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Molecular phylogeny of Pemphiginae (Hemiptera: Aphididae) inferred from nuclear gene EF-1α sequences

Published online by Cambridge University Press:  16 June 2008

H.C. Zhang  and
G.X. Qiao
H.C. Zhang
Affiliation:
Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China Henan Normal University, Xinxiang 453007, China
G.X. Qiao*
Affiliation:
Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
*
*Author for correspondence Fax: +86 10 64807099 E-mail: qiaogx@ioz.ac.cn
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Abstract

Three traditional tribes of Fordini, Pemphigini and Eriosomatini comprise Pemphiginae, and there are two subtribes in Fordini and Pemphigini, respectively. Most of the species in this subfamily live heteroecious holocyclic lives with distinct primary host specificity. The three tribes of Pemphigini (except Prociphilina), Eriosomatini and Fordini use three families of plants, Salicaceae (Populus), Ulmaceae (Ulums) and Anacardiaceae (Pistacia and Rhus), as primary hosts, respectively, and form galls on them. Therefore, the Pemphigids are well known as gall makers, and their galls can be divided into true galls and pseudo-galls in type. We performed the first molecular phylogenetic study of Pemphiginae based on molecular data (EF-1α sequences). Results show that Pemphiginae is probably not a monophylum, but the monophyly of Fordini is supported robustly. The monophyly of Pemphigini is not supported, and two subtribes in it, Pemphigina and Prociphilina, are suggested to be raised to tribal level, equal with Fordini and Eriosomatini. The molecular phylogenetic analysis does not show definite relationships among the four tribes of Pemphiginae, as in the previous phylogenetic study based on morphology. It seems that the four tribes radiated at nearly the same time and then evolved independently. Based on this, we can speculate that galls originated independently four times in the four tribes, and there is no evidence to support that true galls are preceded by pseudo-galls, as in the case of thrips and willow sawflies.

Keywords

Pemphiginaemolecular phylogenyEF-1αtriberadiationgall
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 98 , Issue 5 , October 2008 , pp. 499 - 507
Copyright
Copyright © 2008 Cambridge University Press

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References

Blackman, R.L. & Eastop, V.F. (1994) Aphids on the World's Trees: An Identification and Information Guide. 904 pp. Wallingford, UK, CAB International.CrossRefGoogle Scholar
Crespi, B.J. & Worobey, M. (1998) Comparative analysis of gall morphology in Australian gall thrips: the evolution of extended phenotypes. Evolution 52, 1686–1696.CrossRefGoogle ScholarPubMed
Ghosh, A.K. (1984) The Fauna of India and the Adjacent Countries, Homoptera: Aphidoidea, Part 3, Subfamily Pemphiginae. 420 pp. Calcutta, The Technical and General Press.Google Scholar
Heie, O.E. (1980) The Aphidoidea of Fennoscandia and Denmark. I. Fauna Entomologica Scandinavica 9, 1–236.Google Scholar
Heie, O.E. (1987) Paleontology and phylogeny. pp. 367–391in Minks, A.K. & Harrewijn, P. (Eds) Aphids, their Biology, Natural Enemies and Control. Amsterdam, Elsevier Science Ltd.Google Scholar
Heie, O.E. & Peñalver, E. (1999) Palaeophylloxera nov. gen., the first fossil specimen of the family Phylloxeridae (Hemiptera, Phylloxeroidea); Lower Miocene of Spain. Geobios 32, 593–597.CrossRefGoogle Scholar
Heie, O.E. & Wegierek, P. (1998) A list of fossil aphids (Homoptera: Aphidinea). Annals of the Upper Silesian Museum (Entomology) 8–9, 159–192.Google Scholar
Hillis, D.M. & Bull, J.J. (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systmatic Biology 42, 181–192.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, 2310–2314.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, 504–511.CrossRefGoogle ScholarPubMed
Kumar, S., Tamura, K. & Nei, M. (2004) MEGA 3: integrated software for molecular evolutionary genetic analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.CrossRefGoogle Scholar
Normark, B.B. (2000) Molecular systematics and evolution of the aphid family Lachnidae. Molecular Phylogenetics and Evolution 14, 131–140.CrossRefGoogle ScholarPubMed
Ortiz-Rivas, B., Moya, A. & Martinez-Torres, D. (2004) Molecular systematics of aphids (Homoptera, Aphididae), new insights from the long-wavelength opsin gene. Molecular Phylogenetics and Evolution 30, 24–37.CrossRefGoogle ScholarPubMed
Palumbi, S.R. (1996) Nucleic acids II: the polymerase chain reaction. pp. 205–247in Hillis, D.M., Moritz, C. & Mable, B.K. (Eds) Molecular Systematics. Sunderland, MA, USA, Sinauer.Google Scholar
Posada, D. & Crandall, K.A. (1998) MODELTEST, testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle ScholarPubMed
Price, P.W. (1992) Evolution and ecology of gall-inducing sawflies. pp. 208–224in Shorthouse, J.D. & Rohfritsch, O. (Eds) Biology of Gall Insect-induced Galls. Oxford, Oxford University Press.Google Scholar
Price, P.W. & Roininen, H. (1993) Adaptive radiation in gall induction. pp. 229–257in Wagner, M.R. & Raffa, K.F (Eds) Sawfly Life History Adaptations to Woody Plants. New York, Academic Press.Google Scholar
Reeder, T.W. (2003) A phylogeny of the Australian Sphenomorphus group (Scincidae: Squamata) and the phylogenetic placement of the crocodile skinks (Tribolonotus): Bayesian approaches to assessing congruence and obtaining confidence in maximum likelihood inferred relationships. Molecular Phylogenetics and Evolution 27, 384–397.CrossRefGoogle ScholarPubMed
Remaudière, G. & Remaudière, M. (1997) Catalogue of the world's Aphididae (Homoptera Aphidoidea). 473 pp. ParisINRA.Google Scholar
Rokas, A., Nylander, J.A.A., Ronquist, F. & Stone, G.N. (2002) A maximum-likelihood analysis of eight phylogenetic markers in gallwasps (Hymenoptera: Cynipidae): implications for insect phylogenetic studies. Molecular Phylogenetics and Evolution 22, 206–219.CrossRefGoogle ScholarPubMed
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBAYES 3, Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. pp. 461–512. New York, Coldspring Harbour Laboratory Press.Google Scholar
Sanders, K.L., Malhotra, A. & Thorpe, R.S. (2006) Combining molecular, morphological and ecological data to infer species boundaries in a cryptic tropical pitviper. Biological Journal of the Linnean Society 87, 343–364.CrossRefGoogle Scholar
Stone, G.N. & Schönrogge, K. (2003) The adaptive significance of insect gall morphology. Trends in Ecology and Evolution 18, 512–522.CrossRefGoogle Scholar
Swofford, D.L. (2003) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.0b10. Sunderland, Massachusetts, Sinauer Associates.Google Scholar
Tamura, K. & Nei, M. (1993) Estimation of the number nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512–526.Google ScholarPubMed
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid Research 25, 4876–4882.CrossRefGoogle ScholarPubMed
von Dohlen, C.D. & Moran, N.A. (2000) Molecular data support a rapid radiation of aphid radiation of aphids in the Cretaceous and multiple origins of host alternation. Biological Journal of the Linnean Society 71, 689–717.CrossRefGoogle Scholar
von Dohlen, C.D. & Teulon, D.A.J. (2003) Phylogeny and historical biogeography of New Zealand indigenous Aphidini aphids (Hemiptera, Aphididae): an hypothesis. Annals of the Entomological Society of America 96, 107–116.CrossRefGoogle 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, 257–267.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, 316–329.CrossRefGoogle ScholarPubMed
Wojciechowski, W. (1992) Studies on the Systematic System of Aphids (Homoptera, Aphidinea). Katowice, Poland, Uniwersytet Slaski.Google Scholar
Wool, D. (2004) Galling aphids: specilization, biological complexity, and variation. Annual Review of Entomology 49, 175–192.CrossRefGoogle Scholar
Xia, X. & Xie, Z. (2001) DAMBE: Data analysis in molecular biology and evolution. Journal of Heredity 92, 371–373.CrossRefGoogle ScholarPubMed
Yang, M.M. & Mitter, C. (1994) Biosystematics of hackberry psyllids (Pachypsylla) and the evolution of gall and lerp formation in psyllids (Homoptera: Psylloidea): a preliminary report. pp. 172–185in Price, P.W., Mattson, W.J. & Baranchikov, Y.N. (Eds), The Ecology and Evolution of Gall-forming Insects. St. Paul, MN, USA, USDA Forest Service.Google Scholar
Zhang, G.X. & Chen, X.L. (1999) Study on the phylogeny of Pemphigidae (Homoptera: Aphidinea). Acta Entomologica Sinica 42, 176–183.Google Scholar
Zhang, H.C. & Qiao, G.X. (2006) Application of gene sequences in molecular phylogenetic study on Aphididae (Hemiptera). Acta Entomologica Sinica 49, 521–527.Google Scholar
Zhang, H.C. & Qiao, G.X. (2007a) Molecular phylogeney of Fordini (Hemiptera: Aphididae: Pemphiginae) inferred from nuclear gene EF-1α and mitochondrial gene COI. Bulletin of Entomological Research 97, 379–386.CrossRefGoogle Scholar
Zhang, H.C. & Qiao, G.X. (2007b) Systematic status of genus Formosaphis Takahashi and evolution of galls based on the molecular phylogeny of Pemphigini (Hemiptera: Aphididae: Erisomatinae). Systematic Entomology 32, 690–699.CrossRefGoogle 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, 48–54.Google Scholar
Zkharov, E.V., Caterino, M.S. & Sperling, F.A.H. (2004) Molecular phylogeny, historical biogeography, and divergence time estimates for swallowtail butterflies of the genus Papilio (Lepidoptera: Papilionidae). Systematic Biology 53, 193–215.CrossRefGoogle Scholar