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Armored scale insect endosymbiont diversity at the species level: genealogical patterns of Uzinura diasipipdicola in the Chionaspis pinifoliae–Chionaspis heterophyllae species complex (Hemiptera: Coccoidea: Diaspididae)

Published online by Cambridge University Press:  26 November 2014

J.C. Andersen ,
R.A. Gwiazdowski ,
K. Gdanetz  and
M.E. Gruwell
J.C. Andersen
Affiliation:
Department of Environmental Science Policy and Management, University of California, Berkeley, CA 94720, USA
R.A. Gwiazdowski
Affiliation:
Biodiversity Institute of Ontario, University of Guelph, Guelph, Ontario, Canada
K. Gdanetz
Affiliation:
Department of Plant Biology, Michigan State University, East Lansing, MI 48824, USA
M.E. Gruwell*
Affiliation:
Penn State Erie, The Behrend College, School of Science, Erie, PA 16563, USA
*
*Author for correspondence Phone: 814-898-6276 Fax: 814-898-6213 E-mail: meg26@psu.edu
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Abstract

Armored scale insects and their primary bacterial endosymbionts show nearly identical patterns of co-diversification when viewed at the family level, though the persistence of these patterns at the species level has not been explored in this group. Therefore we investigated genealogical patterns of co-diversification near the species level between the primary endosymbiont Uzinura diaspidicola and its hosts in the Chionaspis pinifoliae–Chionaspis heterophyllae species complex. To do this we generated DNA sequence data from three endosymbiont loci (rspB, GroEL, and 16S) and analyzed each locus independently using statistical parsimony network analyses and as a concatenated dataset using Bayesian phylogenetic reconstructions. We found that for two endosymbiont loci, 16S and GroEL, sequences from U. diaspidicola were broadly associated with host species designations, while for rspB this pattern was less clear as C. heterophyllae (species S1) shared haplotypes with several other Chionaspis species. We then compared the topological congruence of the phylogenetic reconstructions generated from a concatenated dataset of endosymbiont loci (including all three loci, above) to that from a concatenated dataset of armored scale hosts, using published data from two nuclear loci (28S and EF1α) and one mitochondrial locus (COI–COII) from the armored scale hosts. We calculated whether the two topologies were congruent using the Shimodaira–Hasegawa test. We found no significant differences (P = 0.4892) between the topologies suggesting that, at least at this level of resolution, co-diversification of U. diaspidicola with its armored scale hosts also occurs near the species level. This is the first such study of co-speciation at the species level between U. diaspidicola and a group of armored scale insects.

Keywords

genealogical concordanceendosymbiosispine-feedingNorth AmericaTreeMap
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 105 , Issue 1 , February 2015 , pp. 110 - 120
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Copyright
Copyright © Cambridge University Press 2014 

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References

Ahmed, M.Z., De Barro, P.J., Ren, S.-X., Greeff, J.M. & Qiu, B.-L. (2013) Evidence for horizontal transmission of secondary endosymbionts in the Bemisia tabaci cryptic species complex. PLoS ONE 8, e53084.CrossRefGoogle ScholarPubMed
Andersen, J.C., Wu, J., Gruwell, M.E., Gwiazdowski, R.A., Santana, S.E., Feliciano, N.M., Morse, G.E. & Normark, B.B. (2010) A phylogenetic analysis of armored scale insects (Hemiptera: Diaspididae), based upon nuclear, mitochondrial, and endosymbiont gene sequences. Molecular Phylogenetics and Evolution 57, 992–1003.CrossRefGoogle ScholarPubMed
Andersen, J.C., Gwiazdowski, R. & Gruwell, M.E. (2014) Molecular evolution of sexual and parthenogenetic lineages of the armored scale insect Aspidiotus nerii (Hemiptera: Diaspididae) and its primary bacterial endosymbiont, Uzinura diaspidicola . Annals of the Entomological Society of America 107, 954–960.Google Scholar
Baumann, P. (2005) Biology of bacteriocyte-associated endosymbiots of plant sap-sucking insects. Annual Review of Microbiology 59, 155–189.CrossRefGoogle ScholarPubMed
Bennett, G.M. & O'Grady, P.M. (2012) Host-plants shape insect diversity: phylogeny, origin, and species diversity of native Hawaiian leafhoppers (Cicadellidae: Nesophrosyne). Molecular Phylogenetics and Evolution 65, 705–717.Google Scholar
Buchner, P. (1965) Endosymbiosis of Animals with Plant Microorganisms. New York, Interscience Publishers, Inc. Google Scholar
Clement, M., Posada, D. & Crandall, K. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1660.Google Scholar
Drummond, A., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Heled, J., Kearse, M., Moir, R., Stones-Havas, S., Sturrock, S., Thierer, T. & Wilson, A. (2012) Geneious v 5.6.2, Available online at http://www.geneious.com computer program, version By Drummond, A., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Heled, J., Kearse, M., Moir, R., Stones-Havas, S., Sturrock, S., Thierer, T., and Wilson, A. Google Scholar
Earle, C.J. (2014) The Gymnosperm Database, Available online at http://www.conifers.org/zz/gymnosperms.php.Google Scholar
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.Google Scholar
Ehrlich, P.R. & Raven, P.H. (1964) Butterflies and plants – a study in coevolution. Evolution 18, 586–608.Google Scholar
Gruwell, M.E., Morse, G.E. & Normark, B.B. (2007) Phylogenetic congruence of armored scale insects (Hemiptera: Diaspididae) and their primary endosymbionts from the phylum Bacteroidetes. Molecular Phylogenetics and Evolution 44, 267–280.CrossRefGoogle ScholarPubMed
Gruwell, M.E., Wu, J. & Normark, B.B. (2009) Diversity and phylogeny of Cardinium (Bacteroidetes) in armored scale insects (Hemiptera: Diaspididae). Annals of the Entomological Society of America 102, 1050–1061.CrossRefGoogle Scholar
Gruwell, M.E., Hardy, N.B., Gullan, P.J. & Dittmar, K. (2010) Evolutionary relationships among primary endosymbionts of the mealybug subfamily Phenacoccinae (Hemiptera: Coccoidea: Pseudococcidae). Applied and Environmental Microbiology 76, 7521–7525.Google Scholar
Gwiazdowski, R., Vea, I., Andersen, J.C. & Normark, B.B. (2011) Discovery of cryptic species among North American pine-feeding Chionaspis scale insects (Hemiptera: Diaspididae). Biological Journal of the Linnean Society 104, 47–62.Google Scholar
Huelsenbeck, J.P. (2001) MRBAYES: bayesian inference of phylogeny, Version 3.0. Bioinformatics 17, 754–755.CrossRefGoogle Scholar
Jepson Flora Project (eds). (2014) Jepson eFlora, Available online at http://ucjeps.berkeley.edu/IJM.html.Google Scholar
Kuechler, S.M., Gibbs, G., Burckhardt, D., Dettner, K. & Hartung, V. (2013) Diversity of bacterial endosymbionts and bacteria–host co-evolution in Gondwanan relict moss bugs (Hemiptera: Coleorrhyncha: Peloridiidae). Environmental Microbiology 15, 2031–2042.CrossRefGoogle ScholarPubMed
Liu, L., Huang, X., Zhang, R., Jiang, L. & Qiao, G. (2013) Phylogenetic congruence between Mollitrichosiphum (Aphididae: Greenideinae) and Buchnera indicates insect-bacteria parallel evolution. Systematic Entomology 38, 81–92.CrossRefGoogle Scholar
Lozier, J.D., Roderick, G.K. & Mills, N.J. (2007) Genetic evidence from mitochondrial, nuclear, and endosymbiont markers for the evolution of host plant associated species in the aphid genus Hyalopterus (Hemiptera : Aphididae). Evolution 61, 1353–1367.CrossRefGoogle ScholarPubMed
Maddison, D., & Maddison, W. (2005) MacClade 4 computer program, version 4.08. By Maddison, D., and Maddison, W., Sunderland, MA. Google Scholar
Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. pp. 1–8 in Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA.CrossRefGoogle Scholar
Moran, N.A. (2001) The coevolution of bacterial endosymbionts and phloem-feeding insects. Annals of the Missouri Botanical Garden 88, 35–44.CrossRefGoogle Scholar
Moran, N.A., McCutcheon, J.P. & Nakabachi, A. (2008) Genomics and evolution of heritable bacterial symbionts. Annual Review of Genetics 42, 165–190.CrossRefGoogle ScholarPubMed
Moulton, J. & Wiegmann, B. (2004) Evolution and phylogenetic utility of CAD (rudimentary) among Mesozoic-aged Eremoneuran Diptera (Insecta). Molecular Phylogenetics and Evolution 31, 363–378.CrossRefGoogle ScholarPubMed
Posada, D. & Crandall, K. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle ScholarPubMed
Rambaut, A., & Drummond, A. (2007) Tracer v1.4, Available online at http://beast.bio.ed.ac.uk/Tracer computer program, version By Rambaut, A., and Drummond, A. Google Scholar
Sabree, Z.L., Huang, C.Y., Okusu, A., Moran, N.A. & Normark, B.B. (2013) The nutrient supplying capabilities of Uzinura, an endosymbiont of armoured scale insects. Environmental Microbiology 15, 1988–1999.Google Scholar
Swofford, D.L. (2002) PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods) computer program, version 4.0b10. By Swofford, D.L., Sunderland, MA.Google Scholar
Toju, H. & Fukatsu, T. (2011) Diversity and infection prevalence of endosymbionts in natural populations of the chestnut weevil: relevance of local climate and host plants. Molecular Ecology 20, 853–868.Google Scholar
Urban, J. & Cryan, J. (2012) Two ancient bacterial endosymbionts have coevolved with the planthoppers (Insecta: Hemiptera: Fulgoroidea). BMC Evolutionary Biology 12, 87.CrossRefGoogle ScholarPubMed
Vea, I., Gwiazdowski, R. & Normark, B.B. (2012) Corroborating molecular species discovery: four new pine-feeding species of Chionaspis (Hemiptera, Diaspididae). Zookeys 270, 37–58.Google Scholar
von Dohlen, C.D., Kohler, S., Alsop, S.T. & McManus, W.R. (2001) Mealybug beta-proteobacterial endosymbionts contain gamma-proteobacterial symbionts. Nature 412, 433–436.Google Scholar
Weisburg, W.G., Barns, S.M., Pelletier, D.A. & Lane, D.J. (1991) 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology 173, 697–703.CrossRefGoogle ScholarPubMed