, Volume 139, Issue 5, pp 677–684 | Cite as

On the nature of species: insights from Paramecium and other ciliates

  • Meaghan S. Hall
  • Laura A. Katz


The multiple species concepts currently in use by the scientific community (e.g. Morphological, Biological, Phylogenetic) are united in that they all aim to capture the process of divergence between populations. For example, the Biological Species Concept defines a species as a natural group of organisms that is reproductively isolated from other such groups. Here we synthesize nearly a century of research on the ciliate genus Paramecium that highlights the shortcomings of our prevailing notions on the nature of species. In this lineage, there is discordance between morphology, mating behavior, and genetics, features assumed to be correlated, at least after sufficient time has passed, under all species concepts. Intriguingly, epigenetic phenomena are well documented in ciliates where they influence features such as germline/soma differentiation and mating type determination. Consequently, we hypothesize that divergence within ciliate populations is due to a dynamic interaction between genetic and epigenetic factors. The growing list of examples of epigenetic phenomena that potentially impact speciation (i.e. by influencing the dynamics of sex chromosomes, fate of hybrids, zygotic drive and genomic conflicts) suggests that interactions between genetics and epigenetics may also drive divergence in other eukaryotic lineages.


Species concepts Paramecium Epigenetics Ciliates Molecular evolution 



L. A. K. is extremely grateful to R.G. Harrison for the excellent training and continued support. L. A. K. is also supported by grants from the National Science Foundation (DEB RUI:0919152, DEB 043115, DEB 0816828) and National Institutes of Health (1R15GM081865-01).


  1. Ainouche ML, Jenczewski E (2010) Focus on polyploidy. New Phytol 186:1–4PubMedCrossRefGoogle Scholar
  2. Allen SL, Farrow SW, Golembiewski PA (1973) Esterase variations between the 14 syngens of Paramecium aurelia under axenic growth. Genetics 73:561–573PubMedGoogle Scholar
  3. Allen SL, Adams J, Rushford CL (1983) Interspecies relationships in the Paramecium aurelia complex: acid phosphatase variation. J Eukaryot Microbiol 30(1):143–147CrossRefGoogle Scholar
  4. Barnett A (1966) A circadian rhythm of mating type reversals in Paramecium multimicronucleatum, syngen 2, and its genetic control. J Cell Physiol 67(2):239–270PubMedCrossRefGoogle Scholar
  5. Beale GH, Preer JR Jr (2008a) Chapter 5: the determination of mating types in Paramecium. Paramecium: genetics and epigenetics. CRC Press, Boca Raton, pp 51–62Google Scholar
  6. Beale GH, Preer JR Jr (2008b) Chapter 12: Epigenetics. Paramecium: genetics and epigenetics. CRC Press, Boca Raton, pp 175–182CrossRefGoogle Scholar
  7. Bleyman L (1996) Ciliate genetics. In: Hausmann K, Bradbury PC (eds) Ciliates: cells as organisms. Gustav Fischer, Stuttgart, pp 291–324Google Scholar
  8. Brown JD, O’Neill RJ (2010) Chromosomes, conflicts, and epigenetics: chromosomal speciation revisited. Annu Rev Genom Human Genet 11:291–316CrossRefGoogle Scholar
  9. Catania F, Wurmser F, Potehkin AA, Pryzboś E, Lynch M (2009) Genetic diversity in the Paramecium aurelia species complex. Mol Biol Evol 26(2):421–431PubMedCrossRefGoogle Scholar
  10. Coleman AW (2005) Paramecium aurelia revisited. J Eukaryot Microbiol 52(1):68–77PubMedCrossRefGoogle Scholar
  11. Coyne RS, Chalker DL, Yao M-C (1996) Genome downsizing during ciliate development: nuclear division of labor through chromosome restructuring. Annu Rev Genet 30:557–578PubMedCrossRefGoogle Scholar
  12. de Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56(6):876–886Google Scholar
  13. Dobzhansky T (1940) Speciation as a stage in evolutionary divergence. Am Nat 74:312–321CrossRefGoogle Scholar
  14. Donoghue MJ (1985) A critique of the biological species concept and recommendations for a phylogenetic alternative. Bryologist 88(3):172–181CrossRefGoogle Scholar
  15. Giraud T, Refrégier G, Le Gac M, de Vienne DM, Hood ME (2008) Speciation in fungi. Fungal Genet Biol 45:791–802PubMedCrossRefGoogle Scholar
  16. Harrison RG (1998) Linking evolutionary pattern and process: the relevance of species concepts for the study of speciation. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, New York, pp 19–31Google Scholar
  17. Hegarty MJ, Batstone T, Barker GL, Edwards KJ, Abbott RJ, Hiscock SJ (2011) Nonadditive changes to cytosine methylation as a consequence of hybridization and genome duplication in Senecio (Asteraceae). Mol Ecol 20(1):105–113PubMedCrossRefGoogle Scholar
  18. Hey J (2006) On the failure of modern species concepts. Trends Ecol Evol 21(8):447–450PubMedCrossRefGoogle Scholar
  19. Hori M, Tomikawa I, Pryzboś E, Fujishima M (2006) Comparison of the evolutionary distances among syngens and sibling species of Paramecium. Mol Phylogenet Evol 38:697–704PubMedCrossRefGoogle Scholar
  20. Jennings HS, Raffel D, Lynch RS, Sonneborn TM (1932) The diverse biotypes produced by conjugation within a clone of Paramecium aurelia. J Exper Zool 62(2):363–408CrossRefGoogle Scholar
  21. Juranek SA, Lipps HJ (2007) New insights into the macronuclear development in ciliates. Int Rev Cytol 262:219–251PubMedCrossRefGoogle Scholar
  22. Lolle SJ, Victor JL, Young JM, Pruitt RE (2005) Genome-wide non-mendelian inheritance of extra-genomic information in Arabidopsis. Nature 434:505–509PubMedCrossRefGoogle Scholar
  23. Lynn DH (1996) Systematics of ciliates. In: Hausmann K, Bradbury PC (eds) Ciliates: cells as organisms. Gustav Fischer, Stuttgart, pp 51–72Google Scholar
  24. Mayden RL (2002) On biological species, species concepts and individuation in the natural world. Fish Fish 3:171–196Google Scholar
  25. Mayr E (1942) Systematics and the origin of species from the viewpoint of a zoologist. Harvard University Press, Cambridge, p xxiGoogle Scholar
  26. Mayr E (1996) What is a species, and what is not? Philos Sci 63(2):262–277CrossRefGoogle Scholar
  27. Mayr E, Provine WB (1981) The evolutionary synthesis. B Am Acad Arts Sci 34(8):17–32CrossRefGoogle Scholar
  28. McGrath CL, Zufall RA, Katz LA (2006) Ciliate genome evolution. In: Katz LA, Bhattacharya D (eds) Genomics and evolution in microbial eukaryotes. Oxford University Press, New York, pp 64–77Google Scholar
  29. McManus GB, Katz LA (2009) Molecular and morphological methods for identifying plankton: what makes a successful marriage? J Plank Research 31:1119–1129CrossRefGoogle Scholar
  30. Meiklejohn CD, Tao Y (2009) Genetic conflict and sex chromosome evolution. Trends Ecol Evol 25(4):215–223PubMedCrossRefGoogle Scholar
  31. Meyer E, Chalker DL (2007) Epigenetics of ciliates. In: Allis CD, Jenuwein T, Reinberg D, Caperros M-L (eds) Epigenetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 127–150Google Scholar
  32. Mishler BD, Donoghue MJ (1982) Species concepts: a case for pluralism. Syst Zool 31(4):491–503CrossRefGoogle Scholar
  33. Miyake A (1996) Fertilization and sexuality in ciliates. In: Hausmann K, Bradbury PC (eds) Ciliates: cells as organisms. Gustav Fischer, Stuttgart, pp 243–290Google Scholar
  34. Nanney DL (1960) Temperature effects on nuclear differentiation in variety 1 of Tetrahymena pyriformis. Physiol Zool 33(2):146–151Google Scholar
  35. Orias E (1981) Probable somatic DNA rearrangements in mating type determination in Tetrahymena thermophila: a review and a model. Devel Genet 2:185–202CrossRefGoogle Scholar
  36. Parfrey LW, Katz LA (2010) Dynamic genomes of eukaryotes and the maintenance of genomic integrity. Microbe 5(4):156–163Google Scholar
  37. Paulin JJ (1996) Morphology and cytology of ciliates. In: Hausmann K, Bradbury PC (eds) Ciliates: cells as organisms. Gustav Fischer, Stuttgart, pp 1–40Google Scholar
  38. Phadke SS, Zufall RA (2009) Rapid diversification of mating systems in ciliates. Biol J Linn Soc 98:187–197CrossRefGoogle Scholar
  39. Preer JR Jr (2000) Epigenetic mechanisms affecting macronuclear development in Paramecium and Tetrahymena. J Eukaryot Microbiol 47(6):515–524PubMedCrossRefGoogle Scholar
  40. Pryzboś E, Prajer M, Greczek-Stachura M, Skotarczak B, Maciejewska A, Tarcz S (2007) Genetic analysis of the Paramecium aurelia species complex (Protozoa: Ciliophora) by classical and molecular methods. Syst Biodivers 5(4):417–434Google Scholar
  41. Rassoulzadegan M, Grandjean V, Gounon P, Vincent S, Gillot I, Cuzin F (2006) RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse. Nature 441:469–474PubMedCrossRefGoogle Scholar
  42. Rebollo R, Horard B, Hubert B, Vieira C (2010) Jumping genes and epigenetics: towards new species. Gene 454:1–7PubMedCrossRefGoogle Scholar
  43. Rice WR, Gavrilets S, Friberg U (2008) Sexually antagonistic “zygotic drive” of the sex chromosomes. PLOS Genet. doi: 10.1371/journal.pgen.1000313
  44. Schlegel M, Meisterfeld R (2003) The species problem in protozoa revisited. Europ J Protistol 39:349–355CrossRefGoogle Scholar
  45. Schloegel JJ (1999) From anomaly to unification: Tracy Sonneborn and the species problem in protozoa, 1954–1957. J Hist Biol 23(1):93–132CrossRefGoogle Scholar
  46. Sonneborn TM (1937) Sex, sex inheritance and sex determination in Paramecium aurelia. Proc Nat Acad Sci 23(7):378–385PubMedCrossRefGoogle Scholar
  47. Sonneborn TM (1938) Mating types in Paramecium aurelia: diverse conditions for mating in different stocks; occurrence, number and interrelations of the types. P Am Philos Soc 79(3):411–434Google Scholar
  48. Sonneborn TM (1957a) Breeding systems, reproductive methods, and species problems in protozoa. In: Mayr E (ed) The species problem. American Association for the Advancement of Science, Washington DC, pp 155–324Google Scholar
  49. Sonneborn TM (1957b) Diurnal change of mating type in Paramecium. Anat Rec 128:626Google Scholar
  50. Sonneborn TM (1975) The Paramecium aurelia complex of fourteen sibling species. T Am Microsc Soc 94(2):155–178CrossRefGoogle Scholar
  51. Sonneborn TM, Lynch RS (1932) Racial differences in the early physiological effects of conjugation in Paramecium aurelia. Biol Bull 62(3):258–293CrossRefGoogle Scholar
  52. Sonneborn TM, Lynch RS (1934) Hybridization and segregation in Paramecium aurelia. J Exper Zool 67(1):1–72CrossRefGoogle Scholar
  53. Tait A (1970) Enzyme variation between syngens in Paramecium Aurelia. Biochem Genet 4(4):461–470PubMedCrossRefGoogle Scholar
  54. Yao M-C, Duharcourt S, Chalker DL (2002) Genome-wide rearrangements of DNA in ciliates. In: Craig NL, Craigie R, Gellert M, Lambowitz A (eds) Mobile DNA II. ASM Press, Washington DC, pp 730–758Google Scholar
  55. Zufall RA, McGrath CL, Muse SV, Katz LA (2006) Genome architecture drives protein evolution in ciliates. Mol Biol Evol 23(9):1681–1687PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Department of Biological SciencesSmith CollegeNorthamptonUSA
  2. 2.Program in Organismic and Evolutionary BiologyUniversity of MassachusettsAmherstUSA

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