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Molecular phylogenetic evidence for paraphyly of Ceratovacuna and Pseudoregma (Hemiptera, Hormaphidinae) reveals late Tertiary radiation

Published online by Cambridge University Press:  21 June 2013

Zhang Rui-ling ,
Huang Xiao-lei ,
Jiang Li-yun  and
Qiao Ge-xia
Zhang Rui-ling
Affiliation:
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China Department of Biochemistry and Molecular Biology, Liaoning Medical University, Jinzhou, 121000, Liaoning Province, China
Huang Xiao-lei
Affiliation:
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
Jiang Li-yun
Affiliation:
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
Qiao Ge-xia*
Affiliation:
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
*
*Author for correspondence Phone: +86-10-6480-7133 Fax: +86-10-6480-7098 E-mail: qiaogx@ioz.ac.cn
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Abstract

Ceratovacuna and Pseudoregma are important groups in Cerataphidini (Hemiptera, Hormaphidinae) that not only produce soldier aphids in galls on the primary hosts but also produce horned soldiers on the herbaceous secondary hosts. However, due to sampling bias in previous studies, the phylogenetic relationships of these two genera remain inconclusive. In this study, based on more extensive sampling and examination of both mitochondrial (cytochrome c oxidase subunit I (COI); cytochrome b (Cytb)) and nuclear (elongation factor-1α (EF-1α); long-wavelength opsin (LWO)) genes, we reconstructed the phylogenetic relationships of Ceratovacuna and Pseudoregma. Phylogenetic analyses, along with morphological evidence, suggested that these two genera belong to the paraphyletic groups with species clustered into three main groups. The monophyly of Ceratovacuna and Pseudoregma as a whole was generally supported by all analyses. Monophyly of Pseudoregma was also supported. The estimated divergence times demonstrated that diversification of Ceratovacuna and Pseudoregma occurred approximately at 10 mya. The relatively low resolution for the basal relationships of the three main clades may indicate that these two genera have experienced a rapid radiation along with speciation burst of their secondary hosts during the late Tertiary.

Keywords

Divergence timediversificationgeographical isolationphylogeny
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 103 , Issue 6 , December 2013 , pp. 644 - 655
Copyright
Copyright © Cambridge University Press 2013 

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References

Aoki, S. (1987) Evolution of sterile soldiers in aphids. pp. 53–65in Ito, Y., Brown, J.L. & Kikkawa, J. (Eds) Animal Societies: Theories and Facts. Tokyo, Japanese Scientific Society Press.Google Scholar
Aoki, S. & Kurosu, U. (1989) Two kinds of soldiers in the tribe Cerataphidini (Homoptera: Aphidoidea). Journal of Aphidology 3, 1–7.Google Scholar
Aoki, S. & Kurosu, U. (2010) A review of the biology of Cerataphidini (Hemiptera, Aphididae, Hormaphidinae), focusing mainly on their life cycles, gall formation, and soldiers. Psyche 1–34, doi:10.1155/2010/380351.Google Scholar
Costa, J.T. (2006) The Other Insect Societies. Cambridge, Belknap Press of Harvard University.Google Scholar
Dixon, A.F.G. (1985) Aphid Ecology. 1st edn. Glasgow, Blackie.Google Scholar
Dixon, A.F.G. (1998) Aphid Ecology: An Optimization Approach. 2nd edn. London, Chapman and Hall.Google Scholar
Doncaster, J.P. (1966) Notes on Indian aphids described by G Buckton. Entomologist 99, 157–160.Google Scholar
Drummond, A.J. & Suchard, M.A. (2010) Bayesian random local clocks or one rate to rule them all. BMC Biology 8, 114.CrossRefGoogle ScholarPubMed
Foottit, R.G., Maw, B.L., von Dohlen, C.D. & Hebert, P.D.N. (2008) Species identification of aphids (Insecta: Hemiptera: Aphididae) through DNA barcodes. Molecular Ecology Resources 8, 1189–1201.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, 613–623.Google Scholar
Fukatsu, T., Shibao, H., Nikoh, N. & Aoki, S. (2001) Genetically distinct populations in an Asian soldier-producing aphid, Pseudoregma bambucicola (Homoptera: Aphididae), identified by DNA fingerprinting and molecular phylogenetic analysis. Molecular Phylogenetics and Evolution 18, 423–433.Google Scholar
Ghosh, A.K. (1988) The fauna of India and adjacent countries. Homoptera, Aphidoidea, Part 4 inPhloeomyzinae, Anoeciinae and Hormaphidinae. Zoological Survey of India, Calcutta, 1–429.Google Scholar
Guindon, S. & Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.Google Scholar
Harry, M., Solignac, M. & Lachaise, D. (1998) Molecular evidence for parallel evolution of adaptive syndromes in fig-breeding Lissocephala (Drosophilidae). Molecular Phylogenetics and Evolution 9, 3542–551.Google Scholar
Heie, O.E. (1996) The evolutionary history of aphids and a hypothesis on the coevolution of aphids and plants. Bollettino di Zoologia Agraria e di Bachicoltura Ser. II 28, 149–155.Google Scholar
Huang, X.L., Xiangyu, J.G., Ren, S.S., Zhang, R.L., Zhang, Y.P. & Qiao, G.X. (2012) Molecular phylogeny and divergence times of Hormaphidinae (Hemiptera: Aphididae) indicate late Cretaceous tribal diversification. Zoological Journal of the Linnean Society 165, 73–87.Google Scholar
Ortiz-Rivas, B., Moya, A. & Martínez-Torres, D. (2010) Combination of molecular data support the existence of three main lineages in the phylogeny of aphids (Hemiptera: Aphididae) and the basal position of the subfamily Lachninae. Molecular Phylogenetics and Evolution 55, 305–317.Google Scholar
Palumbi, S.R. (1996) Nucleic acids II: the polymerase chain reaction. pp. 205–247in Hillis, D.M., Moritz, C. & Mable, B.K. (Ed.) Molecular Systematics. Sunderland, Sinauer.Google Scholar
Posada, D. & Buckley, T.R. (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology 53, 793–808.CrossRefGoogle ScholarPubMed
Posada, D. & Crandall, K.A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle ScholarPubMed
Rambaut, A. (2009) FigTree, v1.2.2. Available online at http://tree.bio.ed.ac.uk/software/figtree (accessed 21 December 2009).Google Scholar
Rambaut, A. & Drummond, A.J. (2008) Tracer, v1.4.1. Available online at http://tree.bio.ed.ac.uk/software/tracer (accessed 30 November 2009).Google Scholar
Ronquist, F. & Huelsenbeck, J.P. (2005) Bayesian analysis of molecular evolution using MrBayes. pp. 183–232in Nielsen, R. (Ed.) Statistical Methods in Molecular Evolution. New York, Springer.Google Scholar
Stern, D.L. (1994) A phylogenetic analysis of soldier evolution in the aphid family Hormaphididae. Proceedings of the Royal Society B 256, 203–209.Google ScholarPubMed
Stern, D.L. (1995) Phylogenetic evidence that aphids, rather than plants, determine gall morphology. Proceedings of the Royal Society B 260, 85–89.Google Scholar
Stern, D.L. (1998) Phylogeny of the Cerataphidini (Homoptera) and the evolution of the horned soldier aphids. Evolution 52, 155–165.Google Scholar
Stern, D.L., Aoki, S. & Kurosu, U. (1997 a) Determining aphid taxonomic affinities and life cycle with molecular data: a case study of the tribe Cerataphidini (Hormaphididae: Aphidoidea: Hemiptera). Systematic Entomology 22, 81–96.Google Scholar
Stern, D.L., Whitfield, J.A. & Foster, W.A. (1997 b) Behavior and morphology of monomorphic soldiers from the aphid genus Pseudoregma (Cerataphidini, Hormaphididae) implications for the evolution of morphological castes in social aphids. Insectes Sociaux 44, 379–392.Google Scholar
Swofford, D.L. (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods). 4.0th edn. Sunderland, Sinauer Associates.Google Scholar
Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007) MEGA 4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.CrossRefGoogle 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 Acids Research 25, 4876–4882.Google Scholar
Vavre, F., Girin, C. & Boulétreau, M. (1999) Phylogenetic status of a fecundity enhancing Wolbachia that does not induce thelytoky in Trichogramma. Insect Molecular Biology 8, 67–72.Google Scholar
von Dohlen, C.D. & Moran, N.A. (2000) Molecular data support a rapid radiation of aphids in the Cretaceous and multiple origins of host alternation. Biological Journal of the Linnean Society 71, 689–717.Google Scholar
von Dohlen, C.D., Kurosu, U. & Aoki, S. (2002) Phylogenetics and evolution of the eastern Asian–eastern North American disjunct aphid tribe, Hormaphidini (Hemiptera: Aphididae). Molecular Phylogenetics and Evolution 23, 257–267.Google Scholar
Wegierek, P. & ŻYŁA, D. (2011) New Hormaphididae (Hemiptera, Aphidomorpha) from the Baltic amber and its palaeogeographic significance. Acta Geologica Sinica 85, 521–527.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, R.Z. (1999) Zoogeography of China. Beijing, Science Press.Google Scholar
Zehntner, L. (1897) Overzicht van de ziekten van het suikerriet op Java. 2e deel.-Med. Proefst, Oost-Java Nierwe serie, 37. pp. 27–32.Google Scholar
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