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Type: Article
Published: 2016-02-11
Page range: 229–245
Abstract views: 251
PDF downloaded: 92

Bridging the gap between chewing and sucking in the hemipteroid insects:
new insights from Cretaceous amber

Systematic Entomology, School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan.
Natural History Museum of the City of Geneva, CP 6434, CH-1211 Geneva 6, Switzerland
Hemiptera Burmese amber Archipsyllidae Paraneoptera Pancondylognatha Condylognatha new genus and species

Abstract

The diversity of feeding apparatuses in insects far exceeds that observed in any other animal group. Consequently, tracking mouthpart innovation in insects is one of the keys toward understanding their diversification. In hemipteroid insects (clade Paraneoptera or Acercaria: lice, thrips, aphids, cicadas, bugs, etc.), the transition from chewing to piercing-and-sucking mouthparts is widely regarded as the turning point that enabled hyperdiversification of the Hemiptera, the fifth largest insect order. However, the transitional process from chewing to piercing-and-sucking in the Paraneoptera was hitherto completely unknown. In this paper, we report a well preserved mid Cretaceous amber fossil of the paraneopteran insect family Archipsyllidae and describe it as Mydiognathus eviohlhoffae gen. et sp. n. This species has elongate mandibles and styliform laciniae similar to Hemiptera but retains functional chewing mouthparts. A number of morphological characters place the Archipsyllidae as the sister group of the thrips plus hemipterans, which strongly suggests that the mouthparts of M. eviohlhoffae represent a transitional condition from primitive chewing to derived piercing-and-sucking mouthparts. The clade composed of Archipsyllidae, thrips, and hemipterans is here named Pancondylognatha, a new supra-ordinal taxon. Based on newly obtained information, we also assess the monophyly of the Paraneoptera, which was called into question by recent phylogenomic analyses. A phylogenetic analysis that includes Mydiognathus strongly supports the monophyly of the Paraneoptera.

 

References

  1. Akimoto, S.I. (1983) A revision of the genus Eriosoma and its allied genera in Japan (Homoptera: Aphidoidea). Insecta Matsumurana New Series, 27, 37–106.

    Ansorge, J. (1996) Insekten aus dem oberen Lias von Grimmen (Vorpommern, Norddeutschland). Neue Paläontologische Abhandlungen, 2, 1–132.

    Badonnel, A. (1934) Recherches sur l'anatomie des Psoques. Bulletin Biologique de France et de Belgique, Supplément, 18, 1–241.

    Beutel, R.G., Friedrich, F., Hörnschemeyer, T., Pohl, H., Hünefeld, F., Beckmann, F., Meier, R., Misof, B., Whiting, M. & Vilhelmsen, L. (2011) Morphological and molecular evidence converge upon a robust phylogeny for the megadiverse Holometabola. Cladistics, 27, 341–355.
    http://dx.doi.org/10.1111/j.1096-0031.2010.00338.x

    Beutel, R.G., Friedrich, F., Ge, S.Q. & Yang, X.K. (2014) Insect Morphology and Phylogeny. Walter de Gruyter, Berlin, Germany, 516 pp.

    Bromley, A.K., Dunn, J.A. & Anderson, M. (1980) Ultrastructure of the antennal sensilla of aphids. II. Trichoid, chordotonal and campaniform sensilla. Cell and Tissue Research, 205, 493–511.
    http://dx.doi.org/10.1007/BF00232289

    Carpenter, F.M. (1992) Treatise on Invertebrate Paleontology, Part R, Arthropoda 4. Geological Society of America Inc, Boulder, 655 pp.

    Carver, M., Gross, G.F. & Woodward, T.E. (1991) Hemiptera (bugs, leafhoppers, cicadas, aphids, scale insects etc.). In: Naumann, I.D., Carne, P.B., Lawrence,J. F., Nielsen, E.S., Spradbery,J.P., Taylor, R.W., Whitten, M.J., & Littlejohn, M.J. (Eds), The Insects of Australia. Cornell University Press, Ithaca, NY, pp. 429–509.

    Forero, D. (2008) The systematics of the Hemiptera. Revista Colombiana de Entomología, 34, 1–21.

    Friedemann, K., Spangenberg, R., Yoshizawa, K. & Beutel, R.G. (2014) Evolution of attachment structures in the highly diverse Acercaria (Hexapoda). Cladistics, 30, 170–201.
    http://dx.doi.org/10.1111/cla.12030

    Friedrich, F., Matsumura, Y., Pohl, H., Bai, M., Hörnschemeyer, T. & Beutel, R.G. (2014) Insect morphology in the age of phylogenomics: innovative techniques and its future role in systematics. Entomological Science, 17, 1–24.

    http://dx.doi.org/10.1111/ens.12053

    Grimaldi, D. & Engel, M.S. (2005) Evolution of the Insects. Cambridge University Press, Cambridge, 755 pp.

    Hamilton, K.G.A. (1981) Morphology and evolution of the rhynchotan head (Insecta: Hemiptera, Homoptera). Canadian Entomologists, 113, 953–974.

    http://dx.doi.org/10.4039/Ent113953-11

    Hörnschemeyer, T. (2002) Phylogenetic significance of the wing-base of the Holometabola (Insecta). Zoologica Scripta, 31, 17–29.

    http://dx.doi.org/10.1046/j.0300-3256.2001.00086.x

    Huang, D.Y., Nel, A., Azar, D. & Nel, P. (2008) Phylogenetic relationships of the Mesozoic paraneopteran family Archipsyllidae (Insecta: Psocodea). Geobios, 41, 461–464.

    http://dx.doi.org/10.1016/j.geobios.2007.11.003

    Ishiwata, K., Sasaki, G., Ogawa, J., Miyata, T. & Su, Z.H. (2011) Phylogenetic relationships among insect orders based on three nuclear protein-coding gene sequences. Molecular Phylogenetics and Evolution, 58, 169–180.

    http://dx.doi.org/10.1016/j.ympev.2010.11.001

    Jiao, Y., Wickett, N.J, Ayyampalayam, S., Chanderbali, A.S., Landherr, L., Ralph, P.E., Tomsho, L.P., Hu, Y., Liang, H., Soltis, P.S., Soltis, D.E., Clifton, S.W., Schlarbaum, S.E., Schuster, S.C., Ma, H., Leebens-Mack, J. & Depamphilis, C.W. (2011) Ancestral polyploidy in seed plants and angiosperms. Nature, 473, 97–100.

    http://dx.doi.org/10.1038/nature09916

    Kéler, S. (1966) Zur Mechanik der Nahrungsaufnahme bei Corrodentien. Zeitchrift für Parasitenkunde, 27, 64–79.

    Krenn, H.W. (2010) Feeding mechanisms of adult Lepidoptera: structure, function, and evolution of the mouthparts. Annual Review of Entomology, 55, 307–327.

    http://dx.doi.org/10.1146/annurev-ento-112408-085338

    Krenn, H.W., Plant, J.D. & Szucsich, N.U. (2005) Mouthparts of flower-visiting insects. Arthropod Structure and Development, 34, 1–40.

    http://dx.doi.org/10.1016/j.asd.2004.10.002

    Kristensen, N.P. (1991) Phylogeny of Extant Hexapods. In: Naumann, I.D., Lawrence, J.F.,

    Nielsen, E.S., Spradberry, J.P., Taylor, R.W., Whitten, M.J., Littlejohn, M.J. (Eds), The Insects of Australia. Cornell University Press, Ithaca, NY, pp. 125–140.

    Labandeira, C.C. (1997) Insect mouthparts: ascertaining the paleobiology of insect feeding strategies. Annual Review of Ecology and Systematics, 28, 153–193.

    http://dx.doi.org/10.1146/annurev.ecolsys.28.1.153

    Labandeira, C.C. (2014) Amber. In: Laflamme, M., Schiffbauer, J.D. & Darroch, S.A.F. (Eds), Reading and Writing of the Fossil Record: Preservational Pathways to Exceptional Fossilization. Paleontological Society, Boulder, CO, pp. 163–216.

    Labandeira, C.C. & Phillips, T.L. (1996) Insect fluid-feeding on Upper Pennsylvanian tree ferns (Palaeodictyoptera, Marattiales) and the early history of the piercing-and-sucking functional feeding group. Annals of the Entomological Society of America, 89, 157–183.

    http://dx.doi.org/10.1093/aesa/89.2.157

    Lienhard, C. (1998) Psocoptères Euro-Méditerranéens. Faune de France, 83, i–xx 1–517.

    Lyal, C.H.C. (1985) Phylogeny and classification of the Psocodea, with particular reference to the lice (Psocodea: Phthiraptera). Systematic Entomology, 10, 145–165.

    http://dx.doi.org/10.1111/j.1365-3113.1985.tb00525.x

    Maddison, D.R. & Maddison, W.P. (2001) MacClade 4: Analysis of Phylogeny and Character Evolution. Sinauer Inc, Sunderland.

    Mashimo, Y., Matsumura, Y., Machida, R., Dallai, R., Gottardo, M., Yoshizawa, K., Friedrich, F., Wipfler, B. & Beutel, R.G. (2014) 100 years Zoraptera–a phantom in insect evolution and the history of its investigation. Insect Systematics & Evolution, 45, 371–393.
    http://dx.doi.org/10.1163/1876312X-45012110

    Misof, B., Liu, S., Meusemann, K., Peters, R.S., Donath, A., Mayer, C., Frandsen, P.B., Ware, J., Flouri, T., Beutel, R.G., Niehuis, O., Petersen, M., Izquierdo-Carrasco, F., Wappler, T., Rust, J., Aberer, A.J., Aspöck, U., Aspöck, H., Bartel, D., Blanke, A., Berger, S., Böhm ,A., Buckley, T.R., Calcott, B., Chen, J., Friedrich, F., Fukui, M., Fujita, M., Greve, C., Grobe, P., Gu, S., Huang, Y., Jermiin, L.S., Kawahara, A.Y., Krogmann, L., Kubiak, M., Lanfear, R., Letsch, H., Li, Y., Li, Z., Li, J., Lu, H., Machida, R., Mashimo, Y., Kapli, P., McKenna, D.D., Meng, G., Nakagaki, Y., Navarrete-Heredia, J.L., Ott, M., Ou, Y., Pass, G., Podsiadlowski, L., Pohl, H., von Reumont, B.M., Schütte, K., Sekiya, K., Shimizu, S., Slipinski, A., Stamatakis, A., Song, W., Su, X., Szucsich, N.U., Tan, M., Tan, X., Tang, M., Tang, J., Timelthaler, G., Tomizuka, S., Trautwein, M., Tong, X., Uchifune, T., Walzl, M.G., Wiegmann, B.M., Wilbrandt, J., Wipfler, B., Wong, T.K., Wu, Q., Wu, G., Xie, Y., Yang, S, Yang, Q., Yeates, D.K., Yoshizawa, K., Zhang, Q., Zhang, R., Zhang, W., Zhang, Y., Zhao, J., Zhou, C., Zhou, L., Ziesmann, T., Zou, S., Li, Y., Xu, X., Zhang, Y., Yang, H., Wang, J., Wang, J., Kjer, K.M. & Zhou, X. (2014) Phylogenomics resolves the timing and pattern of insect evolution. Science, 346, 763–767.
    http://dx.doi.org/10.1126/science.1257570

    Mound, L.A. & Masumoto, M. (2009) Australian Thripidae of the Anaphothrips genus-group (Thysanoptera), with three new genera and thirty-three new species. Zootaxa, 2042, 1–76.

    Müller, G.B. & Wagner, G.P. (2003) Innovation. In: Hall, B.K. & Olson, W.M. (Eds), Keywords & Concepts in Evolutionary Developmental Biology. Harvard University Press, Cambridge, pp. 218–227.

    Nel, A., Prokop, J., Nel, P., Grandcolas, P., Huang, D.Y., Roques, P., Guilbert, E., Dostál, O. & Szwedo, J. (2012) Traits and evolution of wing venation pattern in paraneopteran insects. Journal of Morphology, 273, 480–506.
    http://dx.doi.org/10.1002/jmor.11036

    Nel, P., Azar, D. & Nel, A. (2007) A new 'primitive' family of thrips from Early Cretaceous Lebanese amber (Insecta, Thysanoptera). Cretaceous Research, 28, 1033–1038.

    http://dx.doi.org/10.1016/j.cretres.2007.02.003

    Nel, P., Retana-Salazar, A.P., Azar, D., Nel, A. & Huang, D.Y. (2014) Redefining the Thripida (Insecta: Paraneoptera). Journal of Systematic Palaeontology, 12, 865–878.

    http://dx.doi.org/10.1080/14772019.2013.841781

    Özdikmen, H. (2009) Psocopsylla nom. nov., a new name for the preoccupied psocid genus Eopsylla Vishniakova, 1976 (Psocodea: Psocidiidae). Munis Entomology & Zoology 4, 613.

    Penny, D. (2010) Biodiversity of Fossils in Amber from the Major World Deposits. Siri Scientific Press, Manchester, 303 pp.

    Ren, D., Shih, C.K. & Labandeira, C.C. (2009) A probable pollination mode before angiosperms: Eurasian long-proboscid scorpionflies. Science 326, 840–847.

    http://dx.doi.org/10.1126/science.1178338

    Seeger, W. (1975) Funktionsmorphologie an Spezialbildungen der Fühlergeissel von Psocoptera und anderen Paraneoptera (Insecta): Psocodea als monophyletische Gruppe. Zeitschrift für Morphologie der Tiere, 81, 137–159.

    Shi, G., Grimaldi, D.A., Harlow, G.E., Wang, J., Wang, J., Yang, M., Lei, W., Li, Q. & Li, X. (2012) Age constraint on Burmese amber based on U–Pb dating of zircons. Cretaceous Research, 37, 155–163.
    http://dx.doi.org/10.1016/j.cretres.2012.03.014

    Smithers, C.N. (1972) The classification and phylogeny of the Psocoptera. The Australian Museum Memoir, 14, 1–349.
    http://dx.doi.org/10.3853/j.0067-1967.14.1972.424

    Snodgrass, R.E. (1935) Principles of Insect Morphology. McGraw-Hill Pub, NY, 667 pp.

    Sorenson, M.D. & Franzosa, E.A. (2007) TreeRot, Version 3. Boston University, Boston, MA.

    Swofford, D.L. (2002) PAUP*: Phylogenetic Analysis Using Parsimony (* and Other Methods), Version 4. Sinauer Inc, Sunderland.

    Tuxen, S.L. (1970) Taxonomists Glossary of Genitalia in Insects, Second Edition. Scandinavian University Books, Copenhagen, 359 pp.

    Vishniakova, V.N. (1976) Relict Archipsyllidae (Insecta: Psocoptera) in the Mesozoic fauna. Paleontology Journal, 2, 76–84.

    Yoshizawa, K. (2002) Phylogeny and higher classification of suborder Psocomorpha (Insecta: Psocodea: 'Psocoptera'). Zoological Journal of the Linnean Society, 136, 371–400.

    http://dx.doi.org/10.1111/zoj.12157

    Yoshizawa, K. (2011) Monophyletic Polyneoptera recovered by wing base structure. Systematic Entomology, 36, 377–394. http://dx.doi.org/10.1111/j.1365-3113.2011.00572.x

    Yoshizawa, K. & Johnson, K.P. (2005) Aligned 18S for Zoraptera (Insecta): Phylogenetic position and molecular evolution. Molecular Phylogenetics and Evolution, 37, 572–580.
    http://dx.doi.org/10.1016/j.ympev.2005.05.008

    Yoshizawa, K. & Johnson, K.P. (2010) How stable is the "Polyphyly of Lice" hypothesis (Insecta: Psocodea)?: A comparison of phylogenetic signal in multiple gene. Molecular Phylogenetics and Evolution, 55, 939–951.

    http://dx.doi.org/10.1016/j.ympev.2010.02.026

    Yoshizawa, K. & Saigusa, T. (2001) Phylogenetic analysis of paraneopteran orders (Insecta: Neoptera) based on forewing base structure, with comments on monophyly of Auchenorrhyncha (Hemiptera). Systematic Entomology, 26, 1–13.

    http://dx.doi.org/10.1046/j.1365-3113.2001.00133.x

    Yoshizawa, K. & Saigusa, T. (2003) Reinterpretations of clypeus and maxilla in Psocoptera, and their significance in phylogeny of Paraneoptera (Insecta: Neoptera). Acta Zoologica, 84, 33–40
    http://dx.doi.org/10.1046/j.1463-6395.2003.00127.x

    Zhao, C., Liu, X. & Yang, D. (2014) Wing base structural data support the sister relationship of Megaloptera and Neuroptera (Insecta: Neuropterida). PLoS ONE, 9, e114695.

    http://dx.doi.org/10.1371/journal.pone.0114695