Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-27T12:35:29.609Z Has data issue: false hasContentIssue false

Molecular phylogeny of Fordini (Hemiptera: Aphididae: Pemphiginae) inferred from nuclear gene EF-1 α and mitochondrial gene COI

Published online by Cambridge University Press:  24 July 2007

H.C. Zhang
Affiliation:
Institute of Zoology, Chinese Academy of Sciences, 25 Beisihuanxi Road, Haidian District, Beijing 100080, China Graduate University of the Chinese Academy of Sciences, Beijing 100049, China
G.X. Qiao*
Affiliation:
Institute of Zoology, Chinese Academy of Sciences, 25 Beisihuanxi Road, Haidian District, Beijing 100080, China
*
*Author for correspondence Fax: +86-10-64807099 E-mail: [email protected]

Abstract

The tribe Fordini is a fascinating group because of its complicated life history, primary host specificity and gall-forming characteristic. Different species produce galls with different morphology on different parts of the host plants. The EF-1α-based, COI-based and combined sequences-based phylogenetic trees with three algorithms MP, ML and Bayes all strongly suggest that Fordini is a monophyletic group with two clades corresponding to two subtribes, Fordina and Melaphidina, each also monophyletic. Some important morphological characters and primary host plants of aphids were mapped onto the phylogenetic tree to analyse the division of subtribes and to uncover at which level the aphids correspond to their primary hosts, Pistacia and Rhus. Results suggest that the division of subtribes in Fordini is closely related to host selection of aphids. The evolution of gall morphology and the probable driving force behind it in this tribe were also discussed. The Fordini aphids seem to have evolved towards a better ability to manipulate their host plant, induce strong sinks and gain high reproductive success. Galls in this tribe evolved mainly along two directions to attain this goal: (i) by enlarging the gall from small bag to spherical, even big cauliflower-like, and changing the galls' location or forming two galls in their life cycle (Fordina); (ii) by moving the gall position from midrib, petiole of the leaflet, and eventually to the common petiole of the compound leaf (Melaphidina).

Type
Research Article
Copyright
Copyright © Cambridge University Press 2007

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

Blackman, R.L. & Eastop, V.F. (1984) Aphids on the world's crops: an identification and information guide. 2nd edn. 466 pp. Chichester, John Wiley and Sons.Google Scholar
Blackman, R.L. & Eastop, V.F. (1994) Aphids on the world's trees: an identification and information guide. 904 pp. Wallingford, Oxon, CAB International.CrossRefGoogle Scholar
Bodenheimer, F.S. & Swirski, E. (1957) The Aphidoidea of the Middle East. 378 pp. Jerusalem, Weizmann.Google Scholar
Börner, C. (1952) Europe Centralis Aphides. Die Blattlause Mitteleuropas. Namen, Synonyme, Wirtspflanzen, Generationszyklen. Mitteilungen der Thüringischen Boanischen Gesellschaft 3, 1488.Google Scholar
Burstein, M. & Wool, D. (1993) Gall aphids do not select optimal galling sites (Smynthurodes betae; Pemphigidae). Ecological Entomology 18, 155164.CrossRefGoogle Scholar
Crespi, B.J. & Worobey, M. (1998) Comparative analysis of gall morphology in Australian gall thrips: the evolution of extended phenotypes. Evolution 52, 16861696.CrossRefGoogle ScholarPubMed
Davatchi, A.G. (1958) Etude biologique de la faune entomologique des Pistacia sauvages et cultives. Revue de Pathologie Vegetale et d' Enomologie Agricole de France 37, 1166.Google Scholar
Farris, J.S., Källersjö, A., Kluge, A.G. & Bult, C. (1995) Testing significance of incongruence. Cladistics 10, 315319.CrossRefGoogle Scholar
Favret, C. & Voegtlin, D.J. (2004) Speciation by host-switching in Cinara (Insecta: Hemiptera: Aphididae). Molecular Phylogenetics and Evolution 32, 139151.CrossRefGoogle ScholarPubMed
Felsenstein, J. (1983) Parsimony in systematics: biological and statistical issues. Annual Review of Ecology and Systematics 14, 313333.CrossRefGoogle Scholar
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783791.CrossRefGoogle ScholarPubMed
Fukatsu, T., Aoki, S., Kurosu, U. & Ishikawa, H. (1994) Phylogeny of Cerataphidini aphids revealed by their symbiotic microorganisms and basic structure of their galls: implications for host–symbiont coevolution and evolution of sterile soldier castes. Zoological Science 11, 613623.Google Scholar
Ghosh, A.K. (1984) Fauna of India, Homoptera, Aphidoidea, Subfamily Pemphiginae. 429 pp. Calcutta, Zoological Survey of India.Google Scholar
Heie, O.E. (1980) The Aphidoidea of Fennoscandia and Denmark. I. Fauna Entomologica Scandinavica 9, 1236.Google Scholar
Huelsenbeck, J.P., Ronquist, F., Nielsen, R. & Bollback, J.P. (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294, 23102314.CrossRefGoogle ScholarPubMed
Inbar, M., Wink, M. & Wool, D. (2004) The evolution of host plant manipulation by insects: molecular and ecological evidence from gall-forming aphids on Pistacia. Molecular Phylogenetics and Evolution 32, 504511.CrossRefGoogle ScholarPubMed
Mani, M.S. (1964) The ecology of plant galls. 434 pp. The Hague, W. Junk.CrossRefGoogle Scholar
Nyman, T., Roininen, H. & Vuorinen, J. (1998) Evolution of different gall types in willow-feeding sawflies (Hymenoptera: Tenthredinidae). Evolution 52, 465474.CrossRefGoogle ScholarPubMed
Palumbi, S.R. (1996) Nucleic acids II: the polymerase chain reaction. pp. 205247in Hillis, D.M., Moritz, C. & Mable, B.K. (Eds) Molecular systematics. Sunderland, Massachusetts, Sinauer.Google Scholar
Posada, D. & Crandall, K.A. (1998) MODELTEST, testing the model of DNA substitution. Bioinformatics 14, 817818.CrossRefGoogle ScholarPubMed
Powell, G., Tosh, C.R. & Hardie, J. (2006) Host plant selection by aphids: behavioral, evolutionary, and applied perspectives. Annual Review of Entomology 51, 309330.CrossRefGoogle ScholarPubMed
Remaudière, G. & Remaudière, M. (1997) Catalogue des Aphididae du Monde. Homoptera Aphidoidea. 473 pp. Paris, INRA.Google Scholar
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBAYES 3, Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.CrossRefGoogle ScholarPubMed
Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular cloning: a laboratory manual. Cold Spring Harbour, New York, Coldspring Harbour Laboratory Press.Google Scholar
Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. & Flook, P. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651701.CrossRefGoogle Scholar
Stern, D.L. (1995) Phylogenetic evidence that aphids, rather than plants, determine gall morphology. Proceedings of the Royal Society of London, Series B 260, 8589.Google Scholar
Stone, G.N. & Cook, J.M. (1998) The structure of cynipid oak galls patterns in the evolution of an extended phenotype. Proceedings of the Royal Society of London, Series B 265, 979988.CrossRefGoogle Scholar
Stone, G.N. & Schönrogge, K. (2003) The adaptive significance of insect gall morphology. Trends in Ecology and Evolution 18, 512522.CrossRefGoogle Scholar
Swofford, D.L. (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4. Sunderland, Massachusetts, Sinauer Associates.Google Scholar
von Dohlen, C.D., Kurosu, U. & Aoki, S. (2002) Phylogenetics and evolution of eastern Asian–eastern North American disjunct aphid tribe, Hormaphidini (Hemiptera: Aphididae). Molecular Phylogenetics and Evolution 23, 257267.CrossRefGoogle ScholarPubMed
von Dohlen, C.D., Rowe, C.A. & Heie, O.E. (2006) A test of morphological hypotheses for tribal and subtribal relationships of Aphidinae (Insecta: Hemiptera: Aphididae) using DNA sequences. Molecular Phylogenetics and Evolution 38, 316329.CrossRefGoogle ScholarPubMed
Wool, D. (1984) Gall forming aphids. pp. 1158in Ananthakrishnan, T.N. (Ed.) Biology of gall insects. New Delhi, Oxford and IBH.Google Scholar
Wool, D. (2004) Galling aphids: specialization, biological complexity, and variation. Annual Review of Entomology 49, 175192.CrossRefGoogle ScholarPubMed
Wool, D. & Burstein, M. (1991) A galling aphid with extra life cycle complexity: population ecology and evolutionary considerations. Research of Population Ecology 33, 307322.CrossRefGoogle Scholar
Zhang, G.X. & Zhong, T.S. (1983) Economic insect fauna of China. Fasc. 25: Homoptera: Aphidinea, Part I. 387 pp. Beijing, Science Press.Google Scholar
Zhang, G.X., Qiao, G.X., Zhong, T.S. & Zhang, W.Y. (1999) Fauna Sinica Insecta Vol. 14. Homoptera: Mindaridae and Pemphigidae. 356 pp. Beijing, Science Press.Google Scholar
Zhang, H.C., Qiao, G.X. & Zhang, G.X. (2006) A study on diversity of aphid's galls in Pemphigidae. Acta Zootaxonomica Sinica 31, 4854.Google Scholar
Zwölfer, H. (1957) Zur Systematik Biologie und Okologie unterirdisch lebender Aphiden (Homoptera: Aphidoidea) (Anoeciinae, Tetraneurini, Pemphigini und Fordinae). Teil. II. Tetraneurini und Pemphigine. Zeitschrift für Angewandte Entomologie 40, 528575.CrossRefGoogle Scholar