Phylogenetic assessment of the earthworm Aporrectodea caliginosa species complex (Oligochaeta: Lumbricidae) based on mitochondrial and nuclear DNA sequences

Molecular Phylogenetics and Evolution

Volumn 52, Issue 2, 2009, Pages 293-302

  Pérez Losada, Marcos ^a   Ricoy, Maigualida ^b   Marshall, Jonathon C ^c   Domínguez, Jorge ^b  

^a CENTRO DE INVESTIGAÇÃO EM BIODIVERSIDADE E RECURSOS GENÉTICOS   (Portugal)

^b UNIVERSITY OF VIGO   (Spain)

^c WEBER STATE UNIVERSITY   (United States)

Author keywords

Aporrectodea; Earthworms; Lumbricidae; Phylogeny; Species complex; Species delimitation; Taxonomy

Indexed keywords

MITOCHONDRIAL DNA;

ANIMAL; ANNELID WORM; ARTICLE; BAYES THEOREM; CELL NUCLEUS; CLASSIFICATION; DNA SEQUENCE; GENETICS; HISTOLOGY; MOLECULAR EVOLUTION; PHYLOGENY; SEQUENCE ALIGNMENT; SPECIES DIFFERENTIATION; STATISTICAL MODEL;

ANIMALS; BAYES THEOREM; CELL NUCLEUS; DNA, MITOCHONDRIAL; EVOLUTION, MOLECULAR; GENETIC SPECIATION; LIKELIHOOD FUNCTIONS; OLIGOCHAETA; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

ANNELIDA; APORRECTODEA; APORRECTODEA CALIGINOSA; APORRECTODEA LONGA; APORRECTODEA NOCTURNA; APORRECTODEA TRAPEZOIDES; APORRECTODEA TUBERCULATA; LUMBRICIDAE; OLIGOCHAETA (METAZOA);

EID: 65649145475     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2009.04.003     Document Type: Article

References (69)

1. Blakemore R.J. Cosmopolitan Earthworms-An Eco-Taxonomic Guide to the Peregrine Species of the World. second ed. (2006), VermEcology, Japan 600 pp
2. Bøgh P.S. Identification of earthworms (Lumbricidae): choice of method and distinction criteria. Megadrilogica 4 (1992) 163-174
3. Bond J.E., and Stockman A.K. An integrative method for delimiting cohesion species: finding the population-species interface in a group of California trapdoor spiders with extreme genetic divergence and geographical structuring. Syst. Biol. 57 (2008) 628-646
4. Bouché M.B. Lombriciens de France. Écologie et Systématique (1972), INRA, Paris 671 pp
5. Briones M.J.I. Two ecotypes in Allolobophora caliginosa (Oligochaeta, Lumbricidae). Acta Oecologica 14 (1993) 317-325
6. Briones M.J.I. A taxonomic study of the Allolobophora caliginosa complex (Oligochaeta, Lumbricidae): a preliminary study. Can. J. Zool. 74 (1996) 240-244
7. Casellato S., and Rodighiero R. Karyology of Lumbricidae. III Contribution. Caryologia 25 (1972) 513-524
8. Casellato S. On polyploidy in oligochaetes with particular reference to Lumbricidae. In: Pagliai A.M.B., and Omodeo P. (Eds). Proceedings of the International Symposium on Earthworms (1987), Mucchi Editore, Modena 75-84
9. Dettman J.R., Jacobson D.J., Turner E., Pringle A., and Taylor J.W. Reproductive isolation and phylogenetic divergence in Nuerospora. Evolution 57 (2003) 2721-2741
10. Domínguez J., Bohlen P.J., and Parmelee R.W. Earthworms increase nitrogen leaching to greater soil depths in row crop agroecosystems. Ecosystems 7 (2004) 672-685
11. Domínguez J., Ferreiro A., and Velando A. Are Eisenia fetida (Savigny, 1826) and Eisenia andrei Bouché, 1972 (Oligochaeta, Lumbricidae) different biological species?. Pedobiologia 49 (2005) 81-87
12. Dugés A. Recherche sur la circulation, la respiration et al reproduction des Annélides sétigéres abranches. Ann. Sci. Nat. 15 (1828) 284-336
13. Dyer R., Fowler J.C.S., and Baker G.H. Detecting genetic variability in exotic earthworms, Aporrectodea spp. (Lumbricidae), in Australian soils using RAPD markers. Soil Biol. Biochem. 30 (1998) 159-165
14. Eisen G. New Englands och Canadas Lumbricider. Ofvers. K. Vetensk. Akad. Forh. 30 (1874) 41-49
15. Evans A.C. A new species of earthworm of the genus Allolobophora. Annu. Mag. Nat. Hist. (Ser.11) 14 (1946) 98-101
16. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39 (1985) 783-791
17. Funk D.J., and Omland K.E. Specie-level paraphyly and polyphyly: frequency causes, and consequences, with insights from animal mitochondrial DNA. Ann. Rev. Ecol. Evol. Syst. 34 (2003) 397-423
18. Gates G.E. Contributions to North American earthworms (Annelida: Oligochaeta). No. 3: towards a revision of the earthworm family Lumbricidae IV. The trapezoides species group. Bull. Tall Timbers Res. Station 12 (1972) 1-146
19. Gerard, B.M., 1964. Synopses of the British fauna: (6) Lumbricidae. Linnean Society of London, pp. 58.
20. Guindon S., and Gascuel O. A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52 (2003) 696-704
21. Huelsenbeck J.P., and Imennov N.S. Geographic origin of human mitochondrial DNA: accommodating phylogenetic uncertainty and model comparison. Syst. Biol. 51 (2002) 155-165
22. Huelsenbeck J.P., Larget B., Miller R.E., and Ronquist F. Potential applications and pitfalls of Bayesian inference of phylogeny. Syst. Biol. 51 (2002) 673-688
23. Katoh K., Kuma K., Toh H., and Miyata T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33 (2005) 511-518
24. King R.A., Tibble A.L., and Symondson W.O. Opening a can of worms: unprecedented sympatric cryptic diversity within British lumbricide earthworms. Mol. Ecol. 17 (2008) 4684-4698
25. Marshall J.C., Arévalo E., Benavides E., Sites J., and Sites Jr. J.W. Delimiting species: Comparing methods for Mendelian characters using lizards of the Sceloporus grammicus (Squamata: Phrynosomatidae) complex. Evolution 60 (2006) 1050-1065
26. Mezhzherin S.V., Vlasenko R.P., and Garbar A.V. Genetic structure and peculiarities of earthworms Aporrectodea (superspecies) caliginosa (Oligochaeta: Lumbricidae) complex on the territory of Ukraine. Cytol. Genet. 42 (2008) 50-57
27. Michaelsen, W., 1900. Das Tierreich 10: Vermes, Oligochaeta. Friedman & Sohn, Germany, pp. 715.
28. Mršić, N., 1991. Monograph on earthworms (Lumbricidae) of the Balkans. Academia scientiarum et atrium Slovenica, Historia naturalis, Ljubljana 31, 1-355; II: 356-757.
29. Omodeo P. Cariologia dei Lumbricidae. Caryologia 4 (1952) 173-178
30. Omodeo P. Carioilogia dei Lumbricidae. II. Contributo. Caryologia 8 (1955) 135-178
31. Omodeo P. Contributo alla revisione dei Lumbricidae. Arch. Zool. Ital. 41 (1956) 129-212
32. Perel T.S. The shape of nephridial bladders as a taxonomic character in the systematics of Lumbricidae. Zoologischer Anzeiger 191 (1973) 310-317
33. Perel T.S. A critical analysis of the Lumbricidae genera system (with key to the USSR fauna genera). Rev. Ecol. Biol. Sol. 13 (1976) 635-643
34. Pérez-Losada M., Høeg J.T., and Crandall K.A. Unraveling the evolutionary radiation of the Thoracican barnacles using molecular and morphological evidence. A comparison of several divergence time estimation approaches. Syst. Biol. 53 (2004) 244-264
35. Pérez-Losada M., Eiroa J., Mato S., and Domínguez J. Phylogenetic species delimitation of the earthworm Eisenia fetida (Savigny, 1826) and Eisenia andrei (Bouché, 1972) (Oligochaeta, Lumbricidae) based on mitochondrial and nuclear DNA genes. Pedobiologia 49 (2005) 317-324
36. Piearce T.G., Oates K., and Carruthers W.J. A fossil earthworm embryo (Oligochaeta) from beneath a Late Bronze Age midden at Potterne, Wiltshire. UK J. Zool. 220 (1990) 537-542
37. Pons J., Barraclough T.G., Gomez-Zurita J., Cardoso A., Duran D.P., Hazell S., Kamoun S., Sumlin W.D., and Vogler A.P. Sequence based species delimitation for the DNA taxonomy of undescribed insects. Syst. Biol. 55 (2006) 595-609
38. Pop A.A., Wink M., and Pop V.V. Using of 18S, 16S rDNA and cytochrome c oxidase sequences in earthworm taxonomy (Oligochaeta, Lumbricidae). Pedobiologia 47 (2003) 428-433
39. Pop V.V. Towards a consistent and convenient genera system of the Lumbricidae family (Oligochaeta). A compromise between splitter and lumper viewpoints, adapted for the Romanian earthworm fauna. In: Moreno A., and Borges S. (Eds). Avances en taxonomía de lombrices de tierra/Advances in Earthworm Taxonomy (Annelida: Oligochaeta) (2004), Editorial Complutense, Madrid 317-333
40. Pop A.A., Csuzdi Cs., Wink M., and Pop V.V. An attempt to reconstruct the molecular phylogeny of the Genus Allolobophora (sensu lato, Pop, 1941) using 16S rDNA and COI sequences (Oligochaeta, Lumbricidae). In: Pop V.V., and Pop A.A. (Eds). Advances in Earthworm Taxonomy II (2006), University Press, Cluj 155-166
41. Posada D., and Crandall K.A. Modeltest: testing the model of DNA substitution. Bioinformatics 14 (1998) 817-818
42. Posada D., and Buckley T.R. Model selection and model averaging in phylogenetics: advantages of Akaike Information Criterion and Bayesian approaches over Likelihood Ratio Tests. Syst. Biol. 53 (2004) 793-808
43. Qiu J.P., and Bouché M.B. Revision des taxons supraspécifiques de Lumbricoidea. Doc. Pedozoologiques et Integrologiques. Montpellier 3 (1998) 179-216
44. Rambaut, A., Drummond, A.J., 2003. Tracer: MCMC trace analysis tool. Available from: .
45. Rissler L.J., and Apodaca J.J. Adding more ecology into species delimitation : ecological niche models and phylogeography help define cryptic species in the Black salamander (Aneides flavipunctatus). Syst. Biol. 56 (2007) 924-942
46. Roe A.D., and Sperling F.A.H. Population structure and species boundaries delimitation of cryptic Dioryctria moths : an integrative approach. Mol. Ecol. 16 (2007) 3617-3633
47. Ronquist F., and Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 (2003) 1572-1574
48. Rosa D. Revisione dei Lumbricidi. Mem. R. Acc. Sci. Torino. 43 (1893) 399-476
49. Sanders K.L., Malhotra A., and Thorpe R.S. Combining molecular, morphological, and ecological data to infer species boundaries in a cryptic tropical pitviper. Biol. J. Linn. Soc. 87 (2006) 343-364
50. Savigny J.C. Anylyse d'un Mémoir sur les Lombrics par Cuvier. Mem. Acad. Sci. Inst. Fr. 5 (1826) 176-184
51. Sbordoni M.C., De Matthaeis E., Omodeo P., Bidoli R., and Rodino R. Allozyme variation and divergence between diploid and triploid population of Allolobophora caliginosa (Lumbricidae; Oligochaeta): particular reference to Lumbricids. In: Pagliai A.M.B., and Omodeo P. (Eds). Proceedings of the International Symposium on Earthworms (1987), Mucchi Editore, Modena 53-74
52. Schlick-Steiner B.C., Steiner F.M., Moder K., Seifert B., Sanetra M., Dryerson E., Stauffer C., and Christian E. A multidisciplinary approach reveals cryptic diversity in Western Paleartic Tetramorium ants (Hymenoptera: Formicidae). Mol. Phylogenet. Evol. 40 (2006) 259-273
53. Sei M., and Porter A.H. Delimiting species boundaries and the conservation genetics of the endangered maritime ringlet butterfly (Coenonympha nipisiquit McDunnough). Mol. Ecol. 16 (2007) 3313-3325
54. Shimodaira H., and Hasegawa M. Multiple comparisons of loglikelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 16 (1999) 1114-1116
55. Sims, R.W, Gerard, B.M., 1985. Earthworms, Keys and Notes for the Identification and Study of the Species. Synopses of the British Fauna (New Series) No. 31. Linnean Society of London and the Estuarine and Brackish-Water Sciences Association, London.
56. Sites J.W., and Marshall J.C. Delimiting species: a renaissance issue in systematic biology. Trends Ecol. Evol. 18 (2003) 462-470
57. Sites J.W., and Marshall J.C. Empirical criteria for delimiting species. Ann. Rev. Ecol. Evol. Syst. 35 (2004) 199-227
58. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22 (2006) 2688-2690
59. Stockman A.K., and Bond J.E. Delimiting cohesion species: extreme population structuring and the role of ecological interchangeability. Mol. Ecol. 2007 (2007) 3374-3392
60. *: Phylogenetic Analysis Using Parsimony (* and other methods), Sinauer, Sunderland, MA.
61. Templeton A.R. The meaning of species and speciation: a genetic perspective. In: Otte D., and Endler J.A. (Eds). Speciation and its Consequences (1989), Sinauer Associates, Sunderland, MA
62. Templeton A.R. Species and speciation: geography, population structure, ecology and gene trees. In: Howard D.J., and Berlocher S.H. (Eds). Endless Forms: Species and Speciation (1998), Oxford University Press, New York, NY 32-41
63. Vedovini A. Contribution à l'étude des variations de l'espèce Allolobophora caliginosa (Lumbricidae). Bull. Soc. Zool. France 94 (1969) 657-662
64. Wiens J. Combining data sets with different phylogenetic histories. Syst. Biol. 47 (1998) 568-581
65. Wiens J.J., and Penkrot T.A. Delimiting species using DNA and morphological variation and discordant species limits in spiny lizards (Sceloporus). Syst. Biol. 51 (2002) 69-91
66. Will K.W., Mishler B.D., and Wheeler Q.D. The perils of DNA barcoding and the need for integrative taxonomy. Syst. Biol. 54 (2005) 844-851
67. Yoder A.D., Olson L.E., Hanley C., Heckman K.L., Rasoloarison R., Russel A.L., Ranivo J., Soarimalala V., Karanth K.P., Raselimanana A.P., and Goodman S.M. A multidimensional approach for detecting species patterns in Malagasy vertebrates. Proc. Natl. Acad. Sci. USA 102 (2005) 6587-6594
68. Zicsi A. Verzeichniss der bis 1971 beschribenen und revidierten Taxa der Familie Lumbricidae (Oligochaeta). Acta Zool. Hung. 28 (1982) 421-454
69. Zicsi A. Über die Regenwürmer Ungarns (Oligochaeta, Lumbricidae) mit Bestimmungstabellen der Arten. Opuscula Zool. 24 (1991) 167-191