Evolutionary Ecology

, Volume 28, Issue 6, pp 1019–1029 | Cite as

Evidence of taxa-, clone-, and kin-discrimination in protists: ecological and evolutionary implications

  • Avelina Espinosa
  • Guillermo Paz-y-Miño-C
Original Paper


Unicellular eukaryotes, or protists, are among the most ancient organisms on Earth. Protists belong to multiple taxonomic groups; they are widely distributed geographically and in all environments. Their ability to discriminate among con- and heterospecifics has been documented during the past decade. Here we discuss exemplar cases of taxa-, clone-, and possible kin-discrimination in five major lineages: Mycetozoa (Dictyostelium, Polysphondylium), Dikarya (Saccharomyces), Ciliophora (Tetrahymena), Apicomplexa (Plasmodium) and Archamoebae (Entamoeba). We summarize the proposed genetic mechanisms involved in discrimination-mediated aggregation (self vs. different), including the csA, FLO and trg (formerly lag) genes, and the Proliferation Activation Factors, which facilitate clustering in some protistan taxa. We caution about the experimental challenges intrinsic to studying recognition in protists, and highlight the opportunities for exploring the ecology and evolution of complex forms of cell–cell communication, including social behavior, in a polyphyletic, still superficially understood group of organisms. Because unicellular eukaryotes are the evolutionary precursors of multicellular life, we infer that their mechanisms of taxa-, clone-, and possible kin-discrimination gave origin to the complex diversification and sophistication of traits associated with species and kin recognition in plants, fungi, invertebrates and vertebrates.


Altruism Green-beard effect Kin selection Local mate competition Recognition alleles Sex ratio 



Horizontal gene transfer


Entamoeba Proliferation Activating Factors


Tetrahymena Proliferation Activating Factors



We thank John A Endler for inviting us to write this article as part of our contribution to the Species Recognition Systems Symposium held in Lisbon, Portugal, August 2013, and sponsored by the European Society for Evolutionary Biology. A Espinosa is supported by NIH grant 8P20GM103430-13. Both authors are sponsored by New England Science Public and the Roger Williams University’s Center for the Public Understanding of Science. Two anonymous reviewers provided valuable comments to improve the manuscript.

Conflict of interest

The authors declare no competing interests.


  1. Benabentos R, Hirose S, Sucgang R, Curk T, Katoh M, Ostrowski EA, Strassmann JE, Queller DC, Zupan B, Shaulsky G, Kuspa A (2009) Polymorphic members of the lag gene family mediate kin discrimination in Dictyostelium. Curr Biol 19:567–572PubMedCrossRefPubMedCentralGoogle Scholar
  2. Bruto M, Prigent-Combaret C, Luis P, Hoff G, Moënne-Loccoz Y, Muller D (2013) Horizontal acquisition of prokaryotic genes for eukaryote functioning and niche adaptation. In: Pontarotti P (ed) Evolutionary biology: exobiology and evolutionary mechanisms. Springer, Berlin, pp 165–179Google Scholar
  3. Caron DA (2013) Towards a molecular taxonomy for protists: benefits, risks, and applications in plankton ecology. J Eukaryot Microbiol 60:407–413PubMedCrossRefGoogle Scholar
  4. Chaine AS, Schtickzelle N, Polard T, Huet M, Clobert J (2010) Kin-based recognition and social aggregation in a ciliate. Evolution 64:1290–1300PubMedGoogle Scholar
  5. Clark CG, Diamond LS (1997) Intraspecific variation and phylogenetic relationships in the genus Entamoeba as revealed by riboprinting. J Eukaryot Microbiol 44:142–154PubMedCrossRefGoogle Scholar
  6. Clark CG, Kaffashian F, Tawari B, Windsor JJ, Twigg-Flesner A, Davies-Morel MCG, Blessmann J, Ebert F, Peschel B, Van AL, Jackson CJ, Macfarlane L, Tannich E (2006) New insights into the phylogeny of Entamoeba spp. provided by analysis of four new small-subunit rRNA genes. Int J Syst Evol Microbiol 56:2235–2239PubMedCrossRefGoogle Scholar
  7. Dawkins R (1976) The selfish gene. Oxford University Press, OxfordGoogle Scholar
  8. Dreyer DA (1961) Growth of a strain of Entamoeba histolytica at room temperature. Tex Rep Biol Med 19:393–396PubMedGoogle Scholar
  9. Espinosa A, Paz-y-Miño-C G (2012) Discrimination, crypticity and incipient taxa in Entamoeba. J Eukaryot Microbiol 59:105–110PubMedCrossRefPubMedCentralGoogle Scholar
  10. Espinosa A, Paz-y-Miño-C G (in press) Examining crypticity in Entamoeba: a behavioral and biochemical tale. In: Trueba G (ed) Why does evolution matter? The importance of understanding evolution. Cambridge Scholars, CambridgeGoogle Scholar
  11. Foster KR (2005) Hamiltonian medicine: why the social lives of pathogens matter. Science 308:1269–1270PubMedCrossRefGoogle Scholar
  12. Gardner A, West SA (2010) Greenbeards. Evolution 64:25–38PubMedCrossRefGoogle Scholar
  13. Ghoul M, Griffin AS, West SA (2014) Toward an evolutionary definition of cheating. Evolution 68:318–331PubMedCrossRefGoogle Scholar
  14. Gilbert OM, Strassmann JE, Queller DC (2012) High relatedness in a social amoeba: the role of kin discriminatory segregation. Proc R Soc B 279:2619–2624PubMedCrossRefPubMedCentralGoogle Scholar
  15. Gray CW, Marcus LC, McCarten WC, Sappington T (1966) Amoebiasis in the Komodo dragon. Int Zoo Yearb 6:279–283CrossRefGoogle Scholar
  16. Hamilton WD (1964) The genetical evolution of social behaviour I. J Theor Biol 7:1–16PubMedCrossRefGoogle Scholar
  17. Hamilton WD (1967) Extraordinary sex ratios. Science 156:477–488PubMedCrossRefGoogle Scholar
  18. Herbers JM (2013) 50 years on: the legacy or William Donald Hamilton. Biol Lett 9:20130792PubMedCrossRefGoogle Scholar
  19. Hirose S, Benabentos R, Ho H-I, Kuspa A, Shaulsky G (2011) Self-recognition in social Amoebae is mediated by allelic pairs of Tiger genes. Science 333:467–470PubMedCrossRefPubMedCentralGoogle Scholar
  20. Kalla SE, Queller DC, Lasagni A, Strassmann JE (2011) Kin discrimination and possible cryptic species in the social amoeba Polysphondylium violaceum. BMC Evol Biol 11:31. doi: 10.1186/1471-2148-11-31 PubMedCrossRefPubMedCentralGoogle Scholar
  21. Kamel SJ, Grosberg RK (2013) Kinship and the evolution of social behaviours in the sea. Biol Lett 9:20130454PubMedCrossRefGoogle Scholar
  22. Kaushik S, Katoch B, Nanjundiah V (2006) Social behaviour in genetically heterogeneous groups of Dictyostelium giganteum. Behav Ecol Sociobiol 59:521–530CrossRefGoogle Scholar
  23. Lecointre G, Le Guyader H (2006) The tree of life: a phylogenetic classification. The Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  24. Maynard-Smith J (1964) Group selection and kin selection. Nature 211:1145–1147CrossRefGoogle Scholar
  25. Medeiros MCI, Hamer GL, Ricklefs RE (2013) Host compatibility rather than vector-host-ecounter rate determines the host range of avian Plasmodium parasites. Proc R Soc B 280:20122947PubMedCrossRefPubMedCentralGoogle Scholar
  26. Meerovitch E (1958) A new host of Entamoeba invadens Rodhain, 1934. Can J Zool 36:423–427CrossRefGoogle Scholar
  27. Mehdiabadi NJ, Jack CN, Talley-Farnham T, Platt TG, Kalla SE, Shaulsky G, Queller DC, Strassmann JE (2006) Kin preference in a social microbe. Nature 442:881–882PubMedCrossRefGoogle Scholar
  28. Mideo N, Reece SE (2012) Plasticity in parasite phenotypes: evolutionary and ecological implications for disease. Future Microbiol 7:17–24PubMedCrossRefGoogle Scholar
  29. Mitta G, Adema CM, Gourbal B, Loker ES, Theron A (2012) Compatibility polymorphism in snail/schistosome interactions: from field to theory to molecular mechanisms. Dev Comp Immunol 37:1–8PubMedCrossRefPubMedCentralGoogle Scholar
  30. Nkhoma SC, Nair S, Cheeseman IH, Rohr-Allegrini C, Singlam S, Nosten F, Anderson TJC (2012) Close kinship within multiple-genotype malaria parasite infections. Proc R Soc B 279:2589–2598PubMedCrossRefPubMedCentralGoogle Scholar
  31. Ostrowski EA, Katoh M, Shaulsky G, Queller DC, Strassmann JE (2008) Kin discrimination increases with genetic distance in a social amoeba. PLoS Biol 6:e287. doi: 10.1371/journal.pbio.0060287 PubMedCrossRefPubMedCentralGoogle Scholar
  32. Pawlowski J (2013) The new micro-kingdoms of eukaryotes. BMC Biol. doi: 10.1186/1741-7007-11-40 PubMedPubMedCentralGoogle Scholar
  33. Paz-y-Miño-C G, Espinosa A (2010) Integrating horizontal gene transfer and common descent to depict evolution and contrast it with “common design”. J Eukaryot Microbiol 57:11–18PubMedCrossRefGoogle Scholar
  34. Penn DJ, Frommen JG (2010) Kin recognition: an overview of conceptual issues, mechanisms and evolutionary theory. In: Kappeler PM (ed) Animal behaviour: evolution and mechanisms. Springer, Berlin, pp 55–85Google Scholar
  35. Pollitt LC, MacGregor P, Mathews K, Reece SE (2011) Malaria and trypanosome transmission: different parasites, same rules? Trends Parasitol 27:197–203PubMedCrossRefPubMedCentralGoogle Scholar
  36. Queller DC, Ponte E, Bozzaro S, Strassmann JE (2003) Single-gene greenbeard effects in the social amoeba Dictyostelium discoideum. Science 299:105–106PubMedCrossRefGoogle Scholar
  37. Reece SE, Drew DR, Gardner A (2008) Sex ratio adjustment and kin discrimination in malaria parasites. Nature 453:609–614PubMedCrossRefGoogle Scholar
  38. Romeralo M, Escalante R, Baldauf SL (2012) Evolution and diversity of dictyostelid social amoebae. Protist 163:327–343PubMedCrossRefGoogle Scholar
  39. Schall JJ (2008) Sex rations writ small. Nature 453:605–606PubMedCrossRefGoogle Scholar
  40. Smukalla S, Caldara M, Pochet N, Beauvais A, Guadagnini S, Yan C, Vinces MD, Jansen A, Prevost MC, Latgé JP, Fink GR, Foster KR, Vestrepen KJ (2008) FLO1 is a variable green beard gene that drives biofilm-like cooperation in budding yeast. Cell 135:726–737PubMedCrossRefPubMedCentralGoogle Scholar
  41. Stensvold CR, Lebbad M, Clark CG (2010) Genetic characterisation of uninucleated cyst-producing Entamoeba spp. from ruminants. Int J Parasitol 40:775–778PubMedCrossRefGoogle Scholar
  42. Stoeck T, Stock A (2010) The protistan gap in the eukaryotic tree of life. Palaeodiversity 3:151–154Google Scholar
  43. Strassmann JE, Queller DC (2011) How social evolution theory impacts our understanding of development in the social amoeba Dictyostelium. Dev Growth Differ 53:597–607PubMedCrossRefGoogle Scholar
  44. Théron A, Coustau C (2005) Are Biomphalaria snails resistant to Schistosoma mansoni? J Helminthol 79:187–191PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.Department of BiologyRoger Williams UniversityBristolUSA
  2. 2.Department of BiologyUniversity of Massachusetts DartmouthNorth DartmouthUSA

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