Reproduction of Earthworms: Sexual Selection and Parthenogenesis

  • Darío J. Díaz CosínEmail author
  • Marta Novo
  • Rosa Fernández
Part of the Soil Biology book series (SOILBIOL, volume 24)


Earthworms are generally cross-fertilization hermaphrodites, but up to 40% of the species can be parthenogenetic. In simultaneous hermaphrodites, a trade-off between male and female sexual functions is expected because the two sexes share limited resources from the same individual. In this chapter, several issues regarding sexual selection such as the role of spermathecae, copulatory behavior, allohormone injection, or adjustment of the donated sperm volume are reviewed. Parthenogenesis is present in some families as Lumbricidae, but is lacking in others. Parthenogenetic reproduction in earthworms is generally automictic and thelytokous, although apomixis and pseudogamy have been occasionally described. This kind of reproduction is poorly understood due to some background limitations such as the species concept in parthenogens or its possible origin, which are discussed in this chapter.


Sexual Selection Sperm Competition Female Function Simultaneous Hermaphrodite Cryptic Female Choice 
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  1. Ankel WE (1927) Neuere Arbeiten zur Zytologie der natürlichen Parthenogenese der Tiere. Z Indikt Abstamm Vererbungsl 45:232–278CrossRefGoogle Scholar
  2. Bateman AJ (1948) Intra-sexual selection in Drosophila. J Hered 2:349–368CrossRefGoogle Scholar
  3. Beatty RA (1957) Parthenogenesis and polyploidy in mammalian development. Cambridge University Press, London, p 134Google Scholar
  4. Beatty RA (1967) Parthenogenesis in vertebrates. In: Metz CB, Monroy A (eds) Fertilization, vol I. Academic, New York, pp 413–440Google Scholar
  5. Blakemore RJ (1994) Earthworms of South East Queensland and their potential in brigalow soils. PhD Thesis, University of QueenslandGoogle Scholar
  6. Blakemore RJ (1999) The diversity of exotic earthworms in Australia – a status report. In: Ponder W, Lunney D (eds). Proceedings of “The other 99%” TRZS NSW, pp 182–187Google Scholar
  7. Bonnet C (1762) Considerations sur les Corps Organisés. Fayard, Tours, 1985:348Google Scholar
  8. Bouché MB (1975) La reproduction de Spermophorodrilus albanianus nov. Gen., nov. Spec. (Lumbricidae) explique-t-elle la fonction des spermatophores? Zoologische Jahrbücher Abteilung für Systematique 102:1–11Google Scholar
  9. Buckley TR, Attanayake D, Park D, Ravindran S, Jewell TR, Normark BB (2008) Investigating hybridization in the parthenogenetic New Zealand stick insect Acanthoxyla (Phasmatodea) using single-copy nuclear loci. Mol Phylogenet Evol 48:335–349CrossRefPubMedGoogle Scholar
  10. Butt KR, Nuutinen V (1998) Reproduction of the earthworm Lumbricus terrestris Linné after the first mating. Can J Zool 76:104–109CrossRefGoogle Scholar
  11. Cameron EK, Bayne EM, Coltman DW (2008) Genetic structure of invasive earthworms Dendrobaena octaedra in the boreal forest of Alberta: insights into introduction mechanisms. Mol Ecol 17:1189–1197CrossRefPubMedGoogle Scholar
  12. Casellato S (1987) On polyploidy in Oligochates with particular reference to lumbricids. In: Bonvicini AM, Omodeo P (eds) On earthworms. Mucchi, Modena, pp 75–87Google Scholar
  13. Casellato S, Rodighiero R (1972) Karyology of Lumbricidae. 3rd contribution. Caryologia 25:513–524Google Scholar
  14. Cobolli Sbordoni M, De Matthaeis E, Omodeo P, Bidoli R, and Rodino E (1987) Allozyme variation and divergence between diploid and triploid populations of Allolobophora caliginosa (Lumbricidae: Oligochaeta). In: Bonvicini Pagliai AM, Omodeo P (eds) On earthworms, pp. 53–74. Selected Symposia and Monographs U.Z.I., vol 2. Mucchi, ModenaGoogle Scholar
  15. Delmotte F, Sabater-Muñoz B, Prunier-Leterme N, Latorre A, Sunnucks P, Rispe C, Simon JC (2003) Phylogenetic evidence for hybrid origins of asexual lineages in an aphid species. Evolution 57:1291–1303PubMedGoogle Scholar
  16. Domínguez J, Velando A, Aira M, Monroy F (2003) Uniparental reproduction of Eisenia fetida and E. andrei (Oligochaeta: Lumbricidae): evidence of self insemination. Pedobiologia 47:530–534Google Scholar
  17. Edwards CA, Bohlen PJ (1996) Biology and ecology of earthworms, 3rd edn. Chapman and Hall, London, p 426Google Scholar
  18. Fernández R, Novo M, Gutiérrez M, Almodóvar A, Díaz Cosín D (2010) Life cycle and reproductive traits in the earthworm Aporrectodea trapezoides (Dugès, 1828) in laboratory cultures. Pedobiologia 53:295–299Google Scholar
  19. Field SG, Michiels NK (2005) Parasitism and growth in the earthworm Lumbricus terrestris: fitness costs of the gregarine parasite Monocystis sp. Parasitology 130:1–7CrossRefGoogle Scholar
  20. Field SG, Schirp HJ, Michiels NK (2003) The influence of Monocystis sp infection on growth and mating behaviour of the earthworm Lumbricus terrestris. Can J Zool 81:1161–1167CrossRefGoogle Scholar
  21. Garvín MH, Trigo D, Hernández P, Díaz Cosín DJ (2003) Gametogenesis and reproduction in Hormogaster elisae (Oligochaeta, Hormogastridae). Inv Biol 122:152–157CrossRefGoogle Scholar
  22. Gates GE (1972) Contributions to North American earthworms. No. 3. IV. The trapezoides species group. Bull Tall Timbers Res Stn 12:146Google Scholar
  23. Gates GE (1974) Contributions to North American Earthworms. No. 10. Contributions to a revision of the Lumbricidae X: Dendrobaena octaedra (Savigny) 1826 with special reference to the importance of its parthenogenetic polymorphism for the importance for the classification of earthworms. Bull Tall Timbers Res Stn 15:57Google Scholar
  24. Grigoropoulou N, Butt KR, Lowe CN (2008) Effects on adult Lumbricus terrestris on cocoons and hatchlings in Evans´ boxes. Pedobiologia 51:343–349CrossRefGoogle Scholar
  25. Grove AJ (1925) On the reproductive processes of the earthworm, Lumbricus terrestris. Q J Microsc Sci 69:245–290Google Scholar
  26. Grove AJ, Cowley LF (1926) On the reproductive processes of the brandling worm, Eisenia fetida (Sav.). Q J Microsc Sci 70:559–581Google Scholar
  27. Haimi J, Knott KE, Yliniemi I (2007) Does metal contamination affect clonal diversity of the parthenogenetic earthworm Dendrobaena octaedra? Eur J Soil Boil 43:268–272CrossRefGoogle Scholar
  28. Hale CM, Frelich LE, Reich PB (2005) Exotic European earthworm invasion dynamics in northern hardwood forest of Minnesota, USA. Ecol Appl 15:848–860CrossRefGoogle Scholar
  29. Heethoff M, Etzold K, Scheu S (2004) Mitochondrial COII sequences indicate that the parthenogenetic earthworm Octolasion tyrtaeum (Savigny 1826) constitutes of two lineages differing in body size and genotype. Pedobiologia 48:9–13CrossRefGoogle Scholar
  30. Hughes RN (1989) A functional biology of clonal animals. Chapman and Hall, London, p 330Google Scholar
  31. ICZN (1999) International code of zoological nomenclature (4th edition). International Trust for Zoological Nomenclature, c/o Natural History Museum, London, p 306Google Scholar
  32. Jaenicke J, Selander RK (1979) Evolution and ecology of parthenogenesis in earthworms. Am Zool 19:729–737Google Scholar
  33. Jaenicke J, Parker ED, Selander RK (1980) Clonal niche structure in the parthenogenetic earthworm Octolasion tyrtaeum. Am Nat 116:196–205CrossRefGoogle Scholar
  34. Jamieson BGM (1992) Oligochaeta. In: Harrison FW, Gardiner SL (eds) Miscroscopic Anatomy of Invertebrates, vol 7. Wiley-Liss, New YorkGoogle Scholar
  35. Jamieson BGM (2006) Non leech Clitellata. In: Rouse GW, Pleijel F (eds) Reproductive biology and phylogeny of Annelida. SP Science Publishers, USA, p 688Google Scholar
  36. King RA, Tibble AL, Symodson WOC (2008) Opening a can of worms: unprecedented sympatric cryptic diversity within British lumbricid earthworms. Mol Ecol 17:4684–4698CrossRefPubMedGoogle Scholar
  37. Koene JM, Sundermann G, Michiels N (2002) On the function of body piercing during copulation in earthworms. Invert Reprod Develop 41:35–40Google Scholar
  38. Koene JM, Pfoertner T, Michiels NK (2005) Piercing the partner’s skin influences sperm uptake in the earthworm Lumbricus terrestris. Behav Ecol Sociobiol 59:243–249CrossRefGoogle Scholar
  39. Ligthart TN, Peek GJCW (1997) Evolution of earthworm burrow systems after inoculation of lumbricid earthworms in a pasture in the Netherlands. Soil Biol Biochem 29:453–462CrossRefGoogle Scholar
  40. Mariño MF, Velando A, Domínguez J (2006) Do earthworms trade sperm? The 8th International Symposium on Earthworm Ecology Krakow Poland, 4–9 September 2006. Sesion 5 Behavioral and Evolutionary Biology. p 149Google Scholar
  41. Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge, p 797Google Scholar
  42. Meyer WJ, Bowman H (1994) Mating period and cocoon production in Eisenia fetida. The 5th International Symposium on Earthworm Ecology Columbus Ohio, 5–9 July 1994. p 128Google Scholar
  43. Michiels NK (1998) Mating conflicts and sperm competition in simultaneous hermaphrodites. In: Birkhead R, Moller AP (eds) Sperm competition and sexual selection. Academic, London, pp 219–254CrossRefGoogle Scholar
  44. Michiels NK, Hohner A, Vorndran IC (2001) Precopulatory mate assessment in relation to body size in the earthworm Lumbricus terrestris: avoidance of dangerous liaisons? Behav Ecol 12:612–618CrossRefGoogle Scholar
  45. Monroy F, Aira M, Velando A, Domínguez J (2003) Have spermatophores in Eisenia fetida (Oligochaeta, Lumbricidae) any reproductive role? Pedobiologia 47:526–529Google Scholar
  46. Monroy F, Aira M, Velando A (2005) Size-assortative mating in the earthworm Eisenia fetida (Oligochaeta, Lumbricidae). J Ethol 23:69–70CrossRefGoogle Scholar
  47. Muldal S (1952) The chromosomes of the earthworms I. The evolution of polyploidy. Heredity 6:55–76CrossRefGoogle Scholar
  48. Novo M, Almodóvar A, Fernández R, Gutiérrez M, Díaz Cosín DJ (in press) Mate choice of an endogeic earthworm revealed by microsatellite markers. doi:10.1016/j.pedobi.2010.07.002Google Scholar
  49. Nuutinen V, Butt KR (1997) The mating behaviour of the earthworm Lumbricus terrestris (Oligochaeta: Lumbricidae). J Zool Lond 242:783–798CrossRefGoogle Scholar
  50. Olive PJW, Clark RB (1978) Physiology of reproduction. In: Mill PJ (ed) Physiology of annelids. Academic, London, pp 271–368Google Scholar
  51. Omodeo P (1951) Corredo cromosomico e spermatogenesi aberrante in Allolobophora caliginosa trapezoides. Boll Zool 18:27–39Google Scholar
  52. Omodeo P (1952) Cariologia dei lumbricidae. Caryologia 4:173–178Google Scholar
  53. Omodeo P (1953) Specie e razze poliploidi nei lombrichi. Convegno di Genetica, Ricerca Scientifica 23, Suppl 43.9Google Scholar
  54. Ortiz-Ceballos A, Fragoso C (2006) Parental care of endogeic earthworm cocoons: is cleaning, construction, and cast surrounding of chambers related to hatching and survival of juvenile worms? The 8th International Symposium on Earthworm Ecology Krakow Poland, 4–9 September 2006. Session 5 Behavioral and Evolutionary Biology. p 150Google Scholar
  55. Owen R (1849) On parthenogenesis, or the successive production of procreating individuals from a single ovum. John van Voorst, LondonGoogle Scholar
  56. Parker GA (1970) Sperm competition and its evolutionary consequences in insects. Biol Rev 45:525–567CrossRefGoogle Scholar
  57. Porto PG, Velando A, Dominguez J. (2008) Effects of mating frequency on sex allocation in the simultaneously hermaphroditic redworm (Eisenia andrei). The 15th International Colloquium on Soil Zoology Curitiba Brazil, 25–29 August 2008. Session 1 Soil Animal Biodiversity: the final frontier. S1T1P14Google Scholar
  58. Qiu JP, Bouché MB (1998) Contribution to the taxonomy of Hormogastridae (Annelida: Oligochaeta) with description of new species from Spain. Doc Pedozool Integro 4:164–177Google Scholar
  59. Reynolds JW (1974) Are oligochaetes really hermaphroditic anphimictic organisms? Biologist 56:90–99Google Scholar
  60. Richards KS, Fleming TP (1982) Spermatozoal phagocytosis by the spermathecae of Dendrobaena subrubicunda and other lumbricids (Oligochaeta, Annelida). Int J Invert Rep 5:233–241Google Scholar
  61. Sahm S, Velavan TP, Schulenburg H, Michiels NK (2009) Reconstruction of mating history – a retrospective analysis of Lumbricus terrestris mate choice criteria in natural populations. In: Velavan TP (ed) Population genetics of host–parasite interactions in Lumbricus terrestris and Monocystis sp (Apicomplexa: Gregarinea). Phd Thesis, Tübingen University, Germany, pp 43–57Google Scholar
  62. Sims RW, Gerard BM (1999) Earthworms, notes for the identification of British species. In: Barnes RSK, Crothers JH (eds) Synopses of the British fauna (new series), no. 31 revised. Field Studies Council, ShrewsburyGoogle Scholar
  63. Suomalainen E (1950) Parthenogenesis in animals. Adv Genet 3:193–253CrossRefPubMedGoogle Scholar
  64. Suomalainen E, Saura A, Lokki J (1987) Cytology and evolution in parthenogenesis. CRC, Boca Ratón, p 216Google Scholar
  65. Tato A, Velando A, Dominguez J (2006) Influence of size and partner preference on the female body function of the earthworm Eisenia andrei (Oligochaeta, Lumbricidae). Eur J Soil Biol 42:S331–S333CrossRefGoogle Scholar
  66. Tembe VB, Dubash PJ (1961) The earthworms: a review. J Bombay Nat Hist Soc 58:171–201Google Scholar
  67. Terhivuo J, Saura A (1993) Genic and morphological variation of the parthenogenetic earthworm Aporrectodea rosea in southern Finland (Oligochaeta, Lumbricidae). Am Zool Fennici 30:215–224Google Scholar
  68. Terhivuo J, Saura A (1996) Clone pool structure and morphometric variation in endogeic and epigeic North-European pathenogenetic earthworms (Oligochaeta: Lumbricidae). Pedobiologia 40:226–239Google Scholar
  69. Terhivuo J, Saura A (2003) Low clonal diversity and morphometrics in the parthenogenetic earthworm Octolasion cyaneum. Pedobiologia 47:434–439Google Scholar
  70. Thomsen M (1927) Studien über die Parthenogenese bei einigen Cocciden und Aleurodinen. Z Zellforsch Mikrosk Anat 5:1–10CrossRefGoogle Scholar
  71. Thornhill R (1983) Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps. Am Nat 122:765–788CrossRefGoogle Scholar
  72. Van Praagh BD (1995) Reproductive biology of Megascolides australis McCoy (Oligochaeta: Megascolecidae). Aust J Zool 43:489–507CrossRefGoogle Scholar
  73. Varuta AT, More NK (1972) Cytochemical study of mucus and mucus secreting cells in spermathecae of the earthworms, Pheretima elongata (Perrier) and Hoplochaetella powelli (Michaelsen). Ind Exp Biol 10:239–241Google Scholar
  74. Velando A, Domínguez J, Ferreiro A (2006) Inbreeding and outbreeding reduces cocoon production in the earthworm Eisenia andrei. Eur J Soil Biol 42:S354–S357CrossRefGoogle Scholar
  75. Velando A, Eiroa J, Dominguez J (2008) Brainless but not clueless: earthworms boost their ejaculates when they detect fecund non-virgin partners. Proc R Soc B 275:1067–1072CrossRefPubMedGoogle Scholar
  76. Victorov AG (1997) Diversity of polyploid races in the family Lumbricidae. Soil Biol Biochem 29:217–221CrossRefGoogle Scholar
  77. Vyas I, Dev B (1972) Histochemical localization of alkaline phosphatase in the spermathecae of the earthworm, Barogaster annandalei (Stephenson). Acta Histochem 42:344–350PubMedGoogle Scholar
  78. Wallwork JA (1983) Earthworm biology. Camelot, SouthhamtonGoogle Scholar
  79. White MJD (1973) Animal cytology and evolution. Cambridge University Press, London, p 961Google Scholar

Copyright information

© Springer Berlin Heidelberg 2011

Authors and Affiliations

  • Darío J. Díaz Cosín
    • 1
    Email author
  • Marta Novo
    • 1
  • Rosa Fernández
    • 1
  1. 1.Departamento de Zoología, Facultad de BiologíaUniversidad Complutense de Madrid, Ciudad UniversitariaMadridSpain

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