Skip to main content Accessibility help
×
Home
Hostname: page-component-6c8bd87754-5dxdz Total loading time: 0.252 Render date: 2022-01-19T11:49:38.099Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": true, "newCiteModal": false, "newCitedByModal": true, "newEcommerce": true, "newUsageEvents": true }

Asymmetric hybridization between non-native winter moth, Operophtera brumata (Lepidoptera: Geometridae), and native Bruce spanworm, Operophtera bruceata, in the Northeastern United States, assessed with novel microsatellites and SNPs

Published online by Cambridge University Press:  23 November 2016

N.P. Havill*
Affiliation:
USDA Forest Service, Northern Research Station, Hamden, Connecticut, USA
J. Elkinton
Affiliation:
Department of Environmental Conservation, University of Massachusetts, Amherst, Massachusetts, USA
J.C. Andersen
Affiliation:
Department of Environmental Conservation, University of Massachusetts, Amherst, Massachusetts, USA
S.B. Hagen
Affiliation:
NIBIO, Norwegian Institute for Bioeconomy Research, Svanvik, Norway
Hannah J. Broadley
Affiliation:
University of Massachusetts Amherst, Organismic and Evolutionary Biology, Amherst, Massachusetts, USA
G.J. Boettner
Affiliation:
Department of Environmental Conservation, University of Massachusetts, Amherst, Massachusetts, USA
A. Caccone
Affiliation:
Department of Ecology & Evolutionary Biology, Yale University, New Haven, Connecticut, USA
*
*Author for correspondence Phone: 203-230-4320 Fax: 203-230-4315 E-mail: nphavill@fs.fed.us

Abstract

The European winter moth, Operophtera brumata, is a non-native pest in the Northeastern USA causing defoliation of forest trees and crops such as apples and blueberries. This species is known to hybridize with O. bruceata, the Bruce spanworm, a native species across North America, although it is not known if there are hybrid generations beyond F1. To study winter moth population genetics and hybridization with Bruce spanworm, we developed two sets of genetic markers, single nucleotide polymorphisms (SNPs) and microsatellites, using genomic approaches. Both types of markers were validated using samples from the two species and their hybrids. We identified 1216 SNPs and 24 variable microsatellite loci. From them we developed a subset of 95 species-diagnostic SNPs and ten microsatellite loci that could be used for hybrid identification. We further validated the ten microsatellite loci by screening field collected samples of both species and putative hybrids. In addition to confirming the presence of F1 hybrids reported in previous studies, we found evidence for multi-generation asymmetric hybridization, as suggested by the occurrence of hybrid backcrosses with the winter month, but not with the Bruce spanworm. Laboratory crosses between winter moth females and Bruce spanworm males resulted in a higher proportion of viable eggs than the reciprocal cross, supporting this pattern. We discuss the possible roles of population demographics, sex chromosome genetic incompatibility, and bacterial symbionts as causes of this asymmetrical hybridization and the utility of the developed markers for future studies.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2016 

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

Anderson, E.C. & Thompson, E.A. (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160, 12171229.Google ScholarPubMed
Baird, N.A., Etter, P.D., Atwood, T.S., Currey, M.C., Shiver, A.L., Lewis, Z.A., Selker, E.U., Cresko, W.A. & Johnson, E.A. (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3, e3376.CrossRefGoogle ScholarPubMed
Benjamini, Y. & Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B, Methodological 5, 289300.Google Scholar
Brownstein, M.J., Carpten, J.D. & Smith, J.R. (1996) Modulation of non-templated nucleotide addition by tag DNA polymerase: primer modifications that facilitate genotyping. Biotechniques 20, 10041010.CrossRefGoogle Scholar
Catchen, J., Hohenlohe, P.A., Bassham, S., Amores, A. & Cresko, W.A. (2013) Stacks: an analysis tool set for population genomics. Molecular Ecology 22, 31243140.CrossRefGoogle ScholarPubMed
Cuming, F.G. (1961) The distribution, life history, and economic importance of the winter moth, Operophtera brumata (L.) (Lepidoptera, Geometridae), in Nova Scotia. Canadian Entomologist 93, 135142.CrossRefGoogle Scholar
Derks, M.F.L., Smit, S., Salis, L., Schijlen, E., Bossers, A., Mateman, C., Pijl, A.S., de Ridder, D., Groenen, M.A.M., Visser, M.E. & Megens, H.J. (2015) The genome of winter moth (Operophtera brumata) provides a genomic perspective on sexual dimorphism and phenology. Genome Biology and Evolution 7, 23212332.CrossRefGoogle ScholarPubMed
du Merle, P. & Brunet, S. (1991) From green to yellow or yellowish white: egg-color changes in relation to oviposition rank in the fir budworm Choristoneura murinana (Hb) (Lep., Tortricidae). Journal of Applied Entomology 111, 342348.CrossRefGoogle Scholar
Eidt, D.C., Embree, D.G. & Smith, C.C. (1966) Distinguishing adults of winter moth Operophtera brumata (L.) and Bruce spanworm O. bruceata (Hulst) (Lepidoptera: Geometridae). Canadian Entomologist 98, 258261.CrossRefGoogle Scholar
Elkinton, J., Boettner, G., Liebhold, A. & Gwiazdowski, R. (2015) Biology, Spread, and Biological Control of the Winter Moth in the Eastern United States. Morgantown, WV, USDA Forest Service, Forest Health Technology Enterprise Team.Google Scholar
Elkinton, J.S., Boettner, G.H., Sremac, M., Gwiazdowski, R., Hunkins, R.R., Callahan, J., Scheufele, S.B., Donahue, C.P., Porter, A.H., Khrimian, A., Whited, B.M. & Campbell, N.K. (2010) Survey for winter moth (Lepidoptera: Geometridae) in northeastern North America with pheromone-baited traps and hybridization with the native Bruce spanworm (Lepidoptera: Geometridae). Annals of the Entomological Society of America 103, 135145.CrossRefGoogle Scholar
Elkinton, J.S., Liebhold, A., Boettner, G.H. & Sremac, M. (2014) Invasion spread of Operophtera brumata in northeastern United States and hybridization with O. bruceata . Biological Invasions 16, 22632272.CrossRefGoogle Scholar
Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 4750.Google Scholar
Gwiazdowski, R.A., Elkinton, J.S., deWaard, J.R. & Sremac, M. (2013) Phylogeographic diversity of the winter moths (Lepidoptera: Geometridae: Operophtera) O. brumata, and O. bruceata in Europe and North America. Annals of the Entomological Society of America 106, 143151.CrossRefGoogle Scholar
Harrison, R.G. & Larson, E.L. (2014) Hybridization, introgression, and the nature of species boundaries. Journal of Heredity 105, 795809.CrossRefGoogle ScholarPubMed
Hebert, P.D.N., Penton, E.H., Burns, J.M., Janzen, D.H. & Hallwachs, W. (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator . Proceedings of the National Academy of Sciences of the United States of America 101, 1481214817.CrossRefGoogle ScholarPubMed
Jiggins, C.D., Linares, M., Naisbit, R.E., Salazar, C., Yang, Z.H. & Mallet, J. (2001) Sex-linked hybrid sterility in a butterfly. Evolution 55, 16311638.CrossRefGoogle Scholar
Jurka, J. (2000) Repbase Update: a database and an electronic journal of repetitive elements. Trends in Genetics 9, 418420.CrossRefGoogle 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 28, 16471649.CrossRefGoogle ScholarPubMed
Kimberling, D.N., Miller, J.C. & Penrose, R.L. (1986) Distribution and parasitism of winter moth, Operophtera brumata (Lepidoptera, Geometridae), in western Oregon. Environmental Entomology 15, 10421046.CrossRefGoogle Scholar
Li, H. & Durbin, R. (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 17541760.CrossRefGoogle ScholarPubMed
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, 13021313.CrossRefGoogle ScholarPubMed
Nielsen, E.E., Bach, L.A. & Kotlicki, P. (2006) HYBRIDLAB (version 1.0): a program for generating simulated hybrids from population samples. Molecular Ecology Notes 6, 971973.CrossRefGoogle Scholar
Peterson, A. (1962) Some eggs of insects that change color during incubation. The Florida Entomologist 45, 8187.CrossRefGoogle Scholar
Pivnick, K.A., Barton, D.L. Millar, J.G. & Underhill, E.W. (1988) Improved pheromone trap exclusion of the Bruce spanworm Operophtera bruceata (Hulst) (Lepidoptera: Geometridae) when monitoring winter moth Operophtera brumata (L.) populations. Canadian Entomologist 120, 389396.CrossRefGoogle Scholar
Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945959.Google ScholarPubMed
Raj, A., Stephens, M. & Pritchard, J.K. (2014) fastSTRUCTURE: variational inference of population structure in large SNP data sets. Genetics 197, 573589.CrossRefGoogle ScholarPubMed
Roelofs, W.L., Hill, A.S., Linn, C.E., Meinwald, J., Jain, S.C., Herbert, H.J. & Smith, R.F. (1982) Sex pheromone of the winter moth, a geometrid with unusually low-temperature pre-copulatory responses. Science 217, 657659.CrossRefGoogle Scholar
Roland, J. & Embree, D.G. (1995) Biological control of the winter moth. Annual Review of Entomology 40, 475492.CrossRefGoogle Scholar
Rose, A.H. & Lindquist, O.H. (1982) Insects of Eastern Hardwood Trees. Canadian Forest Service Publication, Forestry Technical Report 29. Ottawa, Natural Resources Canada.Google Scholar
RStudio Team (2015) RStudio: Integrated Development for R. Boston, MA, RStudio, Inc. Available online at http://www.rstudio.com/.Google Scholar
Schuelke, M. (2000) An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology 18, 233234.CrossRefGoogle ScholarPubMed
Simmons, M.J., Lee, T.D., Ducey, M.J. & Dodds, K.J. (2014) Invasion of winter moth in New England: effects of defoliation and site quality on tree mortality. Forests 5, 24402463.CrossRefGoogle Scholar
Tenow, O., Nilssen, A.C., Bylund, H., Pettersson, R., Battisti, A., Bohn, U., Caroulle, F., Ciornei, C., Cs Ka, G., Delb, H., De Prins, W., Glavendekic, M., Gninenko, Y.I., Hrasovec, B., Matosevic, D., Meshkova, V., Moraal, L., Netoiu, C., Pajares, J., Rubtsov, V., Tomescu, R., Utkina, I. & Gurney, W. (2013) Geometrid outbreak waves travel across Europe. Journal of Animal Ecology 82, 8495.CrossRefGoogle ScholarPubMed
Troubridge, J.T. & Fitzpatrick, S.M. (1993) A revision of the North American Operophtera (Lepidoptera, Geometridae). Canadian Entomologist 125, 379397.CrossRefGoogle Scholar
Underhill, E.W., Millar, J.G., Ring, R.A., Wong, J.W., Barton, D. & Giblin, M. (1987) Use of a sex attractant and an inhibitor for monitoring winter moth and Bruce spanworm populations. Journal of Chemical Ecology 13, 13191330.CrossRefGoogle ScholarPubMed
Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B.C., Remm, M. & Rozen, S.G. (2012) Primer3-new capabilities and interfaces. Nucleic Acids Research 40, e115.CrossRefGoogle ScholarPubMed
van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M. & Shipley, P. (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535538.CrossRefGoogle Scholar
Werren, J.H., Baldo, L. & Clark, M.E. (2008) Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology 6, 741751.CrossRefGoogle ScholarPubMed
Zhang, D.X. (2004) Lepidopteran microsatellite DNA: redundant but promising. Trends in Ecology & Evolution 19, 507509.CrossRefGoogle ScholarPubMed
Supplementary material: File

Havill supplementary material

Supplementary Tables

Download Havill supplementary material(File)
File 53 KB
14
Cited by

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Asymmetric hybridization between non-native winter moth, Operophtera brumata (Lepidoptera: Geometridae), and native Bruce spanworm, Operophtera bruceata, in the Northeastern United States, assessed with novel microsatellites and SNPs
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Asymmetric hybridization between non-native winter moth, Operophtera brumata (Lepidoptera: Geometridae), and native Bruce spanworm, Operophtera bruceata, in the Northeastern United States, assessed with novel microsatellites and SNPs
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Asymmetric hybridization between non-native winter moth, Operophtera brumata (Lepidoptera: Geometridae), and native Bruce spanworm, Operophtera bruceata, in the Northeastern United States, assessed with novel microsatellites and SNPs
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *