Challenging species delimitation in Collembola: Cryptic diversity among common springtails unveiled by DNA barcoding

Invertebrate Systematics

Volumn 26, Issue 5-6, 2012, Pages 470-477

  Porco, D ^a   Bedos, A ^b   Greenslade, Penelope ^c   Janion, C ^d   Skarzynski D ^e   Stevens, M I ^f   Jansen Van Vuuren, B ^g   Deharveng, L ^b  

^a UNIVERSITÉ DE ROUEN   (France)

^b MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^c School of Science   (Australia)

^d STELLENBOSCH UNIVERSITY   (South Africa)

^e UNIVERSITY OF WROC AW   (Poland)

^f SOUTH AUSTRALIAN MUSEUM   (Australia)

^g UNIVERSITY OF JOHANNESBURG   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

ARTHROPOD; DIVERGENCE; EVOLUTIONARY BIOLOGY; FUNCTIONAL GROUP; GENETIC MARKER; TAXONOMY;

EID: 84876459531     PISSN: 14455226     EISSN: None     Source Type: Journal    
DOI: 10.1071/IS12026     Document Type: Article

References (57)

1. Barateiro Diogo, J., Natal-Da-Luz, T., Paulo Sousa, J., Vogt, C., and Nowak, C. (2007). Tolerance of genetically characterized Folsomia candida strains to phenmedipham exposure-a comparison between reproduction and avoidance tests. Journal of Soils and Sediments 7, 388-392.
2. Busmachiu, G., Deharveng, L., and Weiner, W. M. (2010). A new species of the genus Lathriopyga Caroli, 1912 (Collembola, Neanuridae, Neanurinae) from the Republic of Moldova. Zootaxa 2639, 53-58.
3. Carapelli, A., Fanciulli, P. P., Frati, F., and Dallai, R. (1995a). The use of genetic markers for the diagnosis of sibling species in the genus Isotomurus (Insecta, Collembola). Bollettino di Zoologia 62, 71-76. doi:10.1080/11250009509356053
4. Carapelli, A., Frati, F., Fanciulli, P. P., and Dallai, R. (1995b). Genetic differentiation of six sympatric species of Isotomurus (Collembola, Isotomidae)-is there any difference in their microhabitat preference? European Journal of Soil Biology 31, 87-99.
5. Cassagnau, P. (1976). Variability of polytene chromosomes in Bilobella aurantiaca Caroli (Collembola, Neanuridae) its relations with biogeography and ecology of species. Archives De Zoologie Experimentale Et Generale 117, 511-572. [In French]
6. Cassagnau, P. (1991). Les collemboles Neanurinae de l'Himalaya 2: Paranurini et Paleonurini paucitubercules. Travaux du Laboratoire d'Ecobiologie des Arthropodes Edaphiques Toulouse 6, 1-20. [In French]
7. Cassagnau, P., Dallai, R., and Deharveng, L. (1979). Polytene chromosomes polymorphism in Lathriopyga longiseta Caroli (Collembola Neanuridae). Caryologia 32, 461-483.
8. Chenon, P., Rousset, A., and Crouau, Y. (2000). Genetic polymorphism in nine clones of a parthenogenetic collembolan used in ecotoxicological testing. Applied Soil Ecology 14, 103-110. doi:10.1016/S0929-1393(00) 00047-0
9. Cicconardi, F., Nardi, F., Emerson, B. C., Frati, F., and Fanciulli, P. P. (2010). Deep phylogeographic divisions and long-term persistence of forest invertebrates (Hexapoda: Collembola) in the North-Western Mediterranean basin. Molecular Ecology 19, 386-400. doi:10.1111/j.1365-294X.2009.04457.x
10. Crouau, Y., Cazes, L., and Bur, T. (2009). The use of the Collembola reproduction test in bioassays of polluted soils. In 'Progress in Environmental Science and Technology. Vol II, Pts A and B'. (Eds S. C. Li, Y. J. Wang, F. X. Cao, P. Huang and Y. Zhang.) pp. 1843-1845. (Science Press Beijing: Beijing.)
11. D'Haese, C. A. (2002). Were the first springtails semi-aquatic? A phylogenetic approach by means of 28S rDNA and optimization alignment. Proceedings. Biological Sciences 269, 1143-1151. doi:10.1098/rspb.2002.1981
12. Deharveng, L. (2004). Recent advances in Collembola systematics. Pedobiologia 48, 415-433. doi:10.1016/j.pedobi.2004.08.001
13. Fanciulli, P. P., Frati, F., Dallai, R., and Rusek, J. (1991). High genetic divergence among populations of Tetrodontophora bielanensis (Insecta, Collembola) in Europe. Revue D Ecologie Et De Biologie Du Sol 28, 165-173.
14. Fanciulli, P. P., Melegari, D., Carapelli, A., Frati, F., and Dallai, R. (2000). Population structure, gene flow and evolutionary relationships in four species of the genera Tomocerus and Pogonognathellus (Collembola, Tomoceridae). Biological Journal of the Linnean Society. Linnean Society of London 70, 221-238.
15. Fanciulli, P. P., Carapelli, A., Belloni, M., Dallai, R., and Frati, F. (2009). Allozyme variation in the springtails Allacma fusca and A. gallica (Collembola, Sminthuridae). Pedobiologia 52, 309-324. doi:10.1016/j.pedobi.2008. 11.004
16. Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294-299.
17. Frati, F., Fanciulli, P. P., and Dallai, R. (1992). Genetic diversity and taxonomy in soil-dwelling insects-the genus Orchesella. The Journal of Heredity 83, 275-281.
18. Frati, F., Carapelli, A., Fanciulli, P. P., and Dallai, R. (1995). The genus Isotomurus: where molecular markers help to evaluate the importance of morphological characters for the diagnosis of species. Polskie Pismo Entomologiczne 64, 41-51.
19. Frati, F., Negri, I., Fanciulli, P. P., Pellecchia, M., De Paola, V., Scali, V., and Dallai, R. (2004). High levels of genetic differentiation between Wolbachia-infected and non-infected populations of Folsomia candida (Collembola, Isotomidae). Pedobiologia 48, 461-468. doi:10.1016/j.pedobi.2004. 04.004
20. Hajibabaei, M., DeWaard, J. R., Ivanova, N. V., Ratnasingham, S., Dooh, R. T., Kirk, S. L., Mackie, P. M., and Hebert, P. D. N. (2005). Critical factors for assembling a high volume of DNA barcodes. Philosophical Transactions of the Royal Society B-Biological Sciences 360, 1959-1967. doi:10.1098/rstb.2005.1727
21. Hajibabaei, M., Janzen, D. H., Burns, J. M., Hallwachs, W., and Hebert, P. D. N. (2006). DNA barcodes distinguish species of tropical Lepidoptera. Proceedings of the National Academy of Sciences of the United States of America 103, 968-971. doi:10.1073/pnas.0510466103
22. Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95-98.
23. Hammond, P. M. (1992). Species inventory. In 'Global Biodiversity: Status of the Earth's Living Resources. A Report Compiled by the World Conservation Monitoring Centre'. (Ed. B. Groombridge.) pp. 17-39. (Chapman & Hall: London.)
24. Hausmann, A., Hebert, P. D. N., Mitchell, A., Rougerie, R., Sommerer, M., Edwards, T., and Young, C. J. (2009). Revision of the Australian Oenochroma vinaria Guenee, 1858 species-complex (Lepidoptera: Geometridae, Oenochrominae): DNA barcoding reveals cryptic diversity and assesses status of type specimen without dissection. Zootaxa 2239, 1-21.
25. Hebert, P. D. N., Cywinska, A., Ball, S. L., and DeWaard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London. Series B. Biological Sciences 270, 313-321. doi:10.1098/rspb.2002.2218
26. Hogg, I. D., and Hebert, P. D. N. (2004). Biological identification of springtails (Hexapoda: Collembola) from the Canadian Arctic, using mitochondrial DNA barcodes. Canadian Journal of Zoology-Revue Canadienne De Zoologie 82, 749-754. doi:10.1139/z04-041
27. Hopkin, S. P. (1997). 'Biology of the Springtails (Insecta: Collembola).' (Oxford University Press: New York & Tokyo.)
28. Ivanova, N. V., Dewaard, J. R., and Hebert, P. D. N. (2006). An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes 6, 998-1002. doi:10.1111/j.1471-8286.2006. 01428.x
29. James, S. W., Porco, D., Decaëns, T., Richard, B., Rougerie, R., and Erséus, C. (2010). DNA barcoding reveals cryptic diversity in Lumbricus terrestris L., 1758 (Clitellata): resurrection of L. herculeus (Savigny, 1826). PLoS ONE 5, e15629. doi:10.1371/journal.pone.0015629
30. Jordana, R., Schulz, H.-J., and Baquero, E. (2011a). New species of Entomobrya from Germany (Collembola, Entomobryini). Soil Organisms 83, 249-264.
31. Jordana, R., Giuga, L., and Baquero, E. (2011b). New species of Entomobrya from Etna mountain, Sicily (Collembola Entomobryomorpha). Redia-Giornale Di Zoologia 94, 35-38.
32. Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide-sequences. Journal of Molecular Evolution 16, 111-120. doi:10.1007/BF01731581
33. Kovac, L., and Papac, V. (2010). Revision of the genus Neelus Folsom, 1896 (Collembola, Neelida) with the description of twonewtroglobiotic species from Europe. Zootaxa 2663, 36-52.
34. Letunic, I., and Bork, P. (2007). Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics (Oxford, England) 23, 127-128. doi:10.1093/bioinformatics/btl529
35. Lukic, M., Houssin, C., and Deharveng, L. (2010).Anew relictual and highly troglomorphic species of Tomoceridae (Collembola) from a deep Croatian cave. ZooKeys 69, 1-16.
36. Lupetti, P., Marsili, L., Focardi, S., and Dallai, R. (1994). Organochlorine compounds in litter-dwelling arthropods: Collembola (Insecta Apterygota) from central Italy. Acta Zoologica Fennica 195, 94-97.
37. McGaughran, A., Torricelli, G., Carapelli, A., Frati, F., Stevens, M. I., Convey, P., and Hogg, I. D. (2010). Contrasting phylogeographical patterns for springtails reflect different evolutionary histories between the Antarctic Peninsula and continental Antarctica. Journal of Biogeography 37, 103-119. doi:10.1111/j.1365-2699.2009.02178.x
38. Palacios-Vargas, J. G., and Arbea, J. I. (2009). Neotropical species of Proisotoma (Collembola: Isotomidae), with description of two new cave species from America. Revista Mexicana De Biodiversidad 80, 445-453. [In Spanish]
39. Palacios-Vargas, J. G., Deharveng, L., andD'Haese, C. A. (2011). The genus Pronura (Collembola: Neanuridae) in South America, with descriptions of two new species and a barcode sequence for one of them. Revue Suisse de Zoologie 118, 197-205.
40. Porco, D., Bedos, A., and Deharveng, L. (2010a). Description and DNA barcoding assessment of the new species Deutonura gibbosa (Collembola: Neanuridae: Neanurinae), a common springtail of Alps and Jura. Zootaxa 2639, 59-68.
41. Porco, D., Rougerie, R., Deharveng, L., and Hebert, P. (2010b). Coupling nondestructive DNA extraction and voucher retrieval for small soft-bodied arthropods in a high-throughput context: the example of Collembola. Molecular Ecology Resources 10, 942-945. doi:10.1111/j.1755-0998.2010.2839.x
42. Porco, D., Potapov, M., Bedos, A., Busmachiu, G., Weiner, W. M., Hamra-Kroua, S., and Deharveng, L. (2012a). Cryptic diversity in the ubiquist species Parisotoma notabilis (Collembola, Isotomidae): a long used chimeric species? PLoS ONE 7(9), e46056.
43. Porco, D., Decaëns, T., Deharveng, L., James, S., Skar-zy-nski, D., Erséus, C., Butt, K., Richard, B., and Hebert, P. N. (2012b). Biological invasions in soil: DNA barcoding as a monitoring tool in a multiple taxa survey targeting European earthworms and springtails in North America. Biological Invasions. doi:10.1007/s10530-012-0338-2
44. Potapov, M. (2001). Synopses on Palaearctic Collembola. Volume 3. Isotomidae. Abhandlungen und Berichte des Naturkundemuseums Goerlitz 73, 1-603.
45. Riepert, F., and Kula, C. (1996). Development of laboratory methods for testing effects of chemicals and pesticides on Collembola and earthworms. In 'Communications from the Federal Biological Institute for Agriculture and Forestry'. (Ed. Berlin-Dahlem.) pp. 82.
46. Rocha-Ramírez, A., Ramirez-Rojas, A., Chavez-Lopez, R., and Alcocer, J. (2007). Invertebrate assemblages associated with root masses of Eichhornia crassipes (Mart.) Solms-Laubach 1883 in the Alvarado Lagoonal System, Veracruz, Mexico. Aquatic Ecology 41, 319-333. doi:10.1007/s10452-006-9054-2
47. Rost, M. M. (2006). Ultrastructural changes in the midgut epithelium in Podura aquatica L. (Insecta, Collembola, Arthropleona) during regeneration. Arthropod Structure & Development 35, 69-76. doi:10.1016/j.asd.2005.10.001
48. Rougerie, R., Decaens, T., Deharveng, L., Porco, D., James, S. W., Chang, C. H., Richard, B., Potapov, M., Suhardjono, Y., and Hebert, P. D. N. (2009).DNAbarcodes for soil animal taxonomy. Pesquisa Agropecuaria Brasileira 44, 789-802. doi:10.1590/S0100-204X2009000800002
49. Saitou, N., and Nei, M. (1987). The neighbor-joining method-a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406-425.
50. Salmon, S. (2001). Earthworm excreta (mucus and urine) affect the distribution of springtails in forest soils. Biology and Fertility of Soils 34, 304-310. doi:10.1007/s003740100407
51. Soto-Adames, F. N. (2002). Molecular phylogeny of the Puerto Rican Lepidocyrtus and Pseudosinella (Hexapoda: Collembola), a validation of Yoshii's "color pattern species". Molecular Phylogenetics and Evolution 25, 27-42. doi:10.1016/S1055-7903(02)00250-6
52. Stevens, M. I., and Hogg, I. D. (2006). Contrasting levels of mitochondrial DNA variability between mites (Penthalodidae) and springtails (Hypogastruridae) from the Trans-Antarctic Mountains suggest longterm effects of glaciation and life history on substitution rates, and speciation processes. Soil Biology & Biochemistry 38, 3171-3180. doi:10.1016/j.soilbio.2006.01.009
53. Stevens, M. I., Greenslade, P., Hogg, I. D., and Sunnucks, P. (2006). Southern Hemisphere springtails: could any have survived glaciation of Antarctica? Molecular Biology and Evolution 23, 874-882. doi:10.1093/molbev/ msj073
54. Stevens, M. I., Porco, D., D'Haese, C. A., and Deharveng, L. (2011). Comment on "Taxonomy and the DNA Barcoding Enterprise" by Ebach (2011). Zootaxa 2839, 85-88.
55. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007). MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596-1599. doi:10.1093/molbev/msm092
56. Torricelli, G., Carapelli, A., Convey, P., Nardi, F., Boore, J. L., and Frati, F. (2010). High divergence across the whole mitochondrial genome in the "pan-Antarctic" springtail Friesea grisea: evidence for cryptic species? Gene (Amsterdam) 449, 30-40. doi:10.1016/j.gene.2009.09.006
57. Tully, T., D'Haese, C. A., Richard, M., and Ferriere, R. (2006). Two major evolutionary lineages revealed by molecular phylogeny in the parthenogenetic collembola species Folsomia candida. Pedobiologia 50, 95-104. doi:10.1016/j.pedobi.2005.11.003