A molecular phylogeny of the Palaearctic and Oriental members of the tribe Boarmiini (Lepidoptera : Geometridae : Ennominae)
Nan Jiang A D , Xinxin Li A B D , Axel Hausmann C , Rui Cheng A , Dayong Xue A and Hongxiang Han A E
+ Author Affiliations
- Author Affiliations
A Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, No. 1 Beichen West Road, Chaoyang District, Beijing 100101, China.
B University of Chinese Academy of Sciences, 19A Yuquan Road, Shijingshan District, Beijing 100049 China.
C SNSB – Zoologische Staatssammlung München, Münchhausenstraße 21, Munich 81247, Germany.
D These authors contributed equally to this work.
E Corresponding author. Email: hanhx@ioz.ac.cn
Invertebrate Systematics 31(4) 427-441 https://doi.org/10.1071/IS17005
Submitted: 11 January 2017 Accepted: 10 March 2017 Published: 23 June 2017
Abstract
Owing to the high species diversity and the lack of a modern revision, the phylogenetic relationships within the tribe Boarmiini remain largely unexplored. In this study, we reconstruct the first molecular phylogeny of the Palaearctic and Oriental members of Boarmiini, and infer the relationships among tribes within the ‘boarmiine’ lineage. One mitochondrial (COI) and four nuclear (EF-1α, CAD, RpS5, GAPDH) genes for 56 genera and 96 species of Boarmiini mostly from the Palaearctic and Oriental regions were included in the study. Analyses of Bayesian inference and maximum likelihood recovered largely congruent results. The monophyly of Boarmiini is supported by our results. Seven clades and seven subclades within Boarmiini were found. The molecular results coupled with morphological studies suggested the synonymisation of Zanclopera Warren, 1894, syn. nov. with Krananda Moore, 1868. The following new combinations are proposed: Krananda straminearia (Leech, 1897) (comb. nov.), Krananda falcata (Warren, 1894) (comb. nov.), and Krananda fulva (Yazaki, 1994) (comb. nov.). Our results also supported the monophyly of the ‘boarmiine’ lineage. Boarmiini were recovered as sister to the remaining taxa within the ‘boarmiine’ lineage, and Macariini were recovered as sister to Abraxini, Eutoeini and Cassymini.
Additional keywords: ‘boarmiine’ lineage, new combinations, new synonym, systematics, taxonomy.
References
Beljaev, E. A. (2000). Remarkable new genus and new species of the geometrid moths from central Asia, related to the genus Desertobia Viidalepp, 1989 (Lepidoptera, Geometridae, Ennominae) with notes on the taxonomy of the Desertobiini. Tinea 16, 240–245.Beljaev, E. A. (2006a). A morphological approach to the Ennominae (Lepidoptera: Geometridae). Spixiana 29, 215–216.
Beljaev, E. A. (2006b). Alternative order, tentative tribal system of Ennominae based on current family-group names. Personal communication, published in Forum Herbulot www pages without peer review. Available at http://www.herbulot.de/famgroup2.htm [Verified 2 March 2017].
Beljaev, E. A. (2016). Sem. Geometridae – Pyadenitzi [Fam. Geometridae – Geometer moth]. In ‘Annotated Catalogue of the Insects of Russian Far East. Volume II. Lepidoptera’. (Ed. A. S. Lelei.) pp. 518–666. (Dalnauka: Vladivostok, Russia.)
Choi, S. W., Kim, S. S., and Shin, Y. H. (1998). Systematics of the tribe Abraxini (Lepidoptera, Geometridae, Ennominae) in South Korea. Insecta Koreana 15, 41–76.
Cummins, C. A., and McInerney, J. O. (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.
| A method for inferring the rate of evolution of homologous characters that can potentially improve phylogenetic inference, resolve deep divergence and correct systematic biases.Crossref | GoogleScholarGoogle Scholar |
Duponchel, P. A. J. (1829). ‘Histoire Naturelle des Lépidoptères ou Papillons de France. Vol. 7.’ (Crevot: Paris.)
Fletcher, D. S. (1967). A revision of the Ethiopian species and a check list of the world species of Cleora (Lepidotpera: Geometridae). Bulletin of the British Museum (Natural History) 8, 1–119.
Fletcher, D. S. (1974). A revision of the old world genus Zamarada (Lepidoptera: Geometridae). Bulletin of the British Museum (Natural History), Entomology 22, 1–498.
Forbes, W. T. M. (1948). ‘Lepidoptera of New York and Neighboring States. 2 .’ (Memoirs of Cornwell University Agriculture Experimental Station: New York.)
Forum Herbulot (2003). The Forum Herbulot world list of family group names in Geometridae. Available at http://www.herbulot.de [Verified 2 March 2017].
Hampson, G. F. (1895). ‘The Fauna of British India Including Ceylon and Burma (Moths). Vol. 3.’ (Taylor and Francis.)
Hebert, P. D. N., Penton, E. H., Burns, J. M., Janzen, D. H., and Hallwachs, W. (2004). Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America 101, 14812–14817.
| Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVyju7g%3D&md5=fd2c5a6a051e47bbf50378d3f6a90445CAS |
Herbulot, C. (1963). Mise à jour de la liste des Geometridae de France. Alexanor 3, 17–24, 85–93.
Holloway, J. D. (1994). The Moths of Borneo. Part 11. Family Geometridae, Subfamily Ennominae. Malayan Nature Journal 47, 1–309.
Holloway, J. D. (1997). The Moths of Borneo. Part 10. Family Geometridae, Subfamily Sterrhinae, Larentiinae. Malayan Nature Journal 51, 1–242.
Inoue, H. (1956). Check List of the Lepidoptera of Japan. Part 3. (Rikusuisha: Tokyo.)
Inoue, H. (1982a). Geometroidea. In ‘Moths of Japan. Vol. 1’. (Eds H. Inoue, S. Sugi, H. Kuroko, S. Mroiuti and A. Kawabe.) pp. 412–579. (Kodansha: Tokyo.)
Inoue, H. (1982b). Geometroidea. In ‘Moths of Japan. Vol. 2’. (Ed. H. Inoue, S. Sugi, H. Kuroko, S. Mroiuti and A. Kawabe.) pp. 257–312. (Kodansha: Tokyo.)
Inoue, H. (1992). Twenty-four new species, one new subspecies and two new genera of the Geometridae (Lepidoptera) from East Asia. Bulletin of Otsuma Women’s University, Home Economics 28, 149–188.
Jiang, N., Xue, D. Y., and Han, H. X. (2011). A review of Ophthalmitis Fletcher, 1979 in China, with descriptions of four new species (Lepidoptera: Geometridae, Ennominae). Zootaxa 2735, 1–22.
Kawakita, A., Takimura, A., Terachi, T., Sota, T., and Kato, M. (2004). Cospeciation analysis of an obligate pollination mutualism: have Glochidion trees (Euphorbiaceae) and pollinating Epicephala moths (Gracillariidae) diversified in parallel? Evolution 58, 2201–2214.
| 1:CAS:528:DC%2BD2cXhtVentLnP&md5=e2a8659e5bbeef0dd10eac3570745ff8CAS |
Lanfear, R., Calcott, B., Ho, S. Y. W., and Guindon, S. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.
| PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnt1ehsbg%3D&md5=60257dbe2868778a4d0b3f3c019d85e1CAS |
McGuffin, W. C. (1977). Guide to the Geometridae of Canada (Lepidoptera). II. Subfamily Ennominae 2. Memoirs of the Entomological Society of Canada 109, 1–191.
| Guide to the Geometridae of Canada (Lepidoptera). II. Subfamily Ennominae 2.Crossref | GoogleScholarGoogle Scholar |
Miller, M. A., Pfeiffer, W., and Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In ‘Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010, New Orleans, LA’. pp. 1–8.
Õunap, E., Javois, J., Viidalepp, J., and Tammaru, T. (2011). Phylogenetic relationships of selected European Ennominae (Lepidoptera: Geometridae). European Journal of Entomology 108, 267–273.
| Phylogenetic relationships of selected European Ennominae (Lepidoptera: Geometridae).Crossref | GoogleScholarGoogle Scholar |
Õunap, E., Viidalepp, J., and Truuverk, A. (2016). Phylogeny of the subfamily Larentiinae (Lepidoptera: Geometridae): integrating molecular data and traditional classifications. Systematic Entomology 41, 824–843.
| Phylogeny of the subfamily Larentiinae (Lepidoptera: Geometridae): integrating molecular data and traditional classifications.Crossref | GoogleScholarGoogle Scholar |
Pierce, F. N. (1914). ‘The Genitalia of the Group Geometridae of the Lepidoptera of the British Islands.’ (Northern Publishing Company: Liverpool, UK.)
Pitkin, L. M. (2002). Neotropical ennomine moths: a review of the genera (Lepidoptera: Geometridae). Zoological Journal of the Linnean Society 135, 121–401.
| Neotropical ennomine moths: a review of the genera (Lepidoptera: Geometridae).Crossref | GoogleScholarGoogle Scholar |
Prout, L. B. (1912–1916). The Palaearctic Geometrae. In ‘The Macrolepidoptera of the World. Vol. 4’. (Ed. A. Seitz.) pp. 1–479. (Verlag A Kernen: Stuttgart, Germany.)
Rambaut, A., and Drummond, A. J. (2010). Tracer v1.5. Available at http://beast.bio.ed.ac.uk/Tracer.
Regier, J. C., Mitter, C., Kristensen, N. P., Davis, D. R., Van Nieukerken, E. J., Rota, J., Simonsen, T. J., Mitter, K. T., Kawahara, A. Y., Yen, S.-H., Cummings, M. P., and Zwick, A. (2015). A molecular phylogeny for the oldest (nonditrysian) lineages of extant Lepidoptera, with implications for classification, comparative morphology and life-history evolution. Systematic Entomology 40, 671–704.
| A molecular phylogeny for the oldest (nonditrysian) lineages of extant Lepidoptera, with implications for classification, comparative morphology and life-history evolution.Crossref | GoogleScholarGoogle Scholar |
Rindge, F. H. (1973). A revision of the North American species of the genus Pseudoboarmia (Lepidoptera, Geometridae). American Museum Novitates 2514, 1–27.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
| MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar |
Rota, J., and Wahlberg, N. (2012). Exploration of data partitioning in an eight-gene data set: phylogeny of metalmark moths (Lepidoptera, Choreutidae). Zoologica Scripta 41, 536–546.
| Exploration of data partitioning in an eight-gene data set: phylogeny of metalmark moths (Lepidoptera, Choreutidae).Crossref | GoogleScholarGoogle Scholar |
Rota, J., Zacharczenko, B. V., Wahlberg, N., Zahiri, R., Schmidt, B. C., and Wagner, D. L. (2016). Phylogenetic relationships of Acronictinae with discussion of the abdominal courtship brush in Noctuidae (Lepidoptera). Systematic Entomology 41, 416–429.
| Phylogenetic relationships of Acronictinae with discussion of the abdominal courtship brush in Noctuidae (Lepidoptera).Crossref | GoogleScholarGoogle Scholar |
Sato, R. (1981). Taxonomic notes on the genus Calicha Moore and its allied new genus from Japan and adjacent countries (Lepidoptera: Geometridae). Tyô to Ga 31, 103–120.
Sato, R. (1984). Taxonomic study of the genus Hypomecis Hübner and its allied genera from Japan (Lepidoptera: Geometridae: Ennominae). Special Bulletin of Essa Entomological Society 1, 1–213.
Sato, R. (1995a). Descriptions of two new genera and eight new species of the Boarmiini (Geometridae, Ennominae) from Sulawesi. Transactions of the Lepidopterological Society of Japan 46, 33–43.
Sato, R. (1995b). Records of the Boarmiini (Geometridae: Ennominae) from Thailand. II. Transactions of the Lepidopterological Society of Japan 46, 209–227.
Sato, R. (1996). Records of the Boarmiini (Geometridae; Ennominae) from Thailand. III. Transactions of the Lepidopterological Society of Japan 47, 223–236.
Sato, R. (1999). Yazakia, a new genus of the Boarmiini (Ennominae, Geometridae), with descriptions of four new species from Sulawesi. Transactions of the Lepidopterological Society of Japan 50, 41–47.
Sato, R. (2002). Two new species and two new subspecies of the Boarmiini from Taiwan, with notes on Alcis anmashanensis Sato (Geometridae, Ennominae). Transactions of the Lepidopterological Society of Japan 53, 141–149.
Sato, R. (2005). Records of the Boarmiini (Geometridae, Ennominae) from Thailand. IV. Transactions of the Lepidopterological Society of Japan 56, 63–72.
Sato, R. (2007). The genus Monocerotesa Wehrli (Geometridae, Ennominae) in Sumatra, with description of one new species. Transactions of the Lepidopterological Society of Japan 58, 371–378.
Sato, R. (2008). Two new genera and three new species of the Boarmiini (Geometridae, Ennominae) from Sumatra. Tinea 20, 163–169.
Sato, R. (2013). New and unrecorded species of the Boarmiini (Geometridae, Ennominae) from Sumatra, with some taxonomic notes. Tinea 22, 242–252.
Sato, R. (2014). Micromedasina, a new genus of the Boarmiini (Ennominae, Geometridae), with descriptions of two new species from south east Asia. Tinea 23, 78–83.
Sato, R. (2016). Five new species of the genera Hypomecis Hübner, Ophthalmitis Fletcher and Phthonosema Warren (Geometridae; Ennominae) from the Indo-Malayan region. Tinea 23, 241–248.
Sato, R., and Fu, C-M. (2010). Two new species of the Boarmiini (Geometridae, Ennominae) from Taiwan. Tinea 21, 122–128.
Sato, R., and Wang, M. (2004). Records and descriptions of the Boarmiini (Geometridae, Ennominae) from Nanling Mts, S. China. Part 1. Tinea 18, 43–55.
Sato, R., and Wang, M. (2005). Records and descriptions of the Boarmiini (Geometridae, Ennominae) from Nanling Mts, S. China. Part 2. Tinea 19, 36–47.
Sato, R., and Wang, M. (2006). Records and descriptions of the Boarmiini (Geometridae, Ennominae) from Nanling Mts, S. China. Part 3. Tinea 19, 69–79.
Sato, R., and Wang, M. (2007). Records and descriptions of the Boarmiini (Geometridae, Ennominae) from Nanling Mts, S. China. Part 4. Tinea 20, 33–44.
Sato, R., and Wang, M. (2016). Records and descriptions of the Boarmiini (Geometridae, Ennominae) from Nanling Mts, S. China. Part 5. Tinea 23, 257–269.
Scoble, M. J. (1999). ‘Geometrid Moths of the World: A Catalogue (Lepidoptera, Geometridae). Vols 1 and 2’. (CSIRO Publishing & Apollo Books: Stenstrup, Denmark.)
Scoble, M. J., and Hausmann, A. (2007). Online list of valid and available names of the Geometridae of the World. Available at http://www.herbulot.de/globalspecieslist.htm [Verified 2 March 2017].
Sihvonen, P., Mutanen, M., Kaila, L., Brehm, G., Hausmann, A., and Staude, H. S. (2011). Comprehensive molecular sampling yields a robust phylogeny for geometrid moths (Lepidoptera: Geometridae). PLoS One 6, e20356.
| Comprehensive molecular sampling yields a robust phylogeny for geometrid moths (Lepidoptera: Geometridae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnt1GqtLw%3D&md5=a251c6d8ead3603bf0bea433b81005a6CAS |
Sihvonen, P., Staude, H. S., and 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.
| Systematic position of the enigmatic African cycad moths: an integrative approach to a nearly century old problem (Lepidoptera: Geometridae, Diptychini).Crossref | GoogleScholarGoogle Scholar |
Skou, P., and Sihvonen, P. (2015). Ennominae I. In ‘The Geometrid Moths of Europe. Vol. 5’. (Ed. A. Hausmann.) pp. 1–657. (Brill: Leiden, Holland.)
Stamatakis, A., Hoover, P., and Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML web-servers. Systematic Biology 57, 758–771.
| A rapid bootstrap algorithm for the RAxML web-servers.Crossref | GoogleScholarGoogle Scholar |
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
| MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=3f090ed3d6651d2e6c024dc921d7da05CAS |
Velyaev, O. A., and Beljaev, E. A. (2016). Description of skeleton-muscular apparatus of the male genitalia of Ematurga atomaria (Linnaeus, 1758) (Lepidoptera: Geometridae: Ennominae). A. I. Kurentsov’s Annual Memorial Meetings 27, 182–188.
Viidalepp, J., Tammaru, T., Snäll, N., and Wahlberg, N. (2007). Cleorodes Warren, 1894 does not belong in the tribe Boarmiini (Lepidoptera: Geometridae). European Journal of Entomology 104, 303–309.
| Cleorodes Warren, 1894 does not belong in the tribe Boarmiini (Lepidoptera: Geometridae).Crossref | GoogleScholarGoogle Scholar |
Wahlberg, N., Snäll, N., Viidalepp, J., Ruohomäki, K., and Tammaru, T. (2010). The evolution of female flightlessness among Ennominae of the Holarctic forest zone (Lepidoptera, Geometridae). Molecular Phylogenetics and Evolution 55, 929–938.
| The evolution of female flightlessness among Ennominae of the Holarctic forest zone (Lepidoptera, Geometridae).Crossref | GoogleScholarGoogle Scholar |
Wang, H., Wahlberg, N., Holloway, J. D., Bergsten, J., Fan, X., Janzen, D. H., Hallwachs, W., Wen, L., Wang, M., and Nylin, S. (2015). Molecular phylogeny of Lymantriinae (Lepidoptera, Noctuoidea, Erebidae) inferred from eight gene regions. Cladistics 31, 579–592.
| Molecular phylogeny of Lymantriinae (Lepidoptera, Noctuoidea, Erebidae) inferred from eight gene regions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvVamsrnL&md5=bafedc8011ee1110353ad59dd6aef57aCAS |
Wehrli, E. (1938–1954). Subfamilie: Geometrinae. In ‘Die Grossschmetterlinge der Erde. Vol. 4’. (Ed. A. Seitz.) pp. 254–766. (Verlag A Kernen: Stuttgart.)
Yamamoto, M., Nakatomi, K., Sato, R., Nakajima, H., and Owada, M. (1987). ‘Larvae of Larger Moths in Japan.’ (Ed. S. Sugi.) (Kodansha: Tokyo.)
Yamamoto, S., and 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.
| Phylogeny of the Geometridae and the evolution of winter moths inferred from a simultaneous analysis of mitochondrial and nuclear genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnslGgs7c%3D&md5=6e890d922819517d186e3be93a343659CAS |
Young, C. J. (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.
Young, C. J. (2008). Characterisation of the Australian Nacophorini using adult morphology, and phylogeny of the Geometridae based on morphological characters. Zootaxa 1736, 1–141.
Zahiri, R., Kitching, I. J., Lafontaine, J. D., Mutanen, M., Kaila, L., Holloway, J. D., and Wahlberg, N. (2011). A new molecular phylogeny offers hope for a stable family level classification of the Noctuoidea (Lepidoptera). Zoologica Scripta 40, 158–173.
Zahiri, R., Holloway, J. D., Kitching, I. J., Lafontaine, J. D., Mutanen, M., and Wahlberg, N. (2012). Molecular phylogenetics of Erebidae (Lepidoptera, Noctuoidea). Systematic Entomology 37, 102–124.
| Molecular phylogenetics of Erebidae (Lepidoptera, Noctuoidea).Crossref | GoogleScholarGoogle Scholar |
Zahiri, R., Lafontaine, D., Schmidt, C., Holloway, J. D., Kitching, I. J., Mutanen, M., and Wahlberg, N. (2013). Relationships among the basal lineages of Noctuidae (Lepidoptera, Noctuoidea) based on eight gene regions. Zoologica Scripta 42, 488–507.
| Relationships among the basal lineages of Noctuidae (Lepidoptera, Noctuoidea) based on eight gene regions.Crossref | GoogleScholarGoogle Scholar |
