Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-27T23:01:02.379Z Has data issue: false hasContentIssue false
  • English
  • Français

Development of microsatellite markers for an outbreaking species of oak gall wasp, Zapatella davisae (Hymenoptera: Cynipidae), in the northeastern United States

Published online by Cambridge University Press:  29 November 2018

J.C. Andersen Open the ORCID record for J.C. Andersen [Opens in a new window] ,
C.P. Camp ,
M.J. Davis ,
N.P. Havill  and
J.S. Elkinton
J.C. Andersen*
Affiliation:
Department of Environmental Conservation, University of Amherst Massachusetts, 160 Holdsworth Way, Amherst, MA 01003, USA
C.P. Camp
Affiliation:
Department of Environmental Conservation, University of Amherst Massachusetts, 160 Holdsworth Way, Amherst, MA 01003, USA
M.J. Davis
Affiliation:
Department of Environmental Conservation, University of Amherst Massachusetts, 160 Holdsworth Way, Amherst, MA 01003, USA
N.P. Havill
Affiliation:
United States Department of Agriculture Forest Service Northern Research Station, Hamden, CT 06514, USA
J.S. Elkinton
Affiliation:
Department of Environmental Conservation, University of Amherst Massachusetts, 160 Holdsworth Way, Amherst, MA 01003, USA
*
*Author for correspondence Phone: 413-545-2665 Fax: 413-545-4358 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Populations of the recently described black oak gall wasp, Zapatella davisae Buffington (Hymenoptera: Cynipidae), have been identified as the cause of extensive tree damage and mortality to black oaks, Quercus velutina Lamarck (Fagales: Fagaceae), in the northeastern United States. Relatively little is known, however, about the distribution, phylogenetic placement, and lifecycle of this important tree pest. Therefore, we conducted next-generation sequencing using the Ion Torrent™ PGM (ThermoFisher Scientific, Inc.) platform to develop genomic resources for the study of Z. davisae and for other closely related species of oak gall wasps. Individual sequence reads were aligned, assembled into unique contigs, and the contigs were then utilized for the in silico isolation and development of microsatellite markers. In total, we screened 36 candidate microsatellite loci, of which 23 amplified consistently (five polymorphic and 18 monomorphic). We then examined whether the polymorphic loci could be used to infer whether populations of Z. davisae from Cape Cod and Nantucket are sexual or asexual by calculating several metrics of genetic diversity that might indicate the mode of reproduction. These included testing for statistical deviations from Hardy–Weinberg equilibrium (HWE) and for linkage disequilibrium (LD), observations for the presence of the Meselson effect, and by calculating the probability that clonal individuals are more prevalent than would be expected in a randomly mating population. While we found significant deviations from HWE and more clonal individuals than expected, our estimates of the Meselson effect were inconclusive due to limited sampling, and we found no evidence of LD. Therefore, the sexual/asexual status of Z. davisae populations remains uncertain.

Keywords

next-generation sequencingion torrentpopulation geneticsreproductive modeparthenogenesis
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 109 , Issue 4 , August 2019 , pp. 510 - 517
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

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.)

Footnotes

†

Present address: Biomedical Engineering Graduate Interdisciplinary Program, University of Arizona, 1127 E. James E. Rogers Way, Tucson, AZ 85721, USA.

References

Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.Google Scholar
Andersen, J.C. & Mills, N.J. (2014) iMSAT: a novel approach to the development of microsatellite loci using barcoded Illumina libraries. BMC Genomics 15, 1–9.Google Scholar
Askew, R.R., Melika, G., Pujade-Villar, J., Schonrogge, K., Stone, G.N. & Nieves-Aldrey, J.L. (2013) Catalogue of parasitoids and inquilines in cynipid oak galls in the West Palaearctic. Zootaxa 3643, 1–133.Google Scholar
Atkinson, R.J., McVean, G.A.T. & Stone, G.N. (2002) Use of population genetic data to infer oviposition behaviour: species-specific patterns in four oak gallwasps (Hymenoptera: Cynipidae). Proceedings of the Royal Society B-Biological Sciences 269, 383–390.Google Scholar
Bassett, H.F.B. (1900) Callirhytis ceropteroides, Connecticut. Transactions of the American Entomological Society 26, 334.Google Scholar
Benson, D.A., Cavanaugh, M., Clark, K., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J. & Sayers, E.W. (2013) Genbank. Nucleic Acids Research 41, D36–D42.Google Scholar
Bhargava, A. & Fuentes, F.F. (2010) Mutational dynamics of microsatellites. Molecular Biotechnology 44, 250–266.Google Scholar
Birky, C.W. Jr (1996) Heterozygosity, heteromorphy, and phylogenetic trees in asexual eukaryotes. Genetics 144, 427–437.Google Scholar
Buffington, M.L. & Morita, S.I. (2009) Not all oak gall wasps gall oaks: the description of Dryocosmus rileypokei, a new, apostate species of Cynipini from California. Proceedings of the Entomological Society of Washington 111, 244–253.Google Scholar
Buffington, M.L., Melika, G., Davis, M. & Elkinton, J.S. (2016) The description of Zapatella davisae, new species, (Hymenoptera: Cynipidae) a pest gall wasp of black oak (Quercus velutina) in New England, USA. Proceedings of the Entomological Society of Washington 118, 14–26.Google Scholar
Cook, J.M., Rokas, A., Pagel, M. & Stone, G.N. (2002) Evolutionary shifts between host oak sections and host-plant organs in Andricus gallwasps. Evolution 56, 1821–1830.Google Scholar
Cooper, W.R. & Rieske, L.K. (2007) Community associates of an exotic gallmaker, Dryocosmus kuriphilus (Hymenoptera: Cynipidae), in Eastern North America. Annals of the Entomological Society of America 100, 236–244.Google Scholar
Corral, J.M., Piwczynski, M. & Sharbel, T.F. (2009) Allelic sequence divergence in the apomictic Boechera holboellii complex. pp 495–516 in Schön, I., Martens, K. & Dijk, P. (Eds) Lost Sex. Dordrecht, Springer.Google Scholar
Davis, M.J. (2017) Biology, molecular systematics, population dynamics and control of a stem gall wasp, Zapatella davisae (Hymenoptera: Cynipidae). PhD. Dissertation, University of Massachusetts, Amherst.Google Scholar
Davis, M.J. & Elkinton, J.S. (2018) Efficacy of two systemic insecticides with stem gall wasp, Zapatella davisae (Hymenoptera: Cynipidae) on Black Oak. Journal of Economic Entomology 111, 986–988 (doi: https://doi.org/10.1093/jee/tox358).Google Scholar
Drown, D.M. & Brown, J.M. (1998) Molecular phylogeny of North American oak-galling cynipini (Hymenoptera: Cynipidae) supports need for generic revision. Biology of Gall-Inducing Arthropods 199, 241–246.Google Scholar
Eliason, E.A. & Potter, D.A. (2000) Impact of whole-canopy and systemic insecticidal treatments on Callirhytis cornigera (Hymenoptera: Cynipidae) and associated parasitoids on pin oak. Journal of Economic Entomology 93, 165–171.Google Scholar
Ellegren, H. (2004) Microsatellites: simple sequences with complex evolution. Nature Reviews Genetics 5, 435–445.Google Scholar
Faircloth, B.C. (2008) MSATCOMMANDER: detection of microsatellite repeat arrays and automated, locus-specific primer design. Molecular Ecology Resources 8, 92–94.Google Scholar
Hardy, G. H. (1908). Mendelian proportions in a mixed oopulation. Science 28, 49–50.Google Scholar
Ide, T., Wachi, N. & Abe, Y. (2012) Three new species and a new record of Cycloneuroterus (hymenoptera: Cynipidae: Cynipini) inducing galls on Cyclobalanopsis in Japan. Annals of the Entomological Society of America 105, 539–549.Google Scholar
Jurka, J. (2000) Repbase update: a database and an electronic journal of repetitive elements. Trends in Genetics 9, 418–420.Google Scholar
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Mentjies, P. & Drummond, A. (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics (Oxford, England) 28, 1647–1649.Google Scholar
Lewontin, R.C. & Kojima, K. (1960) The evolutionary dynamics of complex polymorphisms. Evolution 14, 458–472.Google Scholar
Liljeblad, J. & Ronquist, F. (1998) A phylogenetic analysis of higher-level gall wasp relationships (Hymenoptera: Cynipidae). Systematic Entomology 23, 229–252.Google Scholar
Luo, R.B., Liu, B.H., Xie, Y.L., Li, Z.Y., Huang, W.H., Yuan, J.Y., He, G.Z., Chen, Y.X., Pan, Q., Liu, Y.J., Tang, J.B., Wu, G.X., Zhang, H., Shi, Y.J., Liu, Y., Yu, C., Wang, B., Lu, Y., Han, C.L., Cheung, D.W., Yiu, S.M., Peng, S.L., Zhu, X.Q., Liu, G.M., Liao, X.K., Li, Y.R., Yang, H.M., Wang, J. & Lam, T.W. (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1, 18.Google Scholar
MacDonald, C., Brookes, C.P., Edwards, K.J., Baker, A., Lockton, S. & Loxdale, H.D. (2003) Microsatellite isolation and characterization in the beneficial parasitoid wasp Diaeretiella rapae (M'Intosh) (Hymenoptera: Braconidae: Aphidiinae). Molecular Ecology Notes 3, 601–603.Google Scholar
Mayer, C. (2010) Phobos v. 3.3.11. Available online at http://www.rub.de/spezzoo/cm/cm_phobos.htm.Google Scholar
Medianero, E., Nieves-Aldrey, J.L. & Melika, G. (2011) Two new Neotropical species of oak gall wasps of the genus Loxaulus mayr (Hymenoptera: Cynipidae: Cynipini) from Panama. Zootaxa 2811, 37–46.Google Scholar
Meglecz, E., Costedoat, C., Dubut, V., Gilles, A., Malausa, T., Pech, N. & Martin, J.F. (2010) QDD: a user-friendly program to select microsatellite markers and design primers from large sequencing projects. Bioinformatics (Oxford, England) 26, 403–404.Google Scholar
Meglecz, E., Pech, N., Gilles, A., Dubut, V., Hingamp, P., Trilles, A., Grenier, R. & Martin, J.F. (2014) QDD version 3.1: a user-friendly computer program for microsatellite selection and primer design revisited: experimental validation of variables determining genotyping success rate. Molecular Ecology Resources 14, 1302–1313.Google Scholar
Meirmans, P.G. & Van Tienderen, P.H. (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Molecular Ecology Notes 4, 792–794.Google Scholar
Melika, G. & Abrahamson, W.G. (2007) Review of the Nearctic gallwasp species of the genus Bassettia ashmead, 1887, with description of new species (Hymenoptera: Cynipidae: Cynipini). Acta Zoologica Academiae Scientiarum Hungaricae 53, 131–148.Google Scholar
Melika, G. & Buss, E.A. (2002) Description of the sexual generation of Callirhytis quercuscornigera and a new inquiline (Hymenoptera: Cynipidae). Florida Entomologist 85, 625–631.Google Scholar
Melika, G., Tang, C.T., Sinclair, F., Yang, M.M., Lohse, K., Hearn, J., Nicholls, J.A. & Stone, G.N. (2013) A new genus of oak gallwasp, Cyclocynips melika, Tang & Sinclair (Hymenoptera: Cynipidae: Cynipini), with descriptions of two new species from Taiwan. Zootaxa 3630, 534–548.Google Scholar
Moriya, S., Inoue, K., Otake, A., Shiga, M. & Mabuchi, M. (1989) Decline of the chestnut gall wasp population, Dryocosmus-kuriphilus Yasumatsu (Hymenoptera, Cynipidae) after the establishment of Torymus-sinensis Kamijo (Hymenoptera, Torymidae). Applied Entomology and Zoology 24, 231–233.Google Scholar
Neiman, M. & Lively, C.M. (2005) Male New Zealand mud snails (Potamopyrgus antipodarum) persist in copulating with asexual and parasitically castrated females. American Midland Naturalist 154, 88–96.Google Scholar
Pike, C.C., Robison, D.J. & Abrahamson, L.P. (2006) Cynipid gall wasps in declining black oak in New York: relationships with prior tree history and crown dieback. pp 123–132 in Ozaki, K., Yukawa, J., Ohgushi, T., & Price, P.W. (Eds) Galling Arthropods and Their Associates. Tokyo, Springer.Google Scholar
Primmer, C.R., Moller, A.P. & Ellegren, H. (1996) A wide-range survey of cross-species microsatellite amplification in birds. Molecular Ecology 5, 365–378.Google Scholar
Pujade-Villar, J., Romero-Rangel, S., Chagoyan-Garcia, C., Equihua-Martinez, A., Estrada-Venegas, E.G. & Melika, G. (2010) A new genus of oak gallwasps, Kinseyella Pujade-Villar & Melika, with a description of a new species from Mexico (Hymenoptera: Cynipidae: Cynipini). Zootaxa 2335, 16–28.Google Scholar
Pujade-Villar, J., Hanson, P., Medina, C.A., Torres, M. & Melika, G. (2012) A new genus of oak gallwasps, Zapatella Pujade-Villar & Melika, gen. n., with a description of two new species from the Neotropics (Hymenoptera, Cynipidae, Cynipini). Zookeys 210, 75–104.Google Scholar
Pujade-Villar, J., Cibrian-Tovar, D., Barrera-Ruiz, U.M. & Melika, G. (2014) Andricus breviramuli Pujade-Villar n. sp. (Hymenoptera: Cynipidae: Cynipini): new pest of oaks in Mexico. Southwestern Entomologist 39, 97–106.Google Scholar
Raymond, M. & Rousset, F. (1995) GENEPOP (VERSION-1.2) – Population-genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248–249.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.Google Scholar
Rokas, A., Melika, G., Abe, Y., Nieves-Aldrey, J.L., Cook, J.M. & Stone, G.N. (2003) Lifecycle closure, lineage sorting, and hybridization revealed in a phylogenetic analysis of European oak gallwasps (Hymenoptera: Cynipidae: Cynipini) using mitochondrial sequence data. Molecular Phylogenetics and Evolution 26, 36–45.Google Scholar
Ronquist, F. & Liljeblad, J. (2001) Evolution of the gall wasp-host plant association. Evolution 55, 2503–2522.Google Scholar
Ronquist, F., Nieves-Aldrey, J.L., Buffington, M.L., Liu, Z.W., Liljeblad, J. & Nylander, J.A.A. (2015) Phylogeny, evolution and classification of gall wasps: the plot thickens. PLoS One 10, e0123301.Google Scholar
Rousset, F. (2008) GENEPOP'007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources 8, 103–106.Google Scholar
Schaefer, I., Domes, K., Heethoff, M., Schneider, K., Schön, I., Norton, R. A., Scheu, S. & Maraun, M. (2006) No evidence for the ‘Meselson effect’ in parthenogenetic oribatid mites (Oribatida, Acari). Journal of Evolutionary Biology 19, 184–193.Google Scholar
Schuelke, M. (2000) An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology 18, 233–234.Google Scholar
Schurko, A.M., Neiman, M. & Logsdon, J.M. (2009) Signs of sex: what we know and how we know it. Trends in Ecology & Evolution 24, 208–217.Google Scholar
Scribner, K. & Pearce, J. (2000) Microsatellites: evolutionary and methodological background and empirical applications at individual, population, and phylogenetic levels. pp. 235–271 in Baker, A. (Ed.) Molecular Methods in Ecology. London, England, Blackwell Science Limited.Google Scholar
Selkoe, K.A. & Toonen, R.J. (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecology Letters 9, 615–629.Google Scholar
Slatkin, M. (2008) Linkage disequilibrium – understanding the evolutionary past and mapping the medical future. Nature Reviews Genetics 9, 477–485.Google Scholar
Stone, G.N., Schonrogge, K., Atkinson, R.J., Bellido, D. & Pujade-Villar, J. (2002) The population biology of oak gall wasps (Hymenoptera: Cynipidae). Annual Review of Entomology 47, 633–668.Google Scholar
Stone, G.N., Atkinson, R.J., Rokas, A., Nieves-Aldrey, J.L., Melika, G., Acs, Z., Csoka, G., Hayward, A., Bailey, R., Buckee, C. & McVean, G.A.T. (2008) Evidence for widespread cryptic sexual generations in apparently purely asexual Andricus gallwasps. Molecular Ecology 17, 652–665.Google Scholar
Tang, C.T., Sinclair, F., Hearn, J., Yang, M.M., Stone, G.N., Nicholls, J.A., Schweger, S. & Melika, G. (2016) Eight new species of Cycloneuroterus melika & Tang gallwasps from Taiwan and mainland China (Hymenoptera: Cynipidae: Cynipini). Zootaxa 4088, 451–488.Google Scholar
Washburn, J.O. & Cornell, H.V. (1981) Parasitoids, patches, and phenology – their possible role in the local extinction of a Cynipid gall wasp population. Ecology 62, 1597–1607.Google Scholar
Supplementary material: File

Andersen et al. supplementary material

Andersen et al. supplementary material 1

Download Andersen et al. supplementary material(File)
File 246.9 KB