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

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Abstract

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.

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References

  • Ainouche ML, Jenczewski E (2010) Focus on polyploidy. New Phytol 186:1–4

    Article  PubMed  Google Scholar 

  • Allen SL, Farrow SW, Golembiewski PA (1973) Esterase variations between the 14 syngens of Paramecium aurelia under axenic growth. Genetics 73:561–573

    PubMed  CAS  Google Scholar 

  • Allen SL, Adams J, Rushford CL (1983) Interspecies relationships in the Paramecium aurelia complex: acid phosphatase variation. J Eukaryot Microbiol 30(1):143–147

    Article  CAS  Google Scholar 

  • Barnett A (1966) A circadian rhythm of mating type reversals in Paramecium multimicronucleatum, syngen 2, and its genetic control. J Cell Physiol 67(2):239–270

    Article  PubMed  CAS  Google Scholar 

  • Beale GH, Preer JR Jr (2008a) Chapter 5: the determination of mating types in Paramecium. Paramecium: genetics and epigenetics. CRC Press, Boca Raton, pp 51–62

    Google Scholar 

  • Beale GH, Preer JR Jr (2008b) Chapter 12: Epigenetics. Paramecium: genetics and epigenetics. CRC Press, Boca Raton, pp 175–182

    Book  Google Scholar 

  • Bleyman L (1996) Ciliate genetics. In: Hausmann K, Bradbury PC (eds) Ciliates: cells as organisms. Gustav Fischer, Stuttgart, pp 291–324

    Google Scholar 

  • Brown JD, O’Neill RJ (2010) Chromosomes, conflicts, and epigenetics: chromosomal speciation revisited. Annu Rev Genom Human Genet 11:291–316

    Article  CAS  Google Scholar 

  • Catania F, Wurmser F, Potehkin AA, Pryzboś E, Lynch M (2009) Genetic diversity in the Paramecium aurelia species complex. Mol Biol Evol 26(2):421–431

    Article  PubMed  CAS  Google Scholar 

  • Coleman AW (2005) Paramecium aurelia revisited. J Eukaryot Microbiol 52(1):68–77

    Article  PubMed  CAS  Google Scholar 

  • Coyne RS, Chalker DL, Yao M-C (1996) Genome downsizing during ciliate development: nuclear division of labor through chromosome restructuring. Annu Rev Genet 30:557–578

    Article  PubMed  CAS  Google Scholar 

  • de Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56(6):876–886

    Google Scholar 

  • Dobzhansky T (1940) Speciation as a stage in evolutionary divergence. Am Nat 74:312–321

    Article  Google Scholar 

  • Donoghue MJ (1985) A critique of the biological species concept and recommendations for a phylogenetic alternative. Bryologist 88(3):172–181

    Article  Google Scholar 

  • Giraud T, Refrégier G, Le Gac M, de Vienne DM, Hood ME (2008) Speciation in fungi. Fungal Genet Biol 45:791–802

    Article  PubMed  CAS  Google Scholar 

  • 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 19–31

  • 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):105–113

    Article  PubMed  CAS  Google Scholar 

  • Hey J (2006) On the failure of modern species concepts. Trends Ecol Evol 21(8):447–450

    Article  PubMed  Google Scholar 

  • Hori M, Tomikawa I, Pryzboś E, Fujishima M (2006) Comparison of the evolutionary distances among syngens and sibling species of Paramecium. Mol Phylogenet Evol 38:697–704

    Article  PubMed  CAS  Google Scholar 

  • 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):363–408

    Article  Google Scholar 

  • Juranek SA, Lipps HJ (2007) New insights into the macronuclear development in ciliates. Int Rev Cytol 262:219–251

    Article  PubMed  CAS  Google Scholar 

  • Lolle SJ, Victor JL, Young JM, Pruitt RE (2005) Genome-wide non-mendelian inheritance of extra-genomic information in Arabidopsis. Nature 434:505–509

    Article  PubMed  CAS  Google Scholar 

  • Lynn DH (1996) Systematics of ciliates. In: Hausmann K, Bradbury PC (eds) Ciliates: cells as organisms. Gustav Fischer, Stuttgart, pp 51–72

    Google Scholar 

  • Mayden RL (2002) On biological species, species concepts and individuation in the natural world. Fish Fish 3:171–196

    Google Scholar 

  • Mayr E (1942) Systematics and the origin of species from the viewpoint of a zoologist. Harvard University Press, Cambridge, p xxi

    Google Scholar 

  • Mayr E (1996) What is a species, and what is not? Philos Sci 63(2):262–277

    Article  Google Scholar 

  • Mayr E, Provine WB (1981) The evolutionary synthesis. B Am Acad Arts Sci 34(8):17–32

    Article  Google Scholar 

  • 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 64–77

    Google Scholar 

  • McManus GB, Katz LA (2009) Molecular and morphological methods for identifying plankton: what makes a successful marriage? J Plank Research 31:1119–1129

    Article  CAS  Google Scholar 

  • Meiklejohn CD, Tao Y (2009) Genetic conflict and sex chromosome evolution. Trends Ecol Evol 25(4):215–223

    Article  PubMed  Google Scholar 

  • 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 127–150

    Google Scholar 

  • Mishler BD, Donoghue MJ (1982) Species concepts: a case for pluralism. Syst Zool 31(4):491–503

    Article  Google Scholar 

  • Miyake A (1996) Fertilization and sexuality in ciliates. In: Hausmann K, Bradbury PC (eds) Ciliates: cells as organisms. Gustav Fischer, Stuttgart, pp 243–290

    Google Scholar 

  • Nanney DL (1960) Temperature effects on nuclear differentiation in variety 1 of Tetrahymena pyriformis. Physiol Zool 33(2):146–151

    Google Scholar 

  • Orias E (1981) Probable somatic DNA rearrangements in mating type determination in Tetrahymena thermophila: a review and a model. Devel Genet 2:185–202

    Article  CAS  Google Scholar 

  • Parfrey LW, Katz LA (2010) Dynamic genomes of eukaryotes and the maintenance of genomic integrity. Microbe 5(4):156–163

    Google Scholar 

  • Paulin JJ (1996) Morphology and cytology of ciliates. In: Hausmann K, Bradbury PC (eds) Ciliates: cells as organisms. Gustav Fischer, Stuttgart, pp 1–40

    Google Scholar 

  • Phadke SS, Zufall RA (2009) Rapid diversification of mating systems in ciliates. Biol J Linn Soc 98:187–197

    Article  Google Scholar 

  • Preer JR Jr (2000) Epigenetic mechanisms affecting macronuclear development in Paramecium and Tetrahymena. J Eukaryot Microbiol 47(6):515–524

    Article  PubMed  CAS  Google Scholar 

  • 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):417–434

    Google Scholar 

  • 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 441:469–474

    Article  PubMed  CAS  Google Scholar 

  • Rebollo R, Horard B, Hubert B, Vieira C (2010) Jumping genes and epigenetics: towards new species. Gene 454:1–7

    Article  PubMed  CAS  Google Scholar 

  • Rice WR, Gavrilets S, Friberg U (2008) Sexually antagonistic “zygotic drive” of the sex chromosomes. PLOS Genet. doi:10.1371/journal.pgen.1000313

  • Schlegel M, Meisterfeld R (2003) The species problem in protozoa revisited. Europ J Protistol 39:349–355

    Article  Google Scholar 

  • Schloegel JJ (1999) From anomaly to unification: Tracy Sonneborn and the species problem in protozoa, 1954–1957. J Hist Biol 23(1):93–132

    Article  Google Scholar 

  • Sonneborn TM (1937) Sex, sex inheritance and sex determination in Paramecium aurelia. Proc Nat Acad Sci 23(7):378–385

    Article  PubMed  CAS  Google Scholar 

  • 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):411–434

    Google Scholar 

  • 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 155–324

    Google Scholar 

  • Sonneborn TM (1957b) Diurnal change of mating type in Paramecium. Anat Rec 128:626

    Google Scholar 

  • Sonneborn TM (1975) The Paramecium aurelia complex of fourteen sibling species. T Am Microsc Soc 94(2):155–178

    Article  Google Scholar 

  • Sonneborn TM, Lynch RS (1932) Racial differences in the early physiological effects of conjugation in Paramecium aurelia. Biol Bull 62(3):258–293

    Article  Google Scholar 

  • Sonneborn TM, Lynch RS (1934) Hybridization and segregation in Paramecium aurelia. J Exper Zool 67(1):1–72

    Article  Google Scholar 

  • Tait A (1970) Enzyme variation between syngens in Paramecium Aurelia. Biochem Genet 4(4):461–470

    Article  PubMed  CAS  Google Scholar 

  • 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 730–758

    Google Scholar 

  • Zufall RA, McGrath CL, Muse SV, Katz LA (2006) Genome architecture drives protein evolution in ciliates. Mol Biol Evol 23(9):1681–1687

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

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).

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Correspondence to Laura A. Katz.

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Hall, M.S., Katz, L.A. On the nature of species: insights from Paramecium and other ciliates. Genetica 139, 677–684 (2011). https://doi.org/10.1007/s10709-011-9571-3

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