Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2016-03-03
Page range: 301–344
Abstract views: 79
PDF downloaded: 53

Species discovery and diversity in Lobocriconema (Criconematidae: Nematoda) and related plant-parasitic nematodes from North American ecoregions

Department of Plant Pathology, University of Nebraska-Lincoln, Lincoln, NE 68583-0722, USA.
Entomology & Plant Pathology, University of Tennessee, 2505 E.J. Chapman Drive, 370 Plant Biotechnology, Knoxville, TN, USA, 37996-4560.
Department of Plant Pathology, University of Nebraska-Lincoln, Lincoln, NE 68583-0722, USA.
Department of Plant Pathology, University of Nebraska-Lincoln, Lincoln, NE 68583-0722, USA
Department of Plant Pathology, University of Nebraska-Lincoln, Lincoln, NE 68583-0722, USA.
Department of Statistics, University of Nebraska-Lincoln, Lincoln, NE 68583-0963
Department of Plant Pathology, University of Nebraska-Lincoln, Lincoln, NE 68583-0722, USA.
Department of Plant Pathology, University of Nebraska-Lincoln, Lincoln, NE 68583-0722, USA.
Department of Plant Pathology, University of Nebraska-Lincoln, Lincoln, NE 68583-0722, USA.
Department of Plant Pathology, University of Nebraska-Lincoln, Lincoln, NE 68583-0722, USA.
Department of Plant Pathology, University of Nebraska-Lincoln, Lincoln, NE 68583-0722, USA.
Nematoda Plant-parasitic nematodes biogeography glacial refugia phylogeography distribution COI haplotypes DNA barcoding species delimitation

Abstract

There are many nematode species that, following formal description, are seldom mentioned again in the scientific literature. Lobocriconema thornei and L. incrassatum are two such species, described from North American forests, respectively 37 and 49 years ago. In the course of a 3-year nematode biodiversity survey of North American ecoregions, specimens resembling Lobocriconema species appeared in soil samples from both grassland and forested sites. Using a combination of molecular and morphological analyses, together with a set of species delimitation approaches, we have expanded the known range of these species, added to the species descriptions, and discovered a related group of species that form a monophyletic group with the two described species. In this study, 148 specimens potentially belonging to the genus Lobocriconema were isolated from soil, individually measured, digitally imaged, and DNA barcoded using a 721 bp region of cytochrome oxidase subunit 1 (COI). One-third of the specimens were also analyzed using amplified DNA from the 3’ region of the small subunit ribosomal RNA gene (18SrDNA) and the adjacent first internal transcribed spacer (ITS1). Eighteen mitochondrial haplotype groups, falling into four major clades, were identified by well-supported nodes in Bayesian and maximum likelihood trees and recognized as distinct lineages by species delimitation metrics. Discriminant function analysis of a set of morphological characters indicated that the major clades in the dataset possessed a strong morphological signal that decreased in comparisons of haplotype groups within clades. Evidence of biogeographic and phylogeographic patterns was apparent in the dataset. COI haplotype diversity was high in the southern Appalachian Mountains and Gulf Coast states and lessened in northern temperate forests. Lobocriconema distribution suggests the existence of phylogeographic patterns associated with recolonization of formerly glaciated regions by eastern deciduous forest, but definitive glacial refugia for this group of plant parasitic nematodes have yet to be identified. Unlike agricultural pest species of plant-parasitic nematodes, there is little evidence of long-distance dispersal in Lobocriconema as revealed by haplotype distribution. Most haplotype groups were characterized by low levels of intragroup genetic variation and large genetic distances between haplotype groups. The localization of nematode haplotypes together with their characteristic plant communities could provide insight into the historical formation of these belowground biotic communities.

 

References

  1. Andrássy, I. (1965) Verzeichnis und Bestimmungsschlüssel der Arten der Nematoden-Gattungen Criconemoides Taylor, 1936 und Mesocriconema n. gen. Opuscula Zoologica Instituti Zoosystematici Universitatis Budapestensis, 5, 153–171.

    Avise, J.C. (2000) Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge, MA, 447 pp.

    Birky, C.W. Jr. & Barraclough, T.G. (2009) Asexual speciation. In: Schön, I., Martens, K. & van Dijk, P. (Eds.), Lost sex: The evolutionary biology of parthenogenesis. Springer, Dordrecht, The Netherlands, pp. 201‒216.

    Cherry, T., Szalanski, A.L., Todd, T.C. & Powers, T.O. (1997) The internal transcribed spacer region of Belonolaimus (Nemata: Belonolaimidae). Journal of Nematology, 29, 23–29.

    Clary, D.O. & Wolstenholme, D.R. (1985) The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization and genetic code. Journal of Molecular Evolution, 22, 252‒271.

    http://dx.doi.org/10.1007/BF02099755

    Clayton, L., Attig, J.W. & Mickelson, D.M. (2001) Effects of late Pleistocene permafrost on the landscape of Wisconsin, USA. Boreas, 30 (3), 173–188.

    http://dx.doi.org/10.1111/j.1502-3885.2001.tb01221.x

    Clement, M., Posada, D. & Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1660.
    http://dx.doi.org/10.1046/j.1365-294x.2000.01020.x

    Cordero, M.A., Robbins, R.T. & Szalanski, A.L. (2012) Taxonomic and molecular identification of Bakernema, Criconema, Hemicriconemoides, Ogma, and Xenocriconemella species (Nematoda: Criconematidae). Journal of Nematology, 44, 427–446.

    De Grisse, A. & Loof, P.A.A. (1965) Revision of the genus Criconemoides (Nematoda). Mededelingen van de Landbouwhogeschool en de Opzoekingsstations van de Staat te Gent, 30, 577–603.

    De Guiran, G. (1963) Quatre espèces nouvelles du genre Criconemoides Taylor (Nematoda – Criconematidae). Revue de Pathologie Végétale et d’Entomologie Agricole de France, 42, 1–11.

    Edgar, R.C. (2004) MUSCLE: A multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics, 5, 113.
    http://dx.doi.org/10.1186/1471-2105-5-113

    Friedman, J.H. (1989) Regularized discriminant analysis. Journal of the American Statisical Association, 84, 165–175.
    http://dx.doi.org/10.1080/01621459.1989.10478752

    Geraert, E. (2010) The Criconematidae of the World. Identification of the Family Criconematidae (Nematoda). Academia Press, Gent, Belgium, 615 pp.

    Guindon, S. & Gascuel, O. (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704.
    http://dx.doi.org/10.1080/10635150390235520

    Hansen, H.P. (1939) Postglacial vegetation of the driftless area of Wisconsin. American Midland Naturalist, 21, 752–762.

    Hastie, T., Tibshirani, R. & Friedman, J.H. (2001) The elements of statistical learning: Data mining, inference, and prediction. Springer-Verlag, New York. 763 pp.

    Hewitt, G. (2000) The genetic legacy of the Quaternary ice ages. Nature, 405 (6789), 907–913.
    http://dx.doi.org/10.1038/35016000

    Hoffmann, J.K. (1974) Morphological variation in species of Bakernema, Criconema, and Criconemoides (Criconematidae: Nematoda). Iowa State Journal of Research, 49, 137–153.

    Hofmänner, B. & Menzel, R. (1914) Neue Arten freilebender Nematoden aus der Schweiz. Zoologischer Anzeiger, 44, 80–91.

    Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755.
    http://dx.doi.org/10.1093/bioinformatics/17.8.754

    Huson, D.H. (1998) SplitsTree: a program for analyzing and visualizing evolutionary data. Bioinformatics, 14, 68–73.
    http://dx.doi.org/10.1093/bioinformatics/14.1.68

    Huson, D.H. & Bryant, D. (2006) Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23, 254‒267.
    http://dx.doi.org/10.1093/molbev/msj030

    Jackson, S.T., Webb, R.S., Anderson, K.H., Overpeck, J.T., Webb III, T., Williams, J.W. & Hansen, B.C. (2000) Vegetation and environment in eastern North America during the last glacial maximum. Quaternary Science Reviews, 19, 489–508.
    http://dx.doi.org/10.1016/S0277-3791(99)00093-1

    Jenkins, W. (1964). A rapid centrifugal-flotation technique for separating nematodes from soil. Plant Disease Reporter, 48, 692.

    Kitamura, K., & Kawano, S. (2001) Regional differentiation in genetic components for the American beech, Fagus grandifolia Ehrh., in relation to geological history and mode of reproduction. Journal of Plant Research, 114, 353–368.
    http://dx.doi.org/10.1007/PL00013997

    Knobloch, N. & Bird, G.W. (1978) Criconematinae habitats and Lobocriconema thornei n. sp. (Criconematidae: Nematoda). Journal of Nematology, 10, 245–249.

    Lim, G.S., Balke, M. & Meier, R. (2012) Determining species boundaries in a world full of rarity: singletons, species delimitation methods. Systematic Biology, 61, 165–169.
    http://dx.doi.org/10.1093/sysbio/syr030

    Loof , P.A.A. & De Grisse, A. (1989) Taxonomic and nomenclatorial observations on the genus Criconemella De Grisse & Loof, 1965 sensu Luc & Raski, 1981. Mededelingen Faculteit Landbouwwetenschappen Rijksuniversiteit Gent, 54, 53–74.

    Masters, B.C., Fan, V. & Ross, H.A. (2011) Species delimitation - a geneious plugin for the exploration of species boundaries. Molecular Ecology Resources, 11, 154–157.
    http://dx.doi.org/10.1111/j.1755-0998.2010.02896.x

    Neher, D.A., Peck, S.L., Rawlings, J.O. & Campbell, C.L. (1995) Measures of nematode community structure and sources of variability among and within fields. Plant and Soil, 170, 167–181.
    http://dx.doi.org/10.1007/BF02183065

    O'Bannon, J.H. (1977) Worldwide dissemination of Radopholus similis and its importance in crop production. Journal of Nematology, 9, 16–25.

    Olson, D.M., Dinerstein, E., Wikramanayake, E.D., Burgess, N.D., Powell, G.V.N., Underwood, E.C., D'Amico, J.A., Itoua, I., Strand, H.E., Morrison, J.C., Loucks, C.J., Allnutt, T.F., Ricketts, T.H., Kura, Y., Lamoreux, J.F., Wettengel, W.W., Hedao, P. & Kassem, K.R. (2004) Terrestrial ecoregions of the world: A new map of life on earth. BioScience, 51, 933–938.
    http://dx.doi.org/10.1641/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2

    Posada, D. (2008) ModelTest: Phylogenetic Model Averaging. Molecular Biology and Evolution, 25, 1253–1256.
    http://dx.doi.org/10.1093/molbev/msn083

    Powers, T., Harris, T., Higgins, R., Mullin, P., Sutton, L. & Powers, K. (2011) MOTUs, morphology and biodiversity estimation: A case study using nematodes of the suborder Criconematina and a conserved 18S DNA barcode. Journal of Nematology, 43, 35–48.

    Powers, T.O., Harris, T., Higgins, R., Sutton, L. & Powers, K.S. (2010) Morphological and molecular characterization of Discocriconemella inarata, an endemic nematode from North American native tallgrass prairies. Journal of Nematology, 42, 35–45.

    Powers, T.O., Bernard, E.C., Harris, T., Higgins, R., Olson, M., Lodema, M., Mullin, P., Sutton, L. & Powers, K.S. (2014) COI haplotype groups in Mesocriconema (Nematoda: Criconematidae) and their morphospecies associations. Zootaxa, 3827 (2), 101–146.
    http://dx.doi.org/10.11646/zootaxa.3827.2.1

    Provan, J. & Bennett, K.D. (2008) Phylogeographic insights into cryptic glacial refugia. Trends in Ecology & Evolution, 23, 564–571.
    http://dx.doi.org/10.1016/j.tree.2008.06.010

    Raski, D.J. & Golden, A.M. (1966) Studies on the genus Criconemoides Taylor, 1936 with descriptions of eleven new species and Bakernema variabile n. sp. (Criconematidae: Nematoda). Nematologica, 11(1965), 501–565.

    Raski , D.J.& Luc, M. (1985) A reappraisal of the genus Criconema Hofmänner & Menzel, 1914 (Nematoda: Criconematidae). Revue de Nématologie, 7, 323–334.

    Rodrigo, A., Bertels, F., Heled, J., Noder, R., Shearman, H. & Tsai, P. (2008) The perils of plenty: what are we going to do with all these genes? Philosophical Transactions of the Royal Society B, 363, 3893–3902.

    http://dx.doi.org/10.1098/rstb.2008.0173

    Rosenberg, N.A. (2007) Statistical tests for taxonomic distinctiveness from observations of monophyly. Evolution, 61, 317–323.

    http://dx.doi.org/10.1111/j.1558-5646.2007.00023.x

    Ross, H.A., Murugan, S. & Li, W.L.S. (2008) Testing the reliability of genetic methods of species identification via simulation. Systematic Biology, 57, 216–230.
    http://dx.doi.org/10.1080/10635150802032990

    Saeki, I., Dick, C.W., Barnes, B.V. & Murakami, N. (2011) Comparative phylogeography of red maple (Acer rubrum L.) and silver maple (Acer saccharinum L.): impacts of habitat specialization, hybridization and glacial history. Journal of Biogeography, 38, 992–1005.
    http://dx.doi.org/10.1111/j.1365-2699.2010.02462.x

    Siddiqi, M.R. (1980) Taxonomy of the plant nematode superfamily Hemicycliophoroidea, with a proposal for Criconematina, new suborder. Revue de Nématologie, 3, 179–199.

    Siddiqi, M.R. (1986) Tylenchida, parasites of plants and insects. Commonwealth Institute of Parasitology, St. Albans, UK. 645 pp.

    Soltis, D.E., Morris, A.B., McLachlan, J.S., Manos, P.S. & Soltis, P.S. (2006) Comparative phylogeography of unglaciated eastern North America. Molecular Ecology, 15, 4261–4293.
    http://dx.doi.org/10.1111/j.1365-294X.2006.03061.x

    Southern, R. (1914) Clare Island Survey. Part 54. Nemathelmia, Kinorhyncha, and Chaetognatha. Proceedings of the Royal Irish Academy, 31, 1–80.

    Steiner, G., Taylor, A.L. & Cobb, G.S. (1951) Cyst-forming plant parasitic nematodes and their spread in commerce. Proceedings of the Helminthological Society of Washington, 18, 13–18.

    Tamura, K., Stecher, G., Peterson, D., Filipski A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.
    http://dx.doi.org/10.1093/molbev/mst197

    Taylor, A.L. (1936) The genera and species of the Criconematinae, a sub-family of the Anguillulinidae (Nematoda). Transactions of the American Microscopical Society, 55, 391–421.
    http://dx.doi.org/10.2307/3222522

    Team, R.C. (2015) R: A language and environment for statistical computing [Internet]. Vienna, Austria: R Foundation for Statistical Computing, 2013. Avaiable from: http://www. r-project.org (Accessed 1 Mar. 2016)

    Van den Berg, E. (1984) New Lobocriconema species from South Africa (Nematoda: Criconematidae). Phytophylactica, 16, 93–100.

    Van den Berg, E., Tiedt, L.R., Inserra, R.N., Stanley, J.D., Vovlas, N., Rius, J.E.P, Castillo, P. & Subbotin, S.A. (2014) Morphological and molecular characterisation of some Hemicriconemoides species (Nematoda: Criconematidae) together with a phylogeny of the genus. Nematology, 16, 519–553.
    http://dx.doi.org/10.1163/15685411-00002786

    Venables, W.N. & Ripley, B.D. (2002) Modern applied statistics with S Springer-Verlag. New York.
    http://dx.doi.org/10.1007/978-0-387-21706-2

    Viglierchio, D.R. & Schmitt, R.V. (1983) On the methodology of nematode extraction from field samples: Comparison of methods for soil extraction. Journal of Nematology, 15, 450–454.

    Widmer, A. & Lexer, C. (2001) Glacial refugia: sanctuaries for allelic richness, but not for gene diversity. Trends in Ecology & Evolution, 16, 267–269.
    http://dx.doi.org/10.1016/S0169-5347(01)02163-2

    Weihs, C., Ligges, U., Luebke, K. & Raabe, N. (2005) klaR analyzing German business cycles. In Data analysis and decision support. Springer Berlin Heidelberg. pp. 335–343.

    Wiens, J.J. (2012) Perspective: why biogeography matters: historical biogeography vs. phylogeography and community phylogenetics for inferring ecological and evolutionary processes. Frontiers of Biogeography, 4, 128–135.