Potential of DNA barcoding for earthworm research in taxonomy and ecology

Applied Soil Ecology

Volumn 65, Issue , 2013, Pages 35-42

  Decaëns, Thibaud ^a   Porco, David ^a,b   Rougerie, Rodolphe ^a,b   Brown, George G ^c   James, Samuel W ^d  

^a UNIVERSITÉ DE ROUEN   (France)

^b UNIVERSITY OF GUELPH   (Canada)

^c EMBRAPA CERRADOS   (Brazil)

^d UNIVERSITY OF IOWA   (United States)

Author keywords

Cryptic diversity; DNA barcoding; Earthworm; Species identification; Taxonomic crisis; Taxonomic deficit

Indexed keywords

EID: 84873598669     PISSN: 09291393     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.apsoil.2013.01.001     Document Type: Review

References (88)

1. Addison J. Distribution and impacts of invasive earthworms in Canadian forest ecosystems. Biol. Invasions 2009, 11:59-79.
2. Amend A.S., Seifert K.A., Bruns T.D. Quantifying microbial communities with 454 pyrosequencing: does read abundance count?. Mol. Ecol. 2010, 19:5555-5565.
3. André H.M., Ducarme X., Anderson J.M., Crossley D., Koehler H., Paoletti M., Walter D., Lebrun P. Skilled eyes are needed to go on studying the richness of the soil. Nature 2001, 409:761.
4. André H.M., Ducarme X., Lebrun P. Soil biodiversity: myth, reality or conning?. Oikos 2002, 96:3-24.
5. André H.M., Noti M.-I., Lebrun P. The soil fauna: the other last biotic frontier. Biodivers. Conserv. 1994, 3:45-56.
6. Behan-Pelletier V. Linking soil biodiversity and ecosystem function - the taxonomic dillema. Bioscience 1999, 99:149-153.
7. Berthier K., Chapuis M.P., Moosavi S.M., Tohidi-Esfahani D., Sword G.A. Nuclear insertions and heteroplasmy of mitochondrial DNA as two sources of intra-individual genomic variation in grasshoppers. Syst. Entomol. 2011, 36:285-299.
8. Bienert F., De Danieli S., Miquel C., Coissac E., Poillot C., Brun J.-J., Taberlet P. Tracking earthworm communities from soil DNA. Mol. Ecol. 2012, 21:2017-2030.
9. Birky C.W., Adams J., Gemmel M., Perry J. Using population genetic theory and DNA sequences for species detection and identification in asexual organisms. PLoS ONE 2010, 5:e10609.
10. Blakemore R.J. Unravelling some Kinki earthworms (Annelida: Oligochaeta: Megadrili: Moniligastridae), Part II. Opusc. Zool. Budapes. 2010, 41:191-206.
11. Blakemore R.J., Kupriyanova E.K. Unravelling some Kinki worms (Annelida: Oligochaeta: Megadrili: Moniligastridae), Part I. Opusc. Zool. Budapes 2010, 41:3-18.
12. Blaxter M.L. The promise of a DNA taxonomy. Philos. T. Roy. Soc. B: Biol. Sci. 2004, 359:669-679.
13. Blaxter M.L., Mann J., Chapman T., Thomas F., Whitton C., Floyd R., Abebe E. Defining operational taxonomic units using DNA barcode data. Philos. T. Roy. Soc. B: Biol. Sci. 2005, 360:1935-1943.
14. Bohlen P.J., Groffman P.M., Fahey T.J., Fisk M.C., Suarez E., Pelletier D.M., Fahey R.T. Ecosystem consequences of exotic earthworm invasion of north temperate forests. Ecosystems 2004, 7:1-12.
15. Bouché M.B. Lombriciens de France, écologie et Systématique 1972, INRA Publ., Paris.
16. Bouché M.B., Beugnot M. La complexité taxonomique de Lumbricus herculeus illustrée par les caractéristiques de populations de stations de la R.C. P. 40. Revue d'écologie et de Biologie du Sol 1972, 9:697-704.
17. Bortolus A. Error cascades in the biological sciences: The unwanted consequences of using bad taxonomy in ecology. Ambio 2008, 37:114-118.
18. Briones M.J.I., Mornán P., Posada D. Are the sexual, somatic and genetic characters enough to solve nomenclatural problems in lumbricid taxonomy?. Soil Biol. Biochem. 2009, 41:2257-2271.
19. Brussaard L., Behan-Pelletier V.M., Bignell D.E., Brown V.K., Didden W., Folgarait P., Fragoso C., Freckman D.W., Gupta V.V.S.R., Hattori T., Hawksworth D.L., Klopatek C., Lavelle P., Malloch D.W., Rusek J., Soderstrom B., Tiedje J.M., Virginia R.A. Biodiversity and ecosystem function in soil. Ambio 1997, 26:563-570.
20. Calvignac S., Konecny L., Malard F., Douady C.J. Preventing the pollution of mitochondrial datasets with nuclear mitochondrial paralogs (numts). Mitochondrion 2011, 11:246-254.
21. Cameron E.K., Bayne E.M., Coltman D.W. Genetic structure of invasive earthworms Dendrobaena octaedra in the boreal forest of Alberta: insights into introduction mechanisms. Mol. Ecol. Resour. 2008, 17:1189-1197.
22. Chang C.-H., Chen J.-H. Taxonomic status and intraspecific phylogeography of two sibling species of Metaphire (Oligochaeta: Megascolecidae) in Taiwan. Pedobiologia 2005, 49:591-600.
23. Chang C.-H., James S. A critique of earthworm molecular phylogenetics. Pedobiologia 2011, 54S:S3-S9.
24. Chang C.-H., Lin Y.-H., Chen I.-H., Chuang S.-C., Chen J.-H. Taxonomic re-evaluation of the Taiwanese montane earthworm Amynthas wulinensis Tsai, Shen & Tsai, 2001 (Oligochaeta: Megascolecidae): poytypic species or species complex?. Organ. Divers. Evol. 2007, 7:231-240.
25. Chang C.-H., Rougerie R., Chen J.-H. Identifying earthworms through DNA barcodes: pitfalls and promise. Pedobiologia 2009, 52:171-180.
26. Chao A. Estimating the population size for capture-recapture data with unequal catchability. Biometrics 1987, 43:783-791.
27. Dabert J., Ehrnsberger R., Dabert M. Glaucalges tytonis sp n. (Analgoidea, Xolalgidae) from the barn owl Tyto alba (Strigiformes, Tytonidae): compiling morphology with DNA barcode data for taxon descriptions in mites (Acari). Zootaxa 2008, 1719:41-52.
28. Dance A. What lies beneath. Nature 2008, 455:724-725.
29. Decaëns T. Macroecological patterns in soil communities. Global Ecol. Biogeogr. 2010, 19:287-302.
30. Decaëns T., Jiménez J.J., Gioia C., Measey G.J., Lavelle P. The values of soil animals for conservation biology. Eur. J. Soil Biol. 2006, 42:S23-S38.
31. Decaëns, T., Lavelle, P., Jiménez, J.J., 2008. Priorities for conservation of soil animals. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 3, No. 14.
32. Decaëns T., Rougerie R. Descriptions of two new species of Hemileucinae (Lepidoptera: Saturniidae) from the region of Muzo in Colombia-evidence from morphology and DNA barcodes. Zootaxa 2008, 1944:34-52.
33. Dupont L., Lazrek F., Porco D., King R.A., Rougerie R., Symondson W.O.C., Livet A., Richard B., Decaëns T., Butt R., Mathieu J. New insight into the genetic structure of the Allolobophora chlorotica aggregate in Europe using microsatellite and mitochondrial data. Pedobiologia 2011, 54:217-224.
34. Fisher B.L., Smith M.A. A revision of Malagasy species of Anochetus Mayr and Odontomachus Latreille (Hymenoptera: Formicidae). PLoS ONE 2008, 3:e1787.
35. Fragoso C., Brown G.G., Patrón J.C., Blanchart E., Lavelle P., Pashanasi B., Senapati S., Kumar T. Agricultural intensification, soil biodiversity and agroecosystem function in the tropics: the role of earthworms. Appl. Soil Ecol. 1997, 6:17-35.
36. Giller P.S. The diversity of soil communities, the 'poor man's tropical rainforest'. Biodivers. Conserv. 1996, 5:135-168.
37. Gonzalez G. Earthworms as invasive species in Latin America. Caribbean J. Sci. 2006, 42:281-284.
38. Gotelli, N.J., Entsminger, G.L., 2001. Ecosim: Null Models Software for Ecology - Version 6.10. Acquired Intelligence Inc. & Kesey-Bear.
39. Hagvar S. The relevance of the Rio-Convention on biodiversity to conserving the biodiversity of soils. Appl. Soil Ecol. 1998, 9:1-7.
40. Hale C.M., Frelich L.E., Reich P.B. Exotic European earthworm invasion dynamics in northern hardwood forests of Minnesota, USA. Ecol. Appl. 2005, 15:848-860.
41. Hawksworth D.L. The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycol. Res. 2001, 105:1422-1432.
42. Hebert P.D.N., Cywinska A., Ball S.L., deWaard J.R. Biological identifications through DNA barcodes. Proc. Roy. Soc. Lond. B 2003, 270:313-321.
43. Hebert P.D.N., Penton R.H., Burns J.M., Janzen D.H., Hallwachs W. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:14812-14817.
44. Hendrix P.F., Bohlen P.J. Exotic earthworm invasions in North America: ecological and policy implications. Bioscience 2002, 52:801-811.
45. Huang J., Xu Q., Sun Z.J., Tang G.L., Su Z.Y. Identifying earthworms through DNA barcodes. Pedobiologia 2007, 51:301-309.
46. James S.W., Porco D., Decaëns T., Richard B., Rougerie R., Erséus C. DNA barcoding reveals cryptic diversity in Lumbricus terrestris L., 1758 (Clitellata): resurrection of L. Herculeus (Savigny, 1826). PLoS ONE 2010, 5:e15629.
47. King R.A., Tibble A.L., Symondson W.O.C. Opening a can of worms: unprecedented sympatric cryptic diversity within British lumbricid earthworms. Mol. Ecol. 2008, 17:4684-4698.
48. Klarica J., Kloss-Brandstätter A., Traugott M., Juen A. Comparing four mitochondrial genes in earthworms - implications for identification, phylogenetics, and discovery of cryptic species. Soil Biol. Biochem. 2011, 45:23-30.
49. Lavelle P., Decaëns T., Aubert M., Barot S., Blouin M., Bureau F., Margerie P., Mora P., Rossi J.P. Soil invertebrates and ecosystem services. Eur. J. Soil Biol. 2006, 42:S3-S15.
50. Lavelle P., Lapied E. Endangered earthworms of Amazonia: and homage to Gilberto Righi. Pedobiologia 2003, 47:419-427.
51. Lavelle P., Spain A.V. Soil Ecology 2001, Kluwer Academic Publishers, Dordrecht.
52. Lowe C.N., Butt K.R. Allolobophora chlorotica (Savigny, 1826): evidence for classification as two separate species. Pedobiologia 2008, 52:81-84.
53. Meusnier I., Singer G.A.C., Landry J.F., Hickey D.A., Hebert P.D.N., Hajibabaei M. A universal DNA mini-barcode for biodiversity analysis. BMC Genomics 2008, 9:214.
54. Minamiya Y., Yokoyama J., Fukuda T. A phylogeographic study of the Japanese earthworm, Metaphire sieboldi (Horst, 1883) (Oligochaeta: Megascolecidae): inferences from mitochondrial DNA sequences. Eur. J. Soil Biol. 2009, 45:423-430.
55. Novo, M., 2010. Algunos aspectos de la biología evolutiva de la familia Hormogastridae Michaelsen, 1900: Filogenia, filogeografía y selección sexual. Ph.D. Thesis. Universidad Complutense, Madrid, p. 340.
56. Novo M., Almodóvar A., Díaz Cosín D.J. High genetic divergence of hormogastrid earthworms (Annelida, Oligochaeta) in the central Iberian Peninsula: evolutionary and demographic implications. Zool. Scripta 2009, 38:537-552.
57. Novo M., Almodóvar A., Fernández R., Trigo D., Díaz Cosín D.J. Cryptic speciation of hormogastrid earthworms revealed by mitochondrial and nuclear data. Mol. Phylogenet. Evol. 2010, 56:507-512.
58. Oksanen, J., Kindt, R., Legendre, P., O'Hara, B., Simpson, G.L., Stevens, M.H.N., Wagner, H., 2008. Vegan: Community Ecology Package. R package version 1.13-1.
59. Perez-Losada M., Eiroa J., Mato S., Dominguez J. Phylogenetic species delimitation of the earthworms Eisenia fetida (Savigny, 1826) and Eisenia andrei Bouche, 1972 (Oligochaeta, Lumbricidae) based on mitochondrial and nuclear DNA sequences. Pedobiologia 2005, 49:317-324.
60. Pérez-Losada M., Bloch R., Breinholt J.W., Pfenninger M., Domínguez J. Taxonomic assessment of Lumbricidae (Oligochaeta) earthworm genera using DNA barcodes. Eur. J. Soil Biol. 2012, 48:41-47.
61. Porazinska D.L., Giblin-Davis R.M., Esquivel A., Powers T.O., Sung W., Thomas W.K. Ecometagenetics confirms high tropical rainforest nematode diversity. Mol. Ecol. 2010, 19:5521-5530.
62. Porco D., Bedos A., Deharveng L. Description and DNA barcoding assessment of the new species Deutonura gibbosa (Collembola: Neanuridae: Neanurinae), a common springtail of Alps and Jura. Zootaxa 2010, 2639:59-68.
63. Porco, D., Decaëns, T., Deharveng, L., James, S.W., Skarzinsky, D., Erseus, C., Butt, K.R., Richard, B., Hebert, P.D.N. DNA barcoding as a monitoring tool for soil invasions: a multiple taxa survey targeting European earthworms and collembolans in North America. Biol. Invasion, in press. doi:10.1007/s10530-012-0338-2.
64. Development Core Team R. R: A language and environment for statistical computing 2004, Vienna, Austria, R Foundation for Statistical Computing.
65. Ratnasingham S., Hebert P.D.N. The barcode of life data system. Mol. Ecol. Notes 2007, 7. 355-364. http://www.barcodinglife.org/.
66. Reynolds J.W., Cook D.G. Nomenclatura Oligochaetologica 1976, The University of New Brunswick, Fredericton.
67. Richard, B., 2008. Evaluation de la diversité spécifique des vers de terre de Haute Normandie par l'utilisation des codes barres ADN. Master Thesis. Université de Lyon, Lyon.
68. Richard B., Decaëns T., Rougerie R., James S.W., Porco D., Hebert P.D.N. Re-integrating earthworm juveniles into soil biodiversity studies: species identification through DNA barcoding. Mol. Ecol. Resour. 2010, 10:606-614.
69. Roesch L.F., Fulthorpe R.R., Riva A., Casella G., Hadwin A.K., Kent A.D., Daroub S.H., Camargo F.A., Farmerie W.G., Triplett E.W. Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J. 2007, 1:283-290.
70. Rougerie R., Decaëns T., Deharveng L., Porco D., James S.W., Chang C.-H., Richard B., Potapov M., Suhardjono Y., Hebert P.D.N. DNA barcodes for soil animal taxonomy. Pesqui. Agropecu. Bras. 2009, 44:789-801.
71. Rubinoff D., Holland B.S. Between two extremes: mitochondrial DNA is neither the panacea nor the nemesis of phylogenetic and taxonomic inference. Syst. Biol. 2005, 54:952-961.
72. Schaefer M., Schauermann J. The soil fauna of beech forests: comparison between a mull and a moder soil. Pedobiologia 1990, 34:299-314.
73. Sims R.W., Gerard B.M. Earthworms 1999, FSC Publications, London.
74. Smith M.A., Fernández-Triana J., Roughley R., Hebert P.D.N. DNA barcode accumulation curves for understudied taxa and areas. Mol. Ecol. Resour. 2009, 9:208-216.
75. Song H., Buhay J.E., Whiting M.F., Crandall K.A. Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:13486-13491.
76. Stoev P., Akkari N., Zapparoli M., Porco D., Enghof H., Edgecombe G.D., Georgiev T., Penev L. The centipede genus Eupolybothrus Verhoeff, 1907 (Chilopoda: Lithobiomorpha: Lithobiidae) in North Africa, a cybertaxonomic revision, with a key to all species in the genus and the first use of DNA barcoding for the group. ZooKeys 2010, 50:29-77.
77. Swift M.J., Heal O.W., Anderson J.M. Decomposition in Terrestrial Ecosystems 1979, Blackwell Scientific, Oxford, U.K.
78. Tomlin A.D. The earthworm bait market in North America. Earthworm Ecology 1983, Chapman and Hall, London, pp. 331-338. J.E. Satchell (Ed.).
79. Torsvik V., Goksoyr J., Daae F.L., Sorheim R., Michelsen J., Salte K. Use of DNA analysis to determine the diversity of microbial communities. Beyond the Biomass 1994, 39-48. Wiley Sayce, London. K. Ritz, J. Dighton, K.E. Diller (Eds.).
80. Trewick S.A. DNA barcoding is not enough: mismatch of taxonomy and genealogy in New Zealand grasshoppers (Orthoptera: Acrididae). Cladistics 2007, 23:1-15.
81. Urich T., Lanzén A., Qi J., Huson D.H., Schleper C., Schuster S.C. Simultaneous assessment of soil microbial community structure and function through analysis of the meta-transcriptome. PLoS ONE 2008, 3:e2527.
82. Vaglia T., Haxaire J., Kitching I.J., Meusnier I., Rougerie R. Morphology and DNA barcoding reveal three cryptic species within the Xylophanes neoptolemus and loelia species-groups (Lepidoptera: Sphingidae). Zootaxa 2008, 1923:18-36.
83. Valade R., Kenis M., Hernandez-Lopez A., Augustin S., Mena N.M., Magnoux E., Rougerie R., Lakatos F., Roques A., Lopez-Vaamonde C. Mitochondrial and microsatellite DNA markers reveal a balkan origin for the highly invasive horse-chestnut leaf miner Cameraria ohridella (Lepidoptera, Gracillariidae). Mol. Ecol. 2009, 18:3458-3470.
84. Wall D.H., Adams G.A., Parsons A.N. Soil biodiversity. Global Biodiversity in a Changing Environment 2001, 47-82. Springer Verlag, New York. F.S. Chapin, O.E. Sala, E. Huber-Sannwald (Eds.).
85. Wardle D.A. Communities and Ecosystems - Linking the Aboveground and Belowground Components 2002, Princeton University Press, Princeton.
86. Wiemers M., Fiedler K. Does the DNA barcoding gap exist? A case study in blue butterflies (Lepidoptera: Lycaenidae). Front. Zool. 2007, 4:8.
87. Will K.W., Mishler B.D., Wheeler Q.D. The perils of DNA barcoding and the need for integrative taxonomy. Syst. Biol. 2005, 54:844-851.
88. Wolters V. Biodiversity of soil animals and its function. Eur. J. Soil Biol. 2001, 37:221-227.