular phylo- Herbulot, 1963 under Terpnini sensu Inoue, 1961 as a genetic analysis of Sihvonen et al. (2011), Oenochrominae subtribe. Stekolnikov & Kuznetzov (1981) presented s.s. or Oenochrominae s.s. + Desmobathrinae was consid- two supertribes, Geometridii and Comibaenidii, based ered a sister-group to Geometrinae with weak support. on the functional morphology of the male genitalia of Considerable progress has been made in systematics ten geometrid species; the former included Geometrini, within Geometrinae. The major global taxonomic revi- Ochrognesiini, Hemitheini and Hemistolini, and the lat- sion of Geometrinae was that of Prout (1912, 1934–38). ter included only Comibaenini. Cook (1993) conducted Subsequently, many regional works on Geometrinae the first cladistic analysis based on 45 geometrine gen- have been produced: Forbes (1948), Ferguson (1969, era and 24 multistate characters. Although he stated 1985) and McGuffin (1988) studied the Geometrinae that his dataset was insufficient to resolve the phyl- of North America, Inoue (1961) reviewed the Japanese ogeny of Geometrinae, the topology still showed that Geometrinae, Pitkin (1996) researched the neotropical many known tribes (such as Thalassodini, Hemitheini, Geometrinae, Holloway (1996) reviewed the Bornean Thalerini, Jodini, Hemistolini, Comostolini, Synchlorini Geometrinae, Hausmann (1996, 2001) investigated and Nemoriini) were grouped in one superclade, which Geometrinae from the Levant and neighbouring coun- somewhat supports some of the morphological results tries and Europe, McQuillan & Edwards (1996) studied mentioned above. Han (2005) conducted a preliminary Australian Geometrinae, Viidalepp (1996) produced a cladistic analysis of the tribe Geometrini, based on 71 checklist of Geometridae from the USSR and erected morphological characters, and found that the mono- a new tribe, Hierochthoniini, Han & Xue (2011a) stud- phyly of Geometra Linnaeus was doubtful, since the spe- ied Chinese representatives, Hausmann, Parisi & cies were clustered in several different clades, and the Sciarretta (2014) and Hausmann, Sciarretta & Parisi phylogenetic relationships among genera were unclear. (2016b) reviewed the Ethiopian Geometrinae (Parts The rapid development of DNA sequencing tech- I and II) and Beljaev (2016) published a catalogue of niques has accelerated the molecular phylogenetic Geometrinae in the insects of the Russian Far East. analysis of Geometridae (Abraham et al., 2001; Young, Almost all of these researchers allocated genera of 2006; Snäll et al., 2007; Yamamoto & Sota, 2007; Geometrinae to tribes or groups. However, due to the lack Õunap, Viidalepp & Saarma, 2008; Strutzenberger of a global review, there is no consensus regarding the sys- et al., 2010; Wahlberg et al., 2010; Õunap et al., 2011; tematic placement of tribes and groups within Geometrinae Sihvonen et al., 2011; Õunap, Viidalepp & Truuverk, and no clear understanding of the relationships between 2016; Sihvonen, Staude & Mutanen, 2015). The most the tribes. Within Geometrinae, Holloway (1996) comprehensive taxon sampling at the tribal level was divided the subfamily into two tribes: Dysphaniini and achieved by Sihvonen et al. (2011): 16 of 18 geometrine Geometrini. The latter included almost all the geometrine tribes sensu Forum Herbulot (2007) and three genera of species and almost all the known tribes as subtribes. Later, unknown affiliation were sampled, and a preliminary Holloway (2011) separated the tribe Pseudoterpnini from molecular phylogeny of Geometrinae was established on

© 2018 The Linnean Society of London, Zoological Journal of the Linnean Society, 2018, 184, 653–672 CLASSIFICATION AND PHYLOGENY OF GEOMETRINAE 655 a global scale. Although the study included most tribes In total, fragments of one mitochondrial pro- of Geometrinae, only one species was sampled for each tein-coding gene (COI), five nuclear protein-cod- of 11 tribes and a total of only 27 geometrine species in ing genes (EF-1α, CAD, GAPDH, RPS5 and MDH) 25 genera representing Geometrinae were included. In and one nuclear rRNA gene (28S) were sequenced. addition, as the authors stated, the bootstrap values of These molecular markers have been widely used Downloaded from https://academic.oup.com/zoolinnean/article-abstract/184/3/653/4996193 by Institute of Zoology, CAS user on 05 November 2018 most nodes were very low and most of the phylogenetic in reconstructing the phylogenies of different fami- relationships in Geometrinae, with the exception of the lies of Lepidoptera (e.g. Wahlberg & Wheat, 2008; position of the Dysphaniini, were not discussed. Rota & Wahlberg, 2012), especially Geometridae The relationships among the tribes of Geometrinae (e.g. Yamamoto & Sota, 2007; Wahlberg et al., 2010; remain largely unexplored. This study aims to further inves- Sihvonen et al., 2011). Several pairs of new prim- tigate the phylogenetic relationships within Geometrinae ers were designed by PRIMER PREMIER 5.0 at the tribal level, to test the monophyletic hypotheses of (Lalitha, 2000) based on sequences that were previ- tribes, to revise the existing tribal classification within ously obtained using universal primers. The primer the subfamily and to revise the tribe Geometrini, which is sequences and the annealing temperatures used mainly based on Palaearctic and Oriental genera, to cover for polymerase chain reactions (PCRs) are provided almost all known tribes (except Dichordophorini) using in the Supporting Information (Table S2), mainly one mitochondrial gene (COI) and six nuclear genes (EF- from Folmer et al. (1994), Belshaw & Quicke (1997), 1α, CAD, GAPDH, RPS5, MDH and 28S). The results of Wahlberg & Wheat (2008) and our previous works this study will shed light on the tribal classification of the (Cheng et al., 2016; Jiang et al., 2017). PCR was per- genera in Geometrinae, improve our understanding of the formed in a total volume of 25 μL; the reaction con- phylogenetic relationships within the subfamily at the glo- tained 12.5 μL of PCR 2×TSINGKETM Master Mix bal scale and provide a phylogenetic framework for study- (TSINGKE, Beijing, China), 0.5 μL of each primer, ing the evolutionary history of Geometrinae. 1 μL of the extracted DNA and 10.5 μL of ultrapure water. The cycling parameters were: a 5-min dena- turing step at 95 °C followed by 30–40 cycles of 30 s at 94 °C, 30 s at a primer-specific annealing tempera- MATERIAL AND METHODS ture, extension at 72 °C for 30 s to 1 min and final Taxon sampling extension at 72 °C for 10 min. A 7-μL PCR mixture A total of 116 species belonging to 56 genera represent- was examined on a 1.0% agarose gel to determine the ing 17 currently recognized Geometrinae tribes (with only quality and quantity of the PCR products before the one monobasic tribe, Dichordophorini, not sampled) were sequencing reaction was performed. The remaining included in this study (Fig. 1). At least two species in each PCR product was sequenced using the same prim- tribe, except Lophochoristini, were sampled to weaken the ers on an ABI PRISM 3730xl automated sequencer at possible effects of long-branch attraction (Hedtke, Townsend BGI (Beijing Genomics Institute, China). & 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. Phylogenetic analyses (2010), Mutanen, Wahlberg & Kaila (2010) and Sihvonen The phylogenetic analyses were conducted both with, et al. (2011). We adopted 12 exemplars representing the and excluding, the 28S rRNA gene fragment. The other six subfamilies (Sterrhinae, Larentiinae, Archiearinae, alignment of the 28S fragment is problematic due to Ennominae, Oenochrominae and Desmobathrinae) of the coexistence of a highly conserved core structure Geometridae as outgroups. A list of taxa with the collecting and highly variable regions (Gutell, 1996; Schnare localities, voucher codes and GenBank accession numbers et al., 1996; Marvaldi et al., 2009), and there is no con- is provided in the Supporting Information (Table S1). Some sensus on how to use this gene fragment (Young, 2006; specimens are unidentified morphologically and molecu- Mengual, Ståhls & Rojo, 2015; Õunap et al., 2016). In larly on BOLD SYSTEMS due to insufficient taxonomy and this study, all the 28S gene loci, after alignment by constitute potential new species. A formal description of new MAFFT, were used for phylogenetic analyses. species is, however, beyond the scope of this study. Partial DNA sequences were downloaded from GenBank, due to the lack of samples. All sequences were manually edited using the SEQMAN module DNA extraction, amplification and sequencing of the LASERGENE software package (DNASTAR, We extracted total genomic DNA from adult unilat- Madison, WI). Sequences of protein-coding genes were eral legs that had been dried or freshly preserved in aligned using CLUSTALW as implemented in MEGA anhydrous ethanol using the DNeasy Blood and Tissue 6.0 (Tamura et al., 2013), and 28S rRNA segments D1 Kit (Qiagen, Beijing, China) following the protocol sug- and D2 were concatenated and aligned in MAFFT v.6 gested by the manufacturer. (Katoh & Toh, 2008).

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Figure 1. Representatives of the tribes of Geometrinae, sampled in the present study. A, Ornithospilini, Ornithospila esmer- alda (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.

Neighbour-joining trees for each gene were con- re-analysed or removed from subsequent analyses. We structed using MEGA 6.0 to check the validity of each obtained 153 samples yielding an assembly of 5805 bp gene of every sample. Problematic sequences were of nucleotide data.

A partition strategy based on the actual evolution sites. The robustness of clades found is presented as rate of nucleotide data has been widely used in recent posterior probabilities (PP, for the Bayesian analysis) phylogenetic analyses (Õunap et al., 2016; Jiang et al., or bootstrap values (BS, for the ML analysis). 2017). Rota & Wahlberg (2012) showed its advan- The two phylogenetic analyses (ML and Bayesian) tages over partitioning by genes or codon positions in of the combined datasets of seven gene regions yield Downloaded from https://academic.oup.com/zoolinnean/article-abstract/184/3/653/4996193 by Institute of Zoology, CAS user on 05 November 2018 Lepidoptera. We partitioned the nucleotide dataset almost identical topologies (Fig. 2). The analyses by the actual rate of evolution in the following analy- excluding 28S also yielded very similar topologies ses; the related substitution models are shown in the (Supporting Information, Fig. S1) except for several Supporting Information (Table S3). small differences in the terminal branches. We used TIGER v.1.02 (Cummins & McInerney, The monophyly of Geometrinae is strongly sup- 2011) to separate slowly evolving characters, which was ported in two phylogenetic analyses (PP = 1, BS = 100) expected to be more reliable for inferring deep diver- in relation to the genera included in this study. Close gences, from rapidly evolving characters, with the total to the root of Geometrinae, two genera, Ornithospila bin number parameter set to 50. PARTITIONFINDER Warren and Agathia Guenée, branch off the main line- 1.1.1 (Lanfear et al., 2012) was used to select the age, one after the other, with strong support. most effective partitioning scheme according to the The tribes Rhomboristini, Heliotheini, Hemistolini, Bayesian information criterion (BIC) (Posada & Comostolini, Hemitheini, Microloxiini, Thalerini, Buckley, 2004) and to determine the best phylogen- Lophochoristini, Jodini, Thalassodini and one unas- etic models for each dataset using the bins defined by signed genus Aporandria Warren are clustered in TIGER. For the maximum likelihood (ML) analyses, a clade with full support (PP = 1, BS = 100). In this PARTITIONFINDER was run with models = raxml clade, the tribe Rhomboristini is at the most basal and search = greedy options, whereas in the Bayesian position with very strong support (PP = 1, BS = 99). analyses, models = mrbayes and search = greedy Three well-supported subclades within this clade are options were performed. recognized: (1) Hemistolini and Comostolini constitute The ML analyses were implemented in RAxML a monophyletic subclade with full support (PP = 1, v.7.7.1 on the RAxML webserver (http://phylobench. BS = 100); (2) the monophyly of the subclade composed vital-it.ch/raxml-bb/index.php) (Stamatakis et al., of Hemitheini, Microloxiini and Thalerini is well sup- 2008) under the GTR+Gamma model for the final ported (PP = 1, BS = 94) – in this subclade, Thalerini is best-scoring ML tree. Bayesian phylogenetic recon- embedded in Hemitheini; (3) Jodini and Thalassodini, structions were generated using MRBAYES v.3.2 together with Aporandria, form a monophyletic (Huelsenbeck & Ronquist 2001) on the CIPRES clade (PP = 0.93, BS = 92) in which the monophyly of Science Gateway v. 3.1 (Miller, Pfeiffer & Schwartz, Thalassodini is fully supported, the sister relationship 2010), with the appropriate models and substitution between Thalassodini and Aporandria is strongly sup- rates. Four simultaneous Markov chains (one cold ported and the monophyly of Jodini is not supported and three heated) were run for 10 000 million gen- because Thalassodini + Aporandria form a sister-group erations until the split frequencies were below 0.01, to part of Jodini and are nested in Jodini. The genus sampling trees every 1000 generations and discard- Maxates Moore is shown as a non-monophyletic assem- ing 25% of the trees as burn-in. blage in which M. grandificaria Graeser and M. acutis- The software TRACER v.1.6 (Rambaut et al., 2014) was sima perplexata Prout cluster with Ecchloropsis Prout, used both to estimate the sample sizes of the parameters and M. thetydaria Guenée, M. sp.1 and M. sp.2 cluster in the Bayesian analyses and to check for the conver- with Berta Walker and Jodis Hübner. gences or otherwise of the parallel MCMC runs. 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 RESULTS with Dysphaniini with full support in Bayesian The analyses conducted in this study are based on the analyses but weak support in ML analyses (PP = 1, sequence data from one mitochondrial gene region BS = 47), after clustering with Xenozancla Warren. (1371 bp of COI), six nuclear gene regions (955 bp of However, many other genera (Herochroma Swinhoe, EF-1α, 847 bp of CAD, 706 bp of GAPDH, 602 bp of Metallolophia Warren, Absala Swinhoe, Actenochroma RPS5, 474 bp of MDH and 850 bp of 28S rRNA). The Warren, Metaterpna Yazaki, Limbatochlamys final aligned data matrix contained 5805 nucleotide Rothschild, Psilotagma Warren, Dindica Moore,

Figure 2. 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.

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Dindicodes Prout, Lophophelma Prout and Pachyodes The genus Eumelea Duncan was transferred from Guenée) are clustered in a separate clade with mod- Oenochrominae s.l. to Desmobathrinae by Holloway erate support in Bayesian analyses (PP = 0.97) and (1996), whilst the author pointed out that Eumelea weak support (BS = 57) in ML analyses. In this clade, lacks the definitive features of the desmobathrines. the sister relationship between Limbatochlamys and Beljaev (2008) considered Eumelea be a member of Downloaded from https://academic.oup.com/zoolinnean/article-abstract/184/3/653/4996193 by Institute of Zoology, CAS user on 05 November 2018 Psilotagma is fully supported (PP = 1, BS = 100) and Geometrinae on the basis of the skeleto-muscular was first found in this study. The genera Dindica, structure of the male genitalia, and pointed out that Dindicodes, Lophophelma and Pachyodes are clus- it may occupy a basal position in Geometrinae. In the tered together with full or strong support (PP = 1, same study, Beljaev doubted the desmobathrine pos- BS = 98). A close relationship between Absala and ition of the genus Celerena Walker (not sampled in the Actenochroma was also identified for the first time. present study) and thought it a possible geometrine The remaining Geometrinae are clustered in a clade member. Although the affinity between Eumelea and (PP = 0.97, BS = 62) embracing seven tribes and two Geometrinae is not directly supported in this study, the unassigned genera: Chlorodontopera Warren, Aracimini, former is clustered with members of Desmobathrinae Neohipparchini, Nemoriini + Synchlorini + Comibaenini, and Oenochrominae with poor support, so the possibil- Iotaphora Warren, Timandromorphini and Geometrini. ity of Eumelea belonging to Geometrinae and occupy- The monophyly of Neohipparchini is well supported ing a basal position is not excluded. in both analyses (PP = 1, BS = 83). The tribe is rede- The multi-gene phylogeny determined in this fined to accommodate Chlororithra Butler in addition study validates the monophyly of the subfamily to Neohipparchus Inoue and Chloroglyphica Warren. Geometrinae and recovers 12 tribes (Dichordophorini Aracimini is fully supported (PP = 1, BS = 100) as a not sampled), two of which are proposed as new. The monophyletic clade consisting of Paramaxates Warren, tribes are Ornithospilini trib. nov., Agathiini trib. Dooabia Warren and Aracima Butler, with Aracima nov., Dysphaniini, Pseudoterpnini, Neohipparchini, embedded within Dooabia. In the analyses excluding Aracimini, Nemoriini, Synchlorini, Comibaenini, 28S, the position of Aracimini is exchanged with that Timandromorphini, Geometrini and Hemitheini of Neohipparchini (Supporting Information, Fig. S1). on a very broad concept embracing nine subtribes. The tribes Nemoriini, Synchlorini and Comibaenini Only three tribes (Dysphaniini, Comibaenini and are clustered in one clade with strong support Timandromorphini) are totally concordant with the (PP = 0.98, BS = 99) but with the relationship previous morphology-based concepts of tribes recog- among them was unresolved. The current concept of nized by Holloway (1996, as subtribes), Hausmann Nemoriini is polyphyletic, as Pyrochlora Warren is (1996) and Forum Herbulot (2007), and five tribes sister to Comibaenini in all trees. The monophyly of (Aracimini, Neohipparchini, Nemoriini, Synchlorini Comibaenini is well supported (PP = 1, BS = 88). and Geometrini) are in rough agreement with them. The sister relationship between Timandromorphini Resolution of the inter-tribal relationships within and Geometrini is moderately supported (PP = 0.95, Geometrinae remains limited, probably due to the BS = 88), and the monophyly of both tribes is strongly to limited sampling of taxa and molecular markers and fully supported. In the tribe Geometrini, the sister rela- sampling bias towards the Palaearctic and Oriental tionship between Chlorozancla Prout and Mixochlora regions. The tribe Ornithospilini is the most basal Warren is strongly supported (PP = 0.95, BS = 96). taxon, followed by Agathiini. The sister relationship Members of Geometra and Tanaorhinus Butler are clus- between Hemitheini and all the remaining geometrine tered in one clade with full support (BS = 100, PP = 1.00) groups is fully supported in Bayesian analyses and only and these genera are confirmed to be polyphyletic groups. weakly supported in ML analyses. In the clade composed of Chlorodontopera, Aracimini, Neohipparchini, Nemoriini + Synchlorini + Comibaenini, Iotaphora, Timandromorphini and Geometrini, Chlorodontopera DISCUSSION and Neohipparchini are the most basal taxa, the This study covers all tribes of the Geometrinae, except close relationship among Nemoriini, Synchlorini and the North American tribe Dichordophorini Ferguson, Comibaenini is strongly supported, and the close rela- which includes only one genus, Dichordophora Prout, tionship between Timandromorphini and Geometrini making this study a comprehensive phylogenetic anal- is moderately supported. ysis to date of Geometrinae at the tribal level. Though Holloway (1996) described the typical ovipositor lobes 17 (18 in total) currently recognized tribes were of Geometrinae (different from those of Dysphaniini) as included in this analysis, our sampling was mainly follows: the distal margin of the ovipositor lobes recedes restricted to the Palaearctic and Oriental regions; obliquely ventrally, and the setae are placed irregu- the data are, therefore, not sufficient to elaborate the larly on papillate projections. He also noted that there whole evolutionary story of Geometrinae. are exceptions in the Geometrini, Timandromorphini,

Paramaxates and Neohipparchini. Combined with the socii. Holloway (1996) considered Ornithospila as present tree (Fig. 2), there is one possible trend: the set apart from the rest of the Geometrinae by the ovipositor lobes are inclined to be more sclerotized, condition of the female signum, which is elong- smoother and slenderer in more evolved groups (e.g. ate, ovate and scobinate. This opinion is supported Geometrini, Neohipparchini and Paramaxates). The here, as Ornithospila is positioned at the base of Downloaded from https://academic.oup.com/zoolinnean/article-abstract/184/3/653/4996193 by Institute of Zoology, CAS user on 05 November 2018 modification of the ovipositor lobes may be related to Geometrinae, and the relationship to Aporandria oviposition preferences and larval host plants. Because and Geometrini is not supported. the phylogenetic relationships among the tribes were not totally resolved, this hypothesis requires further testing with studies that clarify the phylogeny in Agathiini Ban & Han trib. nov. Geometrinae by including more taxa and more genes. Type genus: Agathia Guenée, 1858 (Holloway, 1996: The following sections will describe the tribal clas- plates 7, 8 and 10, figs 194–211, 213–216, 239, 243; sification of the Geometrinae, including the morpho- Han & Xue, 2011a: figs 22–28 of plate 19, figs 1–8 of logical characters and a short review of the main plate 20, figs 371–385, 690–704 and 884–893). taxonomic histories of the respective groups, and the Differential features: Wings are bright green. The credible phylogenetic relationships inferred from the antennae are filiform in both males and females. The phylogenetic trees. Unless major changes occurred in hind tibia of the male is dilated, with hair-pencil. one tribe, the differential features of the tribes will not The forewing usually possesses distinctive medial be repeated. and terminal bands and a series of patches. Veins M3

and CuA1 are connate at the cell on the hindwing, Ornithospilini Ban & Han trib. nov. and 3A is present. Sternite 3 of the male abdomen usually has a pair of setal patches. The two branches Type genus: Ornithospila Warren, 1894 (Holloway, of the socii are close to each other and are fused at 1996: plate 7, figs 217–225 and 315–316; Han & Xue, the base, resembling those of Pseudoterpna, Dooabia 2011a: figs 20–22 of plate 18, figs 342–344, 661–663 and Louisproutia Wehrli. The costa of the valva is and 865–866). ornamented with a dorsal process. In the female Differential features: The wings of the members of genitalia, the corpus bursae usually has a bicornute Ornithospilini are bright green. The hind tibia of the signum. male is not dilated. The veins Sc+R1 are close to the cell Agathiini is established here as a new tribe, ten- at one point, then separate rapidly on the hindwing; tatively including only the genus, Agathia, repre-

CuA1 and M3 are separate, and vein 3A is absent. sented by three species, including the type species of Sternite 3 of the male abdomen lacks setal patches. the genus Hypagathia Inoue (synonym of Agathia), The socii of the male genitalia are developed and are Agathia carissima Butler. Agathia is a large genus, almost the same length as the uncus as in Hemitheini including 77 species worldwide (Scoble, 1999; but sometimes with a basal process. The signum of Scoble & Hausmann, 2007) and is widely distrib- the female genitalia, if present, is elongate, ovate and uted in Southeast Asia, Australia and Africa. Inoue scobinate (Holloway, 1996). (1961), Viidalepp (1981), Hausmann (1996) and Ornithospilini is proposed as a new, currently Beljaev (2016) placed Agathia in Pseudoterpnini (or monobasic tribe that is mainly distributed in the Terpnini) mainly based on morphological studies. Oriental region. In this study, the Ornithospilini Stekolnikov & Kuznetzov (1981) suggested that it exemplars (two different species of Ornithospila) belongs to Ochrognesiini (Nemoriini) on the basis form a distinct group that occupies a basal position of the functional morphology (muscles) of the male in Geometrinae. Prout (1912) placed Ornithospila genitalia. Holloway (1996) did not place it into any in Group IV of the Old World genera and men- tribe and stated that it is unwise to erect a new tioned that it probably derived from Hipparchus tribe without a well-understood classification of (Geometra), but he also stated that the ven- Geometrinae in its entirety. In this study, species ation and genitalia of the type species agree bet- of Agathia form a distinct group that branched off ter with Prasinocyma Warren and the Iodis group after Ornithospilini and are placed in a more basal (Jodis). Later, Prout (1920–41) suggested that position, unlike the results of Sihvonen et al. (2011), some species of Ornithospila are somewhat analo- in which Agathia is positioned at the base of the gous to Aporandria in size, shape and coloration. second major lineage with very weak support. The Although Hausmann (1996) placed Ornithospila in combination of the bright green wing colour, the Geometrini, he also referred to features that differ- structure of the socii and the presence of a dorsal entiate it from Geometrini, such as the presence of ornament of the valva distinguish Agathiini from an uncus and the shorter and slightly sclerotized other known tribes.

Hemitheini of the genera Rhomborista Warren (Rhomboristiti) and The concept of Hemitheini recognized here is broader Petovia (Heliotheiti), three well-supported subclades are than that of Holloway (1996) due to the inclusion of sev- recognized within Hemitheini: Hemistoliti + Comostoliti, eral additional tribes: Rhomboristini, Lophochoristini, Hemitheiti + Microloxiiti, and Joditi + Aporandria + Thalassoditi. Heliotheini and Microloxiini (= Hierochthoniini). For Downloaded from https://academic.oup.com/zoolinnean/article-abstract/184/3/653/4996193 by Institute of Zoology, CAS user on 05 November 2018 this study, the main characters of Hemitheini are: the male antennae are usually bipectinate; the moths are Rhomboristiti mainly bluish, emerald green or greyish green in colour; the outer margin of the hindwing bears a tail process The subtribe Rhomboristiti (as Rhomboristini) was established by Inoue (1961) as embracing three Indo- in many genera; veins M3 and CuA1 of the hindwing are usually stalked (separate or connate in Rhomboristiti Australian genera, Rhomborista, Spaniocentra Prout genera); most genera have a frenulum, but some do not and Rhombocentra Holloway, and was treated as a valid (such as Berta, Comostola Meyrick, Hemistola Warren, tribe by Holloway (1996). Holloway (1996) suggested Jodis, Thalera Hübner and Eucrostes Hübner); and the the synonymy of Lophochoristiti and Heliotheiti with socii and uncus are similar in length and are usually Rhomboristiti for three tribes sharing similar male gen- closely adpressed (a strong uncus with weak socii in italia with features such as a strong uncus with weak Rhomboristiti genera). Holloway (1996) stated that socii, a strong gnathos and often a doubled harpe-like the larvae are usually slender and the resting posture process in the centre of the valva. Hausmann (1996) is stick-like. indicated that the hindwing venation of Rhomboristiti The concept of Hemitheini has long been controver- corresponds well with that of Comostola (Comostoliti) sial and the internal structure has not been resolved, and Berta (Joditi). In this study, close relationships though some researchers suggested a close relation- between Rhomboristiti, Lophochoristiti and Heliotheiti ship among some groups. Viidalepp (1996) indicated a or between Rhomboristiti and Comostoliti were not close relationship between Thalerini and Hemistolini, supported; instead, Rhomboristiti constitutes a basal Jodini and Hemitheini by including Hemistola clade within Hemitheini with full support, implying its in Thalerini and genera of Jodini in Hemitheini, isolated position in Hemitheini. respectively. Hausmann (1996) noted that Thalerini, Hemistolini, Comostolini, Jodini, Hemitheini and Microloxiini are linked by various genera. For exam- Hemistoliti + Comostoliti ple, he stated that the venation of Rhomboristini Hemistoliti and Comostoliti were both erected by Inoue corresponds to that of Jodini and Comostolini, some (1961) as tribes. Hausmann (1996) summarized the dif- features of Comostolini resemble those of Hemistolini, ferential features of these two groups, mentioned that Jodini has a relationship to Hemitheini and Thalerini some features of Comostoliti (e.g. the male genitalia) is close to Hemitheini. Holloway (1996) introduced are reminiscent of Hemistoliti and stated that there is a wide concept of Hemitheini, embracing Thalerini, a close relationship between Comostoliti and Joditi. As Comostolini, Hemistolini, Jodini and Thalassodini. He in Sihvonen et al. (2011), the close relationship between also synonymized Lophochoristini with Rhomboristini. Comostoliti and Hemistoliti, represented by the type Pitkin (1996) still treated Lophochoristini as a valid genus of each, is fully supported here, validating the tribe. Beljaev (2007) stated that the transtilla of the statement by Hausmann (1996). However, the mono- type genus of Hemitheini is quite different from that phyly of Hemistoliti is not supported, as Hemistola ten- of the other genera, which is similar to that in Jodini, uilinea Alphéraky is sister to parts of Hemistoliti and Microloxiini and Hemistolini (sensu Inoue, 1961 and Comostoliti. Therefore, we suggest that Comostoliti Hausmann, 2001). He also indicated that Thalerini is a possible synonym of Hemistoliti and that fur- are probably subordinate to Hemitheini Bruand, ther research, including more genera of Hemistoliti 1946. The Hemitheini concept in Beljaev (2016) is and Comostoliti, is needed. In this analysis, the close wider, embracing Hemitheini Bruand, Comostolini, relationship between Comostoliti and Joditi is not Jodini, Hemistolini, Thalassodini, Rhomboristini, directly supported, and the synonymization between Thalerini, Lophochoristini and Microloxiini (also Hemistoliti and Thalassoditi presented by Hausmann Hierochthoniini). et al. (2016b) is not directly supported because the phy- In this analysis, the broad concept of Hemitheini is fully logeny of Hemitheini is not fully resolved. 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 Hemitheiti + Microloxiiti large, some previous tribes are treated as subtribes, with The subtribe Hemitheiti (i.e Hemitheini s.s.), embrac- subtribes equal to previous tribes. After the branching off ing 18 genera (Inoue, 1961; Ferguson, 1969, 1985;

Hausmann, 1996; Pitkin, 1996; Viidalepp, 1996), is This synonymy is also supported by morphological mainly characterized by the male genitalia, in which characters: the venation (Ferguson, 1969: pl. 5, fig. 5; the uncus is slender, rod-like and pointed or tapered, Han & Xue, 2011a: fig. 63) of both genera is almost and the socii are usually similar to the uncus in shape identical, except that M3 and CuA1 are stalked in and size (Pitkin, 1996). Hethemia and sometimes CuA also diverges from the

1 Downloaded from https://academic.oup.com/zoolinnean/article-abstract/184/3/653/4996193 by Institute of Zoology, CAS user on 05 November 2018 In this study, Microloxiini, Hemitheini s.s. and lower angle of the cell in Thalera. In the male genita- Thalerini listed in Forum Herbulot (2007) are grouped lia, the two genera possess similar uncus, socii, gna- in a clade with good support. The phylogenetic rela- thos and aedeagus (Ferguson, 1969: pl. 29, figs 1 and 2; tionship within this clade is well resolved in Bayesian reference to Han & Xue 2011a, related figures). 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 Joditi + Aporandria + Thalassoditi Thalera, and Chlorochlamys Hulst is clustered with The grouping of the Joditi, Aporandria and Chloropteryx Hulst first and then grouped with Thalassoditi is well supported in this study. The sub- Chlorissa Stephens. tribe Joditi (as Jodini) was established by Inoue (1961) The type genus of the subtribe Thaleriti, Thalera, was and was treated as a provisional tribe, including four placed in Hemitheini by Inoue (1961). Subsequently, Palaearctic and Indo-Pacific genera (Jodis, Berta, Herbulot (1963) established Thaleriti (as Thalerini) Gelasma and Thalerura Swinhoe, the latter two gen- based on Thalera. Hausmann (1996) stated that era as synonyms of Maxates) by Hausmann (1996). Hemitheiti is rather closely related to Thaleriti based Viidalepp (1996) and Holloway (1996) included Joditi on genitalic morphology. In this study, Thaleriti in the wider concept of Hemitheini. Han & Xue (2011a) [including the type species of Thalera, Thalera fim- followed this definition, which is also supported in this brialis (Scopoli)] are embedded in Hemitheiti [includ- molecular study. ing the type species of Hemithea, Hemithea aestivaria The species of Maxates number over 100 and were (Hübner)]. Based on the similarities in the male geni- separated in Gelasma Warren, Maxates and Thalerura talia of the Thaleriti and Hemitheiti, such as the simi- (Prout, 1912, 1920–41) until Holloway (1996) syn- lar shape and size of the uncus and the socii (Han & onymized Gelasma and Thalerura with Maxates and Xue, 2011a: figs 225, 353), Thaleriti (syn. nov.) can summarized the most distinctive feature of Maxates as be synonymized with Hemitheiti. Accordingly, several the possession of a strong hindwing tail and a ventral other genera of Thaleriti, recognized by Hausmann flap on the valva. (1996, 2001) (Culpinia Prout, Bustilloxia Expósito, When Prout (1934–38) described Ecchloropsis, he Dyschloropsis Warren, Heteroculpinia Hausmann, made a comparison with Hemistola and Dyschloropsis Dolosis Prout and Kuchleria Hausmann), should be but did not mention Gelasma and Maxates, perhaps transferred into Hemitheiti. because he did not examine the male genitalia. Han The subtribe Microloxiiti (as Microloxiini) was estab- & Xue (2011a) summarized the diagnostic characters lished by Hausmann (1996) and includes 11 genera. of Ecchloropsis and Maxates and listed the differences

Externally, these genera share stalked M3 and CuA1 between them. Although they noted that Ecchloropsis of the hindwing, and the presence of socii and uncus has a ventral flap in the valva similar to that found in of similar lengths as the Hemitheiti. In this analysis, typical Maxates, the authors did not synonymize the though Microloxia ruficornis Warren is embedded in two, given that Ecchloropsis lacks a frenulum, whereas Hemitheiti, it is not the type species and, therefore, almost all species of Maxates have one. does not necessarily represent the whole of Microloxia In this analysis, the genus Maxates is found to be or even Microloxiiti. We, therefore, hesitate to syn- polyphyletic, as Maxates acutissima perplexata and onymize Microloxiiti with Hemitheiti; the relationship M. grandificaria are sister to Ecchloropsis with full between Microloxiiti and Hemitheiti needs further support, whereas another three species, M. sp.1, M. study with more taxa. sp.2 and M. thetydaria, are grouped as sister to Berta The monotypic genus Hethemia, with Hethemia and Jodis. The genus Berta is also found to be para- pistasciaria (Guenée) as the type species, is found in phyletic, since two species of Jodis are nested within North America. In this study, Hethemia falls within Berta species (including the type species B. chryso- Thalera, forms a monophyletic clade with Thalera lineata Walker). Further research, including the type fimbrialis (= type species of Thalera, T. thymiaria species of Maxates and Jodis and a greater number (Linnaeus)) and is, therefore, synonymized with of other species, is needed to resolve the phylogenetic Thalera (= Hethemia syn. nov.). Pistasciaria is trans- relationship among these four genera, the monophyly ferred to Thalera as Thalera pistasciaria comb. nov. of the Joditi and the monophyly of Maxates and Berta.

The subtribe Thalassoditi (as Thalassodini) was (1996). Holloway (1996) suggested Lophochoristini also erected by Inoue (1961) with the inclusion of the and Heliotheini as junior synonyms of Rhomboristini genus Thalassodes Guenée, from which three gen- on the basis of their similar genitalic features. era (Orothalassodes Holloway, Pelagodes Holloway In this study, both Oospila and Petovia are grouped and Remiformvalva Inoue) were split and erected by in the tribe Hemitheini, with their positions not Downloaded from https://academic.oup.com/zoolinnean/article-abstract/184/3/653/4996193 by Institute of Zoology, CAS user on 05 November 2018 Holloway (1996) and Inoue (2006), mainly based on the resolved. Although Oospila is not the type genus structures of the male genitalia and the eighth seg- of Lophochoristini, it shares some features with ment. Hausmann (1996) summarized the differential Lophochorista, such as a similar wing pattern, bearing features of Thalassoditi as follows: cell of hindwing very abdominal tufts and possessing a medio-ventral scler- short, discocellular vein oblique and lacking abdomi- ite in the valva (Pitkin, 1996). In addition, Pitkin (1996) nal crests. Hausmann et al. (2016b) synonymized pointed out that the ventral sclerite on the valva of Thalassoditi with Hemistoliti because they share many the Lophochoristini also occurred in the Rhomboristini morphological characters. However, the monophyly of and Chlorissa (Hemitheini), which implied a relation- Thalassoditi is fully supported in the present study, ship with Hemitheini. Beljaev (2016) also included with Thalassodes at the basal position of the clade. The Lophochoristini in his broad concept of Hemitheini. genera Prasinocyma and Albinospila Holloway are Thus, it is reasonable to treat Lophochoristini as a closely allied to Orothalassodes (Holloway, 1996), and subtribe of Hemitheini. However, the position of the they are expected to be clustered with Orothalassodes tribe Heliotheini is in doubt, as it has some unique if they are sampled. Hausmann et al. (2016a) sug- features within Geometrinae, such as the shape of the gested that the current generic combinations within ansa in the tympanal organ, the yellow wing colour the large Thalassodes complex (Holloway, 1996) need and some unusual larval features (Hausmann, 2001). to be revised. Further research is needed to explore Considering that Heliotheini has similar genitalic the internal structure of the Thalassoditi by including features with Hemistoliti (Hausmann, 2001: fig. 11; more genera, such as Prasinocyma and Albinospila. Han & Xue, 2009: figs 58–61), and Petovia is clus- Aporandria was placed in Hemistoliti by Hausmann tered in Hemitheini in this study, though not as type (1996). He also stated that the external appearance of genus, we tentatively retain Heliotheini as a subtribe. Aporandria resembles some genera of Geometrini but Further study, including Lophochorista and Heliothea, differs from the latter with respect to the tympanum is needed to resolve the phylogenetic position of the and venation. In this study, the genus Aporandria is Lophochoristiti and Heliotheiti. grouped with Thalassoditi with good support. The close relationship between Aporandria and Thalassoditi was first found in this study. However, we hesitate to Dysphaniini + Xenozancla + Pseudoterpnini s.s. place Aporandria in Thalassoditi due to its distinct In this study, the grouping of Dysphaniini, Xenozancla wing patterns. Genera in Thalassoditi, together with and Pseudoterpnini s.s. is fully supported in Bayesian Aporandria, are sister to part of Joditi and fall within analyses but only weakly supported in ML analy- Joditi. We suspect that the subtribe Thalassoditi may ses, with Dysphaniini constituting a sister-group of be a synonym of Joditi and that Aporandria also Xenozancla + Pseudoterpnini. belongs to Joditi, but additional data are needed to val- The Dysphaniini currently includes only two idate this hypothesis. known genera, Dysphania Hübner and Cusuma Moore, which have been regarded as a natural group. Warren (1895) treated the Dysphaniini as the subfam- Lophochoristiti and Heliotheiti ily Dysphaniinae. Prout (1912) put Dysphania and Ferguson (1969) erected the tribe Lophochoristini Cusuma into Group III of Old World genera. Both by including the genera Lophochorista Warren and treatments reflect the distinctive characters that Eueana Prout. Cook (1993) gave a detailed revision these genera possess. Holloway (1996) presented the of the neotropical genus Oospila Warren, defined this unique features of Dysphaniini (the presence of a fore- monophyletic group by the presence of an anellar com- wing fovea in both sexes, ansa hammer-headed and plex and suggested that Oospila and Lophochorista lacking a central expansion) in detail and treated it as may be sister taxa. Pitkin (1996) added Anomphax a sister-group to the rest of Geometrinae. Our result Warren, Telotheta Warren and Oospila to the tribe is almost concordant with Sihvonen et al. (2011), in Lophochoristini. Heliotheini, a tribe erected based on that we did not find support for a division between Heliothea Boisduval and another Afrotropical genus, Dysphaniini and the remaining Geometrinae. The dif- Petovia, was described as a subfamily, but its rank was ference from Sihvonen et al. (2011) is that the sister challenged by Vives Moreno (1994), Müller (1996) and relationship between Dysphaniini and Pseudoterpnini Viidalepp (1996). Later, it was subordinated under is not supported. Instead, Xenozancla is clustered with Geometrinae by Holloway (1996) and Hausmann Pseudoterpnini.

Xenozancla is a small Asian genus that includes Pseudoterpnini is problematic. We tentatively treat only one species. It has not been placed into any known the concept of Pseudoterpnini of Pitkin et al. (2007) tribes because its combined external and male geni- as Pseudoterpnini s.l. and genera centred around talic features (small size, concavity of forewing distal Pseudoterpna as Pseudoterpnini s.s. margin under apex, the coexistence of a bifid uncus Prout (1912–16) stated that the larva of Pingasa Downloaded from https://academic.oup.com/zoolinnean/article-abstract/184/3/653/4996193 by Institute of Zoology, CAS user on 05 November 2018 and socii, simple valva and long saccus) do not agree seems to be allied with Pseudoterpna and that the with those of known tribes (Han & Xue, 2011a). The latter is probably descended from the former. In this present position of Xenozancla is doubtful, given its study, Pseudoterpna and Pingasa form a monophy- morphology. Xenozancla is morphologically similar letic clade representing Pseudoterpnini s.s. with to some species of Pelagodes in Thalassoditi, as the full support, validating the close relationship men- socii of the male genitalia are attached to the base of tioned by Prout. These genera also share a similar the gnathos (Han & Xue, 2011a: fig. 390; Han & Xue, wing pattern (distinctive transverse lines) and male 2011b: figs 33–34.). Prout (1912) mentioned its affin- genitalia (e.g. bifid socii) with Epipristis Meyrick, ity with the African genus Bathycolpodes Prout; both Mictoschema, Mimandria, Hypodoxa Prout and genera have an anteriorly excavated distal margin of Pullichroma Holloway. However, to determine which the forewing and almost identical wing patterns. In genera belong to Pseudoterpnini s.s., a more extensive Xenozancla, the excavation on the hindwing is shal- phylogenetic study including all the related genera in lower than in Bathycolpodes. Pseudoterpnini s.l. and not only Oriental genera, as in Pitkin et al. (2007) provided a comprehensive mor- this study, is needed. phological review of the tribe Pseudoterpnini, in which 34 genera were recognized, covering most genera in the Pseudoterpninae (Warren, 1893, 1894), Pachyodes-complex in Pseudoterpnini s.l. Groups I and II (Prout, 1912), Terpnini (Inoue, 1961), In this study, many of the genera previously included Archaeobalbini (Viidalepp, 1981), Pingasini (Heppner within Pseudoterpnini in Pitkin et al. (2007) form & Inoue, 1992), Pseudoterpnini (Hausmann, 1996, a separate clade: Herochroma, Metallolophia, 2001) and Pseudoterpniti (Holloway, 1996). They sug- Actenochroma, Absala, Metaterpna, Limbatochlamys, gested that Pseudoterpnini was likely monophyletic, Psilotagma, Dindica, Dindicodes, Lophophelma and although no single defining character was found. Pachyodes. Although these genera are always clus- Hausmann (1996, 2001) stated that some fea- tered together and branch after the clade composed tures of Holoterpna Püngeler and Aplasta Hübner of Dysphaniini + Xenozancla + Pseudoterpnini s.s., were anomalous within Pseudoterpnini, the system- the support value is weak. They are also difficult to atic position of Aplasta being particularly isolated. deliminate from Pseudoterpnini s.s. morphologic- When Holloway (1996) summarized the diagnosis of ally, as sharing many features, including: fairly Pseudoterpnini, he also mentioned that the strong large moth with a robust build, wings undersides black discal dots and broad black bands on the under- usually with strong terminal bands; the socii/uncus side, characteristic of most genera in this broad con- complex often present; and valvae often divided cept, are absent from Pseudoterpna (though present into two parts (a costal lobe and a sacculus) (Pitkin in Pingasa). Pitkin et al. (2007) also referred to the et al., 2007). Further research tends to separate fact that the type genus Pseudoterpna and several Pseudoterpnini s.s. and these genera and studies, apparently related genera (Aplasta, Holoterpna, including more taxa, are needed. We tentatively Mictoschema Prout and Mimandria Warren) are treat these genera as a generic group, Pachyodes- anomalous in comparison with the rest of the tribe. complex, in Pseudoterpnini s.l. All these statements imply that the monophyly of In the Pachyodes-complex, Herochroma and Pseudoterpnini is in doubt. Metallolophia are the two most basal gen- In this study, it is surprising that most Oriental era. The close relationship between the genera and Palaearctic Pseudoterpnini genera in Pitkin Limbatochlamys and Psilotagma is fully supported et al. (2007), such as Herochroma, Metallolophia, and was first discovered in this study. Although Actenochroma, Absala, Metaterpna, Psilotagma, these genera are very different externally, the male Limbatochlamys, Dindica, Dindicodes, Lophophelma genitalia of both have a slender uncus and socii, and and Pachyodes, are not clustered with the type genus of the female genitalia of both possess a short ductus Pseudoterpnini, Pseudoterpna. This result differs from bursae and a large concave corpus bursae (Han & other research, such as Sihvonen et al. (2011), in which Xue 2011a: fig. 110–112, 143, 733, 734 and 755). only two genera and two species of Pseudoterpnini, Sphagnodela Warren (not sampled in this study) Pseudoterpna coronillaria (Hübner) and Crypsiphona probably belongs to this group, based on its similar ocultaria (Donovan), were sampled. This result prob- uncus and socii. Dindica, Dindicodes, Lophophelma ably further proves that the monophyly of the tribe and Pachyodes form a monophyletic group within the

Pachyodes-complex. This relationship was first found Neohipparchini in this study. These genera are mainly character- Inoue (1961) established Neohipparchus, into which ized by the presence of a bifid uncus and usually a he placed three species from Prout’s section C of divided valva in the male genitalia. The sister rela- Hipparchus. He placed the genus into a new tribe, tionship between Absala and Actenochroma was also Neohipparchini, separating it from Geometrini. Downloaded from https://academic.oup.com/zoolinnean/article-abstract/184/3/653/4996193 by Institute of Zoology, CAS user on 05 November 2018 established here. It is possible that the monotypic Species of Chloroglyphica were placed in section D of genera Pachista and Calleremites Warren (not sam- Hipparchus (Prout, 1920–41). pled in this study) also belong to this generic group, Hausmann (1996) synonymized Neohipparchini as Calleremites shares the presence of both uncus with Geometrini and stated that the ansa of the tympa- and socii with Actenochroma, Limbatochlamys, nal organ in Neohipparchus and Chlororithra shares a Metaterpna and Psilotagma, and Pachista shares similar structure with that of Tanaorhinus. Holloway divided costal and saccular lobes with Pachyodes, (1996) treated Neohipparchini (as Neohipparchiti) Metallolophia, Dindica and Dindicodes. as a separate tribe, mentioning that Neohipparchus The monophyly of most genera is fully supported, shares similar venation and facies with Geometrini. except for that of Lophophelma, which is paraphyl- Han & Xue (2011a) placed both Neohipparchus etic, as two species of Pachyodes (type species not and Chloroglyphica in Geometrini, without placing sampled) are nested within Lophophelma. The male Chlororithra in any known tribe. genitalia of Lophophelma vary between species and Our results support Neohipparchus + Chloroglyphica are quite different from those of Pachyodes, which + Chlororithra comprising Neohipparchini, whereas are characterized by a valva divided into two large a close relationship between Neohipparchini and lobes of similar length or with the costal lobe a little Geometrini is not supported. Although the two spe- shorter. Further study, including the type species of cies of Chlororithra are externally different from both genera and more species, is needed to resolve Neohipparchus and Chloroglyphica, considering the the monophyly of Lophophelma and its relationship similar ansa structure mentioned by Hausmann, and with Pachyodes. that Chlororithra shares the presence of both uncus and socii with some species of Neohipparchus, it is better to put Chlororithra in Neohipparchini. Chlorodontopera Warren Hausmann (1996) implied a possible homology The genus Chlorodontopera is characterized by the fol- between Neohipparchus and Iotaphora based on the lowing characters: both fore- and hindwings have large, presence of a stout external spine on the aedeagus. rounded discal spots, which are larger on the hindwing; Members of Iotaphora are characterized by short radial a dull reddish-brown patch is present between the dis- lines outside the postmedial line on both the fore- and cal spot and the costa on the hindwing; in the male geni- hindwings. The male genitalia of Iotaphora are also sim- talia, the socii are stout and setose and the lateral arms ilar to those of Chlororithra, as they possess a similarly of the gnathos are developed, not joined; sternite 3 of developed uncus and socii. Hausmann (1996) placed the male has setal patches; and veins M3 and CuA1 are this genus in Geometrini together with Chlororithra. unstalked on the hindwing. Inoue (1961) suggested that Beljaev (2016) put Iotaphora in Pseudoterpnini. Han Chlorodontopera is more or less related to Aracima, & Xue (2011a) did not place Iotaphora into any known but he hesitated to place it in the tribe Aracimini. tribe. In this analysis, a close relationship between Chlorodontopera was placed in Nemoriini by Hausmann Iotaphora and Neohipparchus is not supported, and the (1996) and in Aracimini by Holloway (1996), followed position of Iotaphora is not resolved. by Han & Xue (2011a). Prout (1920–41) referred to the similar morphological characters of Chlorodontopera and Euxena Warren. Later, Holloway (1996) compared Aracimini Chlorodontopera and Euxena, showing that both genera Inoue (1961) erected the tribe Aracimini, including only have similar wing patterns but different genitalia. In Aracima. Holloway (1996) placed another four genera, this study, Chlorodontopera is sister to the clade includ- Paramaxates, Dooabia, Euxena and Chlorodontopera, ing Neohipparchini, Aracimini, Nemoriini, Synchlorini, in Aracimini, but he also noted the differences among Comibaenini, Timandromorphini and Geometrini. them and suggested that these four genera are prob- Chlorodontopera is not related to Aracimini and, there- ably best placed in the vicinity of Geometrini, this fore, can be excluded from that tribe. Given isolated was also mentioned in Hausmann (1996). Hausmann position, the designation of a new tribe, perhaps includ- (1996) placed Dooabia in Pseudoterpnini together with ing the genus Euxena, is probably appropriate. Further Agathia because the genitalia of Dooabia are close study is needed to confirm a close relationship between to those of Agathia. In this study, the monophyly of these two genera. Aracimini, represented by Paramaxates, Dooabia and

Aracima, is fully supported. Aracima serrata Wileman genera Comibaena, Argyrocosma Turner, Comostolodes is embedded in Dooabia and forms a monophyletic (with Chlorochromodes and Hercoloxia as synonyms clade with the type species of Dooabia, D. viridata, of Comostolodes) and Thetidia, and added a new with strong support. It is possible that Aracima serrata genus, Protuliocnemis Holloway. Han, Galsworthy should be placed in Dooabia, but the male genitalia of & Xue (2012) reviewed Comibaenini worldwide, Downloaded from https://academic.oup.com/zoolinnean/article-abstract/184/3/653/4996193 by Institute of Zoology, CAS user on 05 November 2018 D. puncticostata Prout are very different from those embracing eight genera: Comibaena, Microbaena, of D. viridata (Moore), as they lack a developed costal Thetidia, Proteuchloris, Linguisaccus Han et al., projection at the base of the valva. Thus, a new genus Chlorochromodes, Argyrocosma and Protuliocnemis. may need to be erected for this species. If the isolation The most distinctive feature of Comibaenini is the of D. puncticostata from Dooabia were proven, A. ser- bifid vinculum of the male genitalia. This study sam- rata would no longer be combined into Dooabia. The pled five known genera of Comibaenini and the mono- relationship between A. serrata and A. muscosa Butler phyly of Comibaenini is well supported. Within the (type species of Aracima, not sampled) is still pendent, tribe, Protuliocnemis + Argyrographa are sister to as the male genitalia of the former is unknown and Linguisaccus + (Comibaena + Thetidia). Comibaena their wing patterns and female genitalia show great and Thetidia are closely related, and Comibaena is differences. Further morphological research based on paraphyletic, in that Th. chlorophyllaria (Hedemann) type species and additional species of both genera is and Th. albocostaria (Bremer) are nested within needed. The close relationship between the Aracimini Comibaena, indicating that these two species may be and Timandromorphini proposed in Sihvonen et al. transferred to Comibaena. Han et al. (2012) discussed (2011) is not supported in this study. the similarity among some species of Comibaena (C. hypolampes Prout, C. cenocraspis Prout, C. lati- linea Prout and C. swanni Prout) and Thetidia, stat- Nemoriini + Synchlorini + Comibaenini ing that the frenulum is present in Comibaena species Nemoriini (as Nemoriinae in Gumppenberg, 1887) is but absent in Thetidia. Prout (1932: 20) regarded the a New World tribe including many genera, with absence or presence of a frenulum in the male as an Ochrognesiini as a representative in the Indo- important character at the level of genus and above. Australian tropics. The tribe Ochrognesiini was However, Pitkin (1996) stated that both states can established by Inoue (1961) to include the two gen- occur within a genus, giving as examples Synchlora, era Chloromachia Warren and Ochrognesia Warren, Oospila, Chloractis Warren and Phrudocentra both of which were synonymized with Eucyclodes Warren. Therefore, it is possible to include Thetidia Warren, together with six other genera by Holloway in Comibaena. Given the morphological diversity of (1996). Accordingly, Ochrognesiini was synonymized Comibaena members, it is also possible that it needs with Nemoriini. The diagnostic features of Nemoriini to be split into different genera. were summarized and commented on by Pitkin (1996), Previous studies have shown a close relationship Hausmann (1996) and Holloway (1996). Most recently, among Nemoriini, Synchlorini and Comibaenini. Viidalepp (2017) recognized 25 genera in Nemoriini Ferguson (1985) stated that Synchlorini have much and summarized three main features: the rod-shaped more in common with Nemoriini, and he would have uncus of the male genitalia, the specific shape of the included the Synchlorini in Nemoriini, were it not eighth abdominal sternite of the male abdomen and for differences in genitalia, venation and larval larvae with unclothed chalazae. behaviour. In contrast, Pitkin (1993) stated that Ferguson (1969) first erected Synchlorini and placed the genital differences between Synchlorini and the genera Synchlora Guenée, Merochlora Prout (= Nemoriini appear insufficient to justify separating Synchlora), Cheteoscelis Prout (= Synchlora) in it. tribal status, and deferred formal synonymy due to Synchlorini is characterized by male genitalia in which a lack of information on the early stages of some the uncus is reduced and the socii are rigidly sclerot- other important genera, such as Lissochlora Warren ized, tapered and pointed (Pitkin, 1996). and Chavarriella Pitkin. Later, Pitkin (1996) men- The tribe Comibaenini is a small-sized group in tioned that some genera in Nemoriini share a simi- the Geometrinae and was first established by Inoue lar valva structure with Synchlora (Synchlorini) (1961), including the genera Comibaena Hübner and Chlorissa (Hemitheini), and continued using (Chlorochromodes Warren and Comostolodes Warren Synchlorini, adding Xenopepla Warren to it. Holloway as synonyms, and Colutoceras Warren as a subgenus) (1996) stated that Synchlorini are probably related and Thetidia Boisduval. Hausmann (1996) added two to Comibaenini, based on the larval habit of attach- new genera, Microbaena Hausmann and Proteuchloris ing debris and some aspects of genitalic structure. Hausmann, and suggested that the tribe is monophyl- In summary, these three tribes are closely related, etic. Holloway (1996) recognized Comibaenini (as sub- as shown by their similar larval behaviour and some tribe Comibaeniti) as a discrete group. He included the genitalic features.

In this analysis, Nemoriini, Synchlorini and Oberthür are to some extent intermediate. The spe- Comibaenini form a monophyletic clade with strong cies of section B of Tanaorhinus belong to Mixochlora. support. The tribe Synchlorini is clustered with Prout’s statements and treatment indicated a Nemoria Hübner with full support, and Comibaenini close relationship among Geometra, Tanaorhinus, is recovered as sister to Pyrochlora with moder- Mixochlora, Neohipparchus, Chloroglyphica and Downloaded from https://academic.oup.com/zoolinnean/article-abstract/184/3/653/4996193 by Institute of Zoology, CAS user on 05 November 2018 ate support. A similar result was found by Sihvonen Timandromorpha. et al. (2011), unsurprisingly, as the data for Nemoriini Inoue (1961) included Geometra, Tanaorhinus and (Nemoria, Pyrochlora) and Synchlorini (Synchlora) Mixochlora in Geometrini for the Japanese fauna used in the current study were mainly obtained from based on the absence of abdominal crests, the sepa- their research. The monophyly of Nemoriini is not sup- rated CuA1 and M3, and the structure of the male ported by the present concept, under which it would be genitalia. Holloway (1996) followed Inoue’s tribes, a monophyletic group with the inclusion of Synchlorini emphasizing the distinctive ovipositor lobes of the and Comibaenini. Considering that only five species in Geometrini, which are smoother, more sclerotized three genera of Nemoriini are included in our analy- and more elongated than those of other tribes. He sis, and there are more than 130 species in Nemoria also noted that Timandromorphini, Neohipparchini alone, we defer a decision on this synonymy at present. and Aracimini are perhaps related to Geometrini. Further analysis, including additional taxa, is needed Hausmann (1996) provided a wider concept of to determine the relationship among these tribes and Geometrini, including Paramaxates (Aracimini), the position of Pyrochlora. Neohipparchus (Neohipparchini), Chlororithra, Iotaphora, Ornithospila, Sphagnodela, Mixochlora and Tanaorhinus in addition to the type genus Geometra, Timandromorphini and synonymized Neohipparchini with Geometrini. Inoue (1961) erected Timandromorphini based on Han & Xue (2011a) first placed Chlorozancla into a single genus, Timandromorpha Inoue. The diag- Geometrini, due to the similar wing shape and male nostic characters were summarized in Inoue (1961), genitalia, but they also noted that a developed, collar- Hausmann (1996), Holloway (1996) and Han & like colliculum in the female genitalia is absent in Xue (2011a). Holloway (1996) stated that the Chlorozancla but present in Geometra, Tanaorhinus Timandromorphini share a modified eighth segment and Mixochlora. of the male abdomen with the Aracimini and referred In the present concept of Geometrini, Mixochlora to the fact that the ovipositor lobes of the female and Chlorozancla constitute a monophyletic clade, genitalia are intermediate between the typical type which is sister to the clade embracing Geometra and of Geometrinae (oblique and papillate) and the modi- Tanaorhinus. Han, Galsworthy & Xue (2009) stated fied type of Geometrini (more sclerotized, smoother that the monophyly of Geometra is highly question- and slenderer). Although in Sihvonen et al. (2011), able and that a full phylogenetic revision would prob- Timandromorpha is a sister to Aracimini, in this study, ably entail splitting the genus. Those authors also Timandromorphini is the sister-group to Geometrini, split Geometra into two species-groups (smaragdus indicating a close relationship to the latter. group and papilionaria group) based on the male genitalia, with three species, glaucaria Ménétriés, rana (Oberthür) and sigaria (Oberthür), not placed in Geometrini any group. The authors mentioned that on the basis Geometra, the type genus of this tribe, its subfamily of the male genitalia, some species in Tanaorhinus and family, and its junior synonym, Hipparchus (both centred around kina Swinhoe are similar to the smar- with papilionaria as type species), have been used in agdus group of Geometra, whereas another group cen- the past to describe a number of species that were tred around Tanaorhinus rafflesii (Moore) is similar later split amongst several sections or subgenera on to the papilionaria group. This opinion was validated the basis of wing shape and features of the palpus in this study, in which Tanaorhinus kina is clustered and antenna by Prout (1912, 1920–41). Most sub- with Geometra fragilis (Oberthür), G. sinoisaria and genera were later synonymized with Geometra, with G. smaragdus (smaragdus-group of Geometra) with the exception of Neohipparchus and Chloroglyphica, full support and Tanaorhinus reciprocata confuci- which were placed in Sections C and D of Hipparchus aria (Walker) (type species of Tanaorhinus), T. viridi- in Prout (1920–41). luteata (Walker) and T. luteivirgatus Yazaki & Wang Prout (1912–16, 1920–41) stated that Tanaorhinus are clustered with most species of the papilionaria is scarcely more than a subgenus of Hipparchus group with full support. Although not all species of (Geometra), with a more or less strongly falcate apex. Geometra and Tanaorhinus were sampled, we propose, Section C of Tanaorhinus (as Timandromorpha), on the basis of the combination of morphological char- Geometra smaragdus (Butler) and G. sinoisaria acters and molecular analysis, that T. kina, G. fragilis,

G. sinoisaria, G. smaragdus and most likely G. bur- Beljaev EA. 2008. Phylogenetic relationships of the family mensis and T. tibeta Chu (Han et al., 2009: fig. 2: L–O; Geometridae and its subfamilies (Lepidoptera). Meetings in Han & Xue, 2011a: fig. 161; Orhant, 2014: photograph Memory of N. A. Cholodkovsky. Iss. 60. St. Petersburg; 1–283. 6) should be placed in a separate genus. The genus [in Russian with English abstract.]. Loxochila Butler stat. rev., which was established Beljaev EA. 2016. Sem. Geometridae – Pyadenitzi [Fam. Downloaded from https://academic.oup.com/zoolinnean/article-abstract/184/3/653/4996193 by Institute of Zoology, CAS user on 05 November 2018 based on Tanaorhinus smaragdus Butler, was treated Geometridae – Geometer moth]. In: Lelei AS, ed. Annotated as a subgenus of Hipparchus by Prout (1912, 1920–41) catalogue of the insects of Russian Far East, Vol. II. but as a valid genus by Fletcher (1979) and is listed Lepidoptera. Vladivostok, Russia Dalnauka, 518–666. as a synonym of Geometra by Scoble (1999). Here, we Belshaw R, Quicke DLJ. 1997. A molecular phylogeny of the Aphidiinae (Hymenoptera, Braconidae). Molecular revive its generic status and transfer the species men- Phylogenetics and Evolution 7: 281–293. tioned above to it as L. smaragdus stat. rev., L. kina Canfield MR, Greene E, Moreau CS, Chen N, Pierce comb. nov., L. fragilis comb. nov., L. sinoisaria NE. 2008. Exploring phenotypic plasticity and biogeog- comb. nov., L. burmensis comb. nov. and L. tibeta raphy in emerald moths: a phylogeny of the genus Nemoria comb. nov. We also tentatively speculate that (Lepidoptera: Geometridae). Molecular Phylogenetics and Tanaorhinus reciprocata (Walker), T. viridiluteata Evolution 49: 477–487. and perhaps T. celebensis Yazaki, T. dohertyi Prout, Cheng R, Jiang N, Xue DY, Li XX, Ban XS, Han HX. 2016. T. rafflesii, T. unipuncta Warren, T. waterstradti Prout, The evolutionary history of Biston suppressaria (Guenée) T. philippinensis Yazaki and T. luteivirgatus should be (Lepidoptera: Geometridae) related to complex topography combined into Geometra. However, further molecular and geological history. Systematic Entomology 41: 732–743. studies, including additional taxa, are needed to con- Cook MA. 1993. The systematics of Emerald Moths firm this hypothesis. (Geometridae, Geometrinae): wing pigments, tympanal organs and a revision of the neotropical genus Oospila Warren. Unpublished D. Phil. Thesis, Oxford University. ACKNOWLEDGEMENTS Cook MA, Harwood LM, Scoble MJ, McGavin GC. 1994. The chemistry and systematic importance of the green We are grateful to all collectors whose contributions wing pigment in emerald moths (Lepidoptera: Geometridae, made our work possible. We thank Professor Aibing Geometrinae). Biolchemical Systematics and Ecology 22: Zhang (Capital Normal University, Beijing, China) for 43–51. kindly providing the DNA of Pamphlebia rubrolim- Cummins CA, McInerney JO. 2011. A method for inferring braria, and thank Professor Jaan Viidalepp (Estonian the rate of evolution of homologous characters that can poten- University of Life Sciences, Estonia) for sending tially improve phylogenetic inference, resolve deep diver- us valuable literature. We thank Dr Chaodong Zhu gence and correct systematic biases. Systematic Biology 60: (Institute of Zoology, Chinese Academy of Sciences, 833–844. Beijing, China) for providing valuable suggestions Ferguson DC. 1969. A revision of the moths of the sub- on selecting genes. We sincerely appreciate Dr Axel family Geometridae of America, north of Mexico (Insecta, Hausmann (Zoologische Staatssammlung München, Lepidoptera). Bulletin of the Peabody Museum of Natural Munich, Germany) and two anonymous referees for History 29: 1–251. the valuable comments to the manuscript. We are Ferguson DC. 1985. Geometroidea, geometridae (part): subfamily geometrinae. In: Ferguson DC, Lawrence LH, Paige grateful for Sir Anthony Galsworthy (The Natural EM, Dominick RB, eds. The moths of America North of History Museum, London, UK) for correcting the Mexico (Lepidoptera). Fascicle 18.1. Washington, DC: Wedge English. This work was supported by the National Entomological Research Foundation, 1–131. Science Foundation of China (No. 31672331, 31372176, Fletcher DS. 1979. Geometroidea. In: Nye IWB, ed. The gen- 31702041) and the Ministry of Science and Technology eric names of moths of the World, Vol. 3. London: British of China (No. 2015FY210300). Museum (Natural History); 1–243. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. 1994. 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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.