Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-24T18:28:21.042Z Has data issue: false hasContentIssue false
  • English
  • Français

Allopatric separation represents an overlooked cryptic species in the Anania hortulata species complex (Lepidoptera: Crambidae: Pyraustinae): congruence between genetic and morphological evidence

Published online by Cambridge University Press:  18 March 2019

Zhaofu Yang Open the ORCID record for Zhaofu Yang [Opens in a new window]  and
Jean-François Landry
Zhaofu Yang*
Affiliation:
Key laboratory of Plant Protection Resources and Pest Management, Ministry of Education; Entomological Museum, College of Plant Protection, Northwest A&F University, Yangling, China
Jean-François Landry
Affiliation:
Agriculture and Agri-Food Canada, Ottawa Research & Development Centre, 960 Carling Avenue, Ottawa, Ontario, K1A 0C6, Canada
*
1Corresponding author (email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Anania hortulata (Linnaeus, 1758) (Lepidoptera: Crambidae: Pyraustinae) is a strikingly coloured, common, and widespread species that has long been recognised as a single species widely distributed in Asia, Europe, and North America. Using a combination of molecular and morphometric data, this study resolved that A. hortulata is actually a species complex of two superficially indistinguishable species. Phylogenetic and network analyses based on the mitochondrial COI gene discriminated lineages from all major geographical regions of China as distinct, A. sinensis Yang and Landry new species, whereas A. hortulata occurs in Central Asia, Europe, and North America. Nuclear gene (CAD) and morphological differences in the genital characters provided further evidence for the separation of A. hortulata and A. sinensis.

Type
Systematics and Morphology
Information
The Canadian Entomologist , Volume 151 , Issue 2 , April 2019 , pp. 163 - 186
Creative Commons
Parts of this are a work of Her Majesty the Queen in Right of Canada.
Copyright
© Entomological Society of Canada 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Atay, E. and Can, F. 2007. External and genital morphology of Eurrhypara hortulata (Linnaeus, 1758) (Crambidae). Journal of Entomology, 4: 479–483.CrossRefGoogle Scholar
Bae, Y.S., Byun, B.K., and Paek, M.K. 2008. Pyralid moths of Korea (Lepidoptera: Pyraloidea). Korean National Arboretum, Samsungad-Com, Seoul, South Korea.Google Scholar
Bandelt, H.-J., Forster, P., and Röhl, A. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology & Evolution, 16: 37–48.CrossRefGoogle ScholarPubMed
Brower, A.V. 1994. Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proceedings of the National Academy of Sciences of the United States of America, 91: 6491–6495.CrossRefGoogle ScholarPubMed
Chen, Q.H., Wu, B., Xing, M.X., and Wu, S. 2013. Experiment for trapping insects by pests forecasting lamp in semiarid region of Qiqihar. Protection Forest Science and Technology, 4: 21–23. [In Chinese].Google Scholar
Denis, J.N.C.M. and Schiffermüller, I. 1775. Ankündung eines systematischen Werkes von den Schmetterlingen der Wienergegend. Augustin Bernardi, Wien. 322 pp. + 2 pls.Google Scholar
deWaard, J.R., Ivanova, N.V., Hajibabaei, M., and Hebert, P.D.N. 2008. Assembling DNA barcodes: analytical protocols. In Methods in molecular biology: environmental genetics. Edited by Cristofre, M.. Humana Press, Totowa, New Jersey, United States of America. Pp. 275–293.Google Scholar
Dincă, V., Lukhtanov, V.A., Talavera, G., and Vila, R. 2011. Unexpected layers of cryptic diversity in wood white Leptidea butterflies. Nature Communications, 2: 1–8.CrossRefGoogle ScholarPubMed
Drummond, A.J. and Rambaut, A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7: 1–8.CrossRefGoogle ScholarPubMed
Edgar, R.C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32: 1792–1797.CrossRefGoogle ScholarPubMed
Ganev, J. 1996. Crambinae. In The Lepidoptera of Europe. A distributional checklist. Edited by Karsholt, O. and Razowski, J.. Apollo Books, Stenstrup, Denmark. Pp. 183–187.Google Scholar
Gillespie, D.P. and Gillespie, B.I. 1982. A list of plant-feeding Lepidoptera introduced into British Columbia. Journal of the Entomological Society of British Columbia, 79: 38–48.Google Scholar
Guindon, S. and Gascuel, O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52: 696–704.CrossRefGoogle ScholarPubMed
Haines, P.W. and Rubinoff, D. 2012. Molecular phylogenetic of the moth genus Omiodes Guenée (Crambidae: Spilomelinae), and the origins of the Hawaiian lineage. Molecular Phylogenetics and Evolution, 65: 305–316.CrossRefGoogle Scholar
Hajibabaei, M., Janzen, D.H., Burns, J.M., Hallwachs, W., and Hebert, P.D.N. 2006. DNA barcodes distinguish species of tropical Lepidoptera. Proceedings of the National Academy of Sciences of the United States of America, 103: 968–971.CrossRefGoogle ScholarPubMed
Hannemann, H.-J. 1964. Kleinschmetterlinge oder Microlepidoptera II. Die Wickler (s.l.) (Cochylidae und Carposinidae). Die Zünslerartigen (Pyraloidea). In Die Tierwelt Deutschlands, Teil 50, volume 8 Edited by Dahl, F.. Gustav Fischer, Jena, Germany.Google Scholar
Hebert, P.D.N., deWaard, J.R., Zakharov, E.V., Prosser, S.W., Sones, J.E., McKeown, J.T., et al. 2013. A DNA ‘barcode blitz’: rapid digitization and sequencing of a natural history collection. Public Library of Science One, 8: e68535.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Huemer, P., Elsner, G., and Karsholt, O. 2013. Review of the Eulamprotes wilkella species-group based on morphology and DNA barcodes, with descriptions of new taxa (Lepidoptera, Gelechiidae). Zootaxa, 3746: 69–100.CrossRefGoogle Scholar
Huemer, P., Karsholt, O., and Mutanen, M. 2014. DNA barcoding as a screening tool for potential unrecognized cryptic diversity exemplified by the genus Caryocolum, with description of a new species (Lepidoptera, Gelechiidae). ZooKeys, 404: 91–111.CrossRefGoogle Scholar
Huemer, P. and Mutanen, M. 2012. Taxonomy of spatially disjunct alpine Teleiopsis albifemorella s. lat. (Lepidoptera: Gelechiidae) revealed by molecular data and morphology—how many species are there? Zootaxa, 3580: 1–23.CrossRefGoogle Scholar
Inoue, H. 1982. Pyralidae. In Moths of Japan. Edited by Inoue, H., Sugi, S., Kuroko, H., Moriuti, S., and Kawabe, A.. Kodansha, Tokyo, Japan. Volume 1, Pp. 307–404; volume 2, pp. 223–254, 296–314, plates 36–48.Google Scholar
Ivanova, N.V., deWaard, J.R., and Hebert, P.D.N. 2006. An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes, 6: 998–1002.CrossRefGoogle Scholar
Karsholt, O. and van Nieukerken, E.J. 2013. Lepidoptera, moths. Fauna Europaea version 2017.06. Available from https://fauna-eu.org/cdm_dataportal/taxon/b64a743d-0469-4571-9ed4-061779300ac0 [accessed 25 November 2018].Google Scholar
Kimura, M. 1980. A simple model for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16: 111–120.CrossRefGoogle Scholar
Kozlov, M.V., Mutanen, M., Lee, K.M., and Huemer, P. 2017. Cryptic diversity in the long-horn moth Nemophora degeerella (Lepidoptera: Adelidae) revealed by morphology, DNA barcodes and genome-wide ddRAD-seq data. Systematic Entomology, 42: 329–346.CrossRefGoogle Scholar
Kristensen, N.P. 2003. Skeleton and muscles: adults. In Handbook of zoology, volume 4: Arthropoda: Insecta, part 36: Lepidoptera, moths and butterflies; volume 2: morphology, physiology, and development. Edited by Kristensen, N.P.. Walter de Gruyter, Berlin, Germany. Pp. 39–131.Google Scholar
Kumar, S., Stecher, G., and Tamura, K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33: 1870–1874.CrossRefGoogle ScholarPubMed
Landry, J.-F. 2007. Taxonomic review of the leek moth genus Acrolepiopsis (Lepidoptera: Acrolepiidae) in North America. The Canadian Entomologist, 139: 319–353.CrossRefGoogle Scholar
Landry, J.-F. and Hebert, P.D.N. 2013. Plutella australiana (Lepidoptera, Plutellidae), an overlooked diamondback moth revealed by DNA barcodes. ZooKeys, 327: 43–63.CrossRefGoogle Scholar
Leraut, P. 2005. Contributions à l’étude de quelques genres et espèces de Pyraustinae (Lepidoptera, Crambidae). Nouvelle Revue d’Entomologie (N.S.), 22: 123–139.Google Scholar
Li, H.H., Ren, Y.D., Zhang, D.D., Du, X.C., Li, W.C., and You, P. 2009. Insect fauna of Henan (Lepidoptera: Pyraloidea). Science Press, Beijing, China. Pp. 211–212. [In Chinese].Google Scholar
Li, H.H., Wang, S.X., Zhen, H., Zhang, J., Hu, B.B., Jing, Q., et al. 2012. Microlepidoptera of Qinling Mountains (Insecta: Lepidoptera). Science Press, Beijing, China. [In Chinese].Google Scholar
Linnaeus, C. 1758. Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Laurentii Salvii, Stockholm, Sweden.Google Scholar
Linnaeus, C. 1761. Fauna Suecica. Laurentii Salvii, Stockholm, Sweden. [1]–[43], pp. 1–578, plates 1–2.Google Scholar
Moth Photographers Group. 2017. Anania hortulata–small magpie moth [online]. Available from http://mothphotographersgroup.msstate.edu/species.php?hodges=4952 [accessed 25 November 2018].Google Scholar
Munroe, E.G. 1976. Pyraloidea Pyralidae comprising the subfamily Pyraustinae tribe Pyraustini (part). In The moths of America north of Mexico 13.2A. Edited by Dominick, R.B., Ferguson, D.C., Franclemont, J.G., Hodges, R.W., Munroe, E.G., and Classey, E.W.. The Wedge Entomological Research Foundation, London, United Kingdom. Pp. 1–78, plates 1–4, A–H.Google Scholar
Mutanen, M., Aarvik, L., Landry, J.-F., Segerer, A., and Karsholt, O. 2012. Epinotia cinereana (Haworth, 1811) bona sp., a Holarctic tortricid distinct from E. nisella (Clerck, 1759) (Lepidoptera: Tortricidae: Eucosmini) as evidenced by DNA barcodes, morphology and life history. Zootaxa, 3318: 1–25.CrossRefGoogle Scholar
Mutanen, M., Kekkonen, M., Prosser, S.W.J., Hebert, P.D.N., and Kaila, L. 2015. One species in eight: DNA barcodes from type specimens resolve a taxonomic quagmire. Molecular Ecology Resources, 15: 967–984.CrossRefGoogle ScholarPubMed
Mutanen, M., Wahlberg, N., and Kaila, L. 2010. Comprehensive gene and taxon coverage elucidates radiation patterns in moths and butterflies. Proceedings of the Royal Society of London B: Biological Sciences, 1695: 2839–2848.Google Scholar
Nuss, M., Landry, B., Mally, R., Vegliante, F., Tränkner, A., Bauer, F., et al. 2017. Global information system on Pyraloidea. Available from www.pyraloidea.org [accessed 22 November 2017].Google Scholar
Nylander, J.A.A., Ronquist, F., Huelsenbeck, J.P., and Nieves-Aldrey, J. 2004. Bayesian phylogenetic analysis of combined data. Systematic Biology, 53: 47–67.CrossRefGoogle ScholarPubMed
Padial, J.M. and De La Riva, I. 2010. A response to recent proposals for integrative taxonomy. Biological Journal of the Linnean Society, 101: 747–756.CrossRefGoogle Scholar
Pierce, F.N. Metcalfe, J.W. 1938. The genitalia of the British pyrales with the deltoids and plumes, Vol. 8. Published by the first author, Oundle, Northants, United Kingdom.Google Scholar
Posada, D. 2008. jModelTest: phylogenetic model averaging. Molecular Biology & Evolution, 25: 1253–1256.CrossRefGoogle ScholarPubMed
Rambaut, A., Drummond, A.J., Xie, D., Baele, G., and Suchard, M.A. 2018. Tracer v1.7. Available from http://beast.community/tracer [accessed 10 April 2018].Google Scholar
Ronquist, F. and Huelsenbeck, J.P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19: 1572–1574.CrossRefGoogle ScholarPubMed
Rozas, J., Sanchez-Delbarrio, J.C., Messeguer, X., and Rozas, R. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics, 19: 2496–2497.CrossRefGoogle ScholarPubMed
Shorthouse, D.P. 2010. SimpleMappr, an online tool to produce publication-quality point maps. Available from www.simplemappr.net [accessed 10 April 2018].Google Scholar
Sinev, S.J. 2008. Pyralidae. In Catalogue of the Lepidoptera of Russia. Edited by Sinev, S.J.. KMK Scientific Press, Saint Petersburg and Moscow, Russia. Pp. 156–170. [In Russian].Google Scholar
Slamka, F. 2013. Pyraloidea of Europe (Lepidoptera), volume 3, Pyraustinae and Spilomelinae. Slamka, Bratislava, Slovakia.Google Scholar
Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30: 1312–1313.CrossRefGoogle ScholarPubMed
Tamura, K. and Nei, N. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology & Evolution, 10: 512–526.Google ScholarPubMed
Tränker, A., Li, H.H., and Nuss, M. 2009. On the systematics of Anania Hübner, 1823. Nota lepidopterologica, 32: 63–80.Google Scholar
Treitschke, F. 1829. Die Schmetterlinge von Europa, 7 (Fortsetzung des Ochsenheimer’schen Werkes). Volume 6. Gerhard Fleischer, Leipzig, Germany.Google Scholar
van Nieukerken, E.J., Doorenweerd, C., Stokvis, F.R., and Groenenberg, D.S.J. 2012. DNA barcoding of the leaf-mining moth subgenus Ectoedemia s. str. (Lepidoptera: Nepticulidae) with COI and EF1-α: two are better than one in recognising cryptic species. Contributions to Zoology, 81: 1–24.CrossRefGoogle Scholar
Wahlberg, N. and Wheat, C.W. 2008. Genomic outposts serve the phylogenomic pioneers: designing novel nuclear markers for genomic DNA extractions of Lepidoptera. Systematic Biology, 57: 231–242.CrossRefGoogle ScholarPubMed
Wang, P.Y. 1980. Lepidoptera: Pyralidae. Economic insect fauna of China, supplement 21. Science Press, Beijing, China.Google Scholar
Xu, W., Lu, H., Yuan, H.B., and Kang, Z.X. 1999. A preliminary investigation of Pyralidae insect species in Changchun suburbs. Journal of Jilin Agricultural University, 21: 23–28. [In Chinese].Google Scholar
Yang, Z.F., Landry, J.-F. Handfield, L. Zhang, Y.L. Solis, M.A. Handfield, D., et al. 2012. DNA barcoding and morphology reveal three cryptic species of Anania (Lepidoptera: Crambidae: Pyraustinae) in North America, all distinct from their European counterpart. Systematic Entomology, 37: 686–705.CrossRefGoogle Scholar
Yang, Z.F., Landry, J.-F., and Hebert, P.D.N. 2016. A DNA barcode library for North American Pyraustinae (Lepidoptera: Pyraloidea: Crambidae). Public Library of Science One, 11: e0161449.Google Scholar