Abstract
This paper reports the recent discovery of flightless populations of weevils of the genus Notaris in Yunnan and Sichuan provinces of China. Specimens were found in the middle or high altitude mountains (2440–4195 m), by either sifting leaf litter in the deciduous forest and among alpine Rhododendron shrubs, or by turning rocks in the alpine zone. These finds extend southwards the Asian range of this Holarctic genus and report its highest altitudinal records. DNA barcodes of 127 specimens were phylogenetically analysed, of them 42 are those of newly discovered Notaris from Southwest China. The genera Notaris and Tournotaris consistently formed a clade, with Tournotaris nested inside Notaris in Maximum Parsimony (MP) and Maximum Likelihood (ML) analysis. The newly discovered flightless Notaris from Southwest China were either monophyletic (MP) or paraphyletic with respect to volant Holarctic N. aethiops (ML); the latter placement being likely an artefact. A strict linear molecular clock approach suggests a pre-Pliocene separation of Notaris populations in Southwest China. Habitat associations of these high-altitude flightless Notaris contrast sharply with that of the predominantly volant lowland riparian Notaris and other Erirhinini. We hypothesis that evolution of habitat selection in Notaris went from lowland riparian, to high altitude (via uplift of the Tibetan Plateau and adjacent regions of Central Asia), and then to forest leaf litter (via subsequent erosions of isolated mountains such as Emei Shan in Sichuan losing the alpine zone and forcing Notaris into the forest floor). Taxonomic uncertainty of Asian Notaris is addressed and remains unresolved due to uninformative morphology and conflicting DNA signal. Identities of two obscure and likely closely related species, Notaroides brevirostris and Notaris kozlovi from nearby SE Qinghai and NW Sichuan, respectively, are discussed and illustrated. Pending further research, all reported flightless Notaris from Yunnan and Sichuan are hypothesised to form a clade, for which the available name N. kozlovi is used. Habitus and genitalia of Notaris specimens from the newly detected populations are illustrated.
References
Alonso-Zarazaga, M.A. (2007) On terminology in Curculionoidea (Coleoptera). Boletín Sociedad Entomológica Aragonesa, 40, 210.
Alonso-Zarazaga, M.A. & Lyal, C.H.C. (1999) A world catalogue of families and genera of Curculionoidea (Insecta: Coleoptera) (excepting Scolytidae and Platypodidae). Entomopraxis, Barcelona, 315 pp.
Bajtenov, M.S. (1974) Zhuki-dolgonosiki (Coleoptera: Attelabidae, Cucrulionidae) Srednej Azii i Kazakhstana. Illjustrirovannyj Opredelitel’ Rodov i Katalog Vidov. Izdatel’stvo Nauka Kazakhskoy SSR, Alma-Ata, 285 pp.
Belousov, I.A. (1998) Le complexe générique de Nannotrechus Winkler du Caucase et de la Crimée (Coleoptera, Carabidae, Trechini). Pensoft Series Faunistica N 8, Sofia–Moscow–St. Petersburg, 256 pp.
Bouchard, P., Bousquet, Y., Davies, A.E., Alonso-Zarazaga, M.A., Lawrence, J.F., Lyal, C.H.C., Newton, A.F., Reid, C.A.M., Schmitt, M., Ślipinśki, S.A. & Smith, A.B.T. (2011) Family-group names in Coleoptera (Insecta). ZooKeys, 88, 1–972.
http://dx.doi.org/10.3897/zookeys.88.807
Bromham, L. (2008) Reading the story in DNA: a beginner’s guide to molecular evolution. Oxford University Press, Oxford, 368 pp.
Caldara, R. (2011) Erirhinidae. In: Löbl, I. & Smetana, A. (Eds.), Catalogue of Palaearctic Coleoptera, Volume 7 Curculionoidea I. Apollo Books, Stenstrup, pp. 192–198
Caldara, R. & O'Brian, C.W. (1995) Curculionidae: aquatic weevils of China (Coleoptera). In: Jäch, M.A. & Ju, L. (Eds.), Water Beetles of China Volume 1. Zoologisch-Botanische Gesellschaft in Österreich and Wiener Coleopterologenverein, Wien, pp. 389–408.
Cohen, K.M., Finney, S. & Gibbard, P.L. (2013) International Chronostratigraphic Chart, International Commission on Stratigraphy. Available from: http://www.stratigraphy.org/ICSchart/ChronostratChart2013-01.pdf (accessed 12 March 2014)
Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969–1973.
http://dx.doi.org/10.1093/molbev/mss075
Egorov, A.B., Zherikhin, V.V. & Korotyaev, B.A. (1996) 112b. Curculionidae – Dolgonosiki. In: Ler, P.A. (Ed.), Opredelotel’ Nasekomykh Dal’nego Vostoka Rossii. Tom 3. Zhestkokrylye, ili Zhuki. Chast’ 3. Vladivostiok, Dal’nauka, pp. 341–522.
Favre, A., Päckert, M., Pauls, S.U., Jähnig, S.C., Uhl, D., Michalak, I. & Muellner-Riehl, A.N. (2015) The role of the uplift of the Qinghai-Tibetan Plateau for the evolution of Tibetan biotas. Biological Reviews, 90, 236–253.
http://dx.doi.org/10.1111/brv.12107
Faust, J. (1885) Turkestanische Russelkäfer. Stettiner Entomologische Zeitung, 46, 149–202.
Germar, E.F. (1817) Miscellen und Correspondenz-Nachrichten. Magazin der Entomologie, 2, 339–341. [not seen, cited after Thompson 2006]
Grebennikov, V.V. (2014a) DNA barcode and phylogeography of six new high altitude wingless Niphadomimus (Coleoptera: Curculionidae: Molytinae) from South-West China. Zootaxa, 3838, 151–173.
http://dx.doi.org/10.11646/zootaxa.3838.2.1
Grebennikov, V.V. (2014b) Morimotodes, a new genus for two minute wingless litter species from southwest China and Taiwan with an illustrated overview of Molytina and Plinthina genera (Coleoptera: Curculionidae: Molytini). Bonn Zoological Bulletin, 63, 123–147.
Grebennikov, V.V. (2015) Neglected Trichalophus (Coleoptera: Curculionidae): DNA barcode and phylogeography of high-altitude flightless weevils rediscovered in Southwest China. Bonn Zoological Bulletin, 64, 59–76.
Grebennikov, V.V. & Smetana, A. (2015) DNA barcoding and regional diversity of understudied Micropeplinae (Coleoptera: Staphylinidae) in Southwest China: phylogenetic implications and a new Micropeplus from Mount Emei. Zootaxa, 3919, 583–599.
http://dx.doi.org/10.11646/zootaxa.3919.3.8
Gültekin, L. (2013) Two erirhinid weevils, Notaris scirpi (F.) and Tournotaris bimaculata (F.) (Coleoptera: Curculionoidea: Erirhinidae) new from Turkey. Journal of the Entomological Research Society, 15, 67–70.
Harris, N. (2006) The elevation history of the Tibetan Plateau and its implications for the Asian monsoon. Palaeogeography, Palaeoclimatology, Palaeoecology, 241, 4–15.
http://dx.doi.org/10.1016/j.palaeo.2006.07.009
Hendrich, L., Morinière, J., Haszprunar, G., Hebert, P.D.N., Hausmann, A., Köhler, F. & Balke, M. (2015) A comprehensive DNA barcode database for Central European beetles with a focus on Germany: adding more than 3500 identified species to BOLD. Molecular Ecology Resources, 15, 795–818.
http://dx.doi.org/10.1111/1755-0998.12354
Kojima, H., Kantoh, J. & Okajima, S. (2010) Two erirhinid weevils (Coleoptera, Erirhinidae) known as rice pests new to Laos. Elytra, 38, 226.
Korotyaev, B.A. (1979) To the knowledge of the weevil fauna (Coleoptera, Curculionidae) of Mongolia and adjacent territories. 1. Insects of Mongolia, 6, 135–183.
Legalov, A.A. (1997) Neue Taxone aus den Familien Apionidae und Curculionidae der Russelkäfer (Coleoptera) aus Sibirien. Entomologica Basiliensia, 20, 467–475.
http://dx.doi.org/10.1603/0013-8746(2007)100[649:PAAAMF]2.0.CO;2Li, S., Sun, L., Oseto, C.Y. & Ferris, V.R. (2007) Phylogenetic analyses and a method for rapid molecular diagnosis of two sunflower seed weevils (Coleoptera: Curculionidae). Annals of the Entomological Society of America, 100, 649–654.
http://dx.doi.org/10.1603/0013-8746(2007)100[649:paaamf]2.0.co;2
Lyal, C.H.C. (1990) A new genus and species of rice weevil from the Sahel (Coleoptera: Curculionidae: Erirhininae). Bulletin of Entomological Research, 80, 183–189.
http://dx.doi.org/10.1017/s0007485300013407
McKenna, D.D., Sequeira, A.S., Marvaldi, A.E. & Farrell B.D. (2009) Temporal lags and overlap in the diversification of weevils and flowering plants. Proceedings of the National Academy of Sciences USA, 106, 7083–7088.
http://dx.doi.org/10.1073/pnas.0810618106
Mitterboeck, T.F. & Adamowicz, S.J. (2013) Flight loss linked to faster molecular evolution in insects. Proceeding of the Royal Society, Series B Biological Sciences, 280, 20131128.
http://dx.doi.org/10.1098/rspb.2013.1128
Oberprieler, R.G. (2014) 3.7.1 Brachycerinae Billberg, 1820. In: Leschen, R.A.B. & Beutel, R.G. (Eds.), Handbook of Zoology, Arthropoda: Insecta: Coleoptera. Volume 3: Morphology and Systematics (Phytophaga). Walter de Gruyter, Berlin, pp. 424–451.
O'Brien, C.W. & Anderson, D.M. (1996) A catalog of the Coleoptera on America north of Mexico. Family: Curculionidae, subfamily: Erirhininae. Agriculture Handbook, 529–143f: x+39 pp.
Papadopoulou, A., Anastasiou, I. & Vogler, A.P. (2010) Revisiting the insect mitochondrial molecular clock: the mid-aegean trench calibration. Molecular Biology and Evolution, 27, 1659–1672.
http://dx.doi.org/10.1093/molbev/msq051
Pierce R.A. (1960) Russian Central Asia 1867–1917. A Study in Colonial Rule. University of California Press, Berkeley, viii+359 pp.
Popper, K. (1959) The Logic of Scientific Discovery. Basic Books, New York, 484 pp.
http://dx.doi.org/10.1177/00027162603280017451
Rambaut, A. (2014) FigTree, Version 1.4. Available from: http://tree.bio.ed.ac.uk/software/figtree/ (accessed 12 March 2014)
Ratnasingham, S. & Hebert, P.D.N. (2013) A DNA-based registry for all animal species: the barcode index number (BIN) system. PLoS ONE, 8(8), e66213.
http://dx.doi.org/10.1371/journal.pone.0066213
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.
http://dx.doi.org/10.1093/sysbio/sys029
Shorthouse, D.P. (2010) SimpleMappr, an online tool to produce publication-quality point maps. Available from: http://www.simplemappr.net (accessed 12 March 2014)
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30, 2725–2729.
http://dx.doi.org/10.1093/molbev/mst197
Tänzler, R., Van Dam, M.H., Toussaint, E.F.A., Suhardjono, Y.R., Balke, M. & Riedel, A. (2016) Macroevolution of hyperdiverse flightless beetles reflects the complex geological history of the Sunda Arc. Scientific Reports, 6, 18793, 1–12.
http://dx.doi.org/10.1038/srep18793
Thompson, R.T. (1992) Observations on the morphology and classification of weevils (Coleoptera, Curculionoidea) with a key to major groups. Journal of Natural History, 26, 835–891.
http://dx.doi.org/10.1080/00222939200770511
Thompson, R.T. (2005) On the nomenclature and taxonomy of Tournotaris Alonso-Zarazaga & Lyal, 1999 and related genera (Coleoptera: Curculionoidea: Erirhinidae). Deutsche Entomologische Zeitschrift, 52, 125–130.
http://dx.doi.org/10.1002/mmnd.200310005
Thompson, R.T. (2006) A revision of the weevil genus Procas Stephens (Coleoptera: Curculionoidea: Erirhinidae). Zootaxa, 1234, 1–63.
Wanat, M. (2007) Alignment and homology of male terminalia in Curculionoidea and other Coleoptera. Invertebrate Systematics, 21, 147–171.
http://dx.doi.org/10.1071/is05055
Welch, J.J. & Bromham, L. (2005) Molecular dating when rates vary. Trends in Ecology and Evolution, 20, 320–327.
http://dx.doi.org/10.1016/j.tree.2005.02.007
Westra, P.H., Wyse, D.L. & Cook, E.F. (1981) Weevil (Notaris bimaculatus) feeding reduces effectiveness of glyphosate on quackgrass (Agropyron repens). Weed Science, 29, 540–547.
Westwood, J.O. (1838) Synopsis of the genera of British insects. In: An introduction to the modern classification of insects, founded on the natural history and corresponding organisation of the different families, Vol. II. Longman, Orme, Brown, Green & Longmans, London, pp. 1–48. [not seen, cited after Thompson 2006]