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Genetic Heterogeneity in Wild Isolates of Cellular Slime Mold Social Groups

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Abstract

This study addresses the issues of spatial distribution, dispersal, and genetic heterogeneity in social groups of the cellular slime molds (CSMs). The CSMs are soil amoebae with an unusual life cycle that consists of alternating solitary and social phases. Because the social phase involves division of labor with what appears to be an extreme form of “altruism”, the CSMs raise interesting evolutionary questions regarding the origin and maintenance of sociality. Knowledge of the genetic structure of social groups in the wild is necessary for answering these questions. We confirm that CSMs are widespread in undisturbed forest soil from South India. They are dispersed over long distances via the dung of a variety of large mammals. Consistent with this mode of dispersal, most social groups in the two species examined for detailed study, Dictyostelium giganteum and Dictyostelium purpureum, are multi-clonal.

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References

  1. Agnihothrudu V (1956) Occurrence of Dictyosteliaceae in the rhizosphere of plants in Southern India. Experientia 12:149–150

    Article  Google Scholar 

  2. Atzmony D, Zahavi A, Nanjundiah V (1997) Altruistic behaviour in Dictyostelium discoideum explained on the basis of individual selection. Curr Sci 72:142–145

    Google Scholar 

  3. Bonner JT (1959) Evidence for the sorting out of cells in the development of the cellular slime mold. Proc Natl Acad Sci USA 45:379–384

    Article  CAS  PubMed  Google Scholar 

  4. Bonner JT (1967) The cellular slime molds. Princeton University Press, Princeton

    Google Scholar 

  5. Bonner JT (1982) Evolutionary strategies and developmental constraints in the cellular slime molds. Am Naturalist 119:530–552

    Article  Google Scholar 

  6. Bonner JT (2009) The social amoebae. Princeton University Press, Princeton

    Google Scholar 

  7. Brefeld O (1869) Dictyostelium mucoroides. Ein neuer Organismus aus der Verwandtschaft der Myxomyceten. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft Frankfurt 7:85–107

    Google Scholar 

  8. Buss LW (1982) Somatic cell parasitism and the evolution of somatic tissue compatibility. Proc Natl Acad Sci USA 79:5337–5341

    Article  CAS  PubMed  Google Scholar 

  9. Cavender JC, Lakhanpal TN (1986) Distribution of dictyostelid cellular slime molds in forest soils of India. Mycologia 78:56–65

    Article  Google Scholar 

  10. Chuang JS, Rivoire O, Leibler S (2009) Simpson’s paradox in a synthetic microbial system. Science 323:272–275

    Article  CAS  PubMed  Google Scholar 

  11. Crespi BJ (2001) The evolution of social behavior in microorganisms. Trends Ecol Evol 16:178–183

    Article  PubMed  Google Scholar 

  12. Ennis HL, Dao DN, Pukatzki SU, Kessin RH (2000) Dictyostelium amoebae lacking an F-box protein form spores rather than stalk in chimeras with wild type. Proc Natl Acad Sci USA 97:3292–3297

    Article  CAS  PubMed  Google Scholar 

  13. Fiegna F, Velicer GJ (2005) Exploitative and hierarchical antagonism in a cooperative bacterium. PLoS Biol 3:e370

    Article  PubMed  Google Scholar 

  14. Filosa MF (1962) Heterocytosis in cellular slime molds. Am Naturalist XCVI(no. 887):79–92

    Google Scholar 

  15. Fisher RA (1930) The genetical theory of natural selection. Clarendon, Oxford

    Google Scholar 

  16. Fortunato A, Strassmann JE, Santorelli L, Queller DC (2003) Co-occurrence in nature of different clones of the social amoeba, Dictyostelium discoideum. Mol Ecol 12:1031–1038

    Article  CAS  PubMed  Google Scholar 

  17. Fortunato A, Queller DC, Strassmann JE (2003) A linear dominance hierarchy among clones in chimeras of the social amoeba Dictyostelium discoideum. J Evol Biol 16:438–445

    Article  CAS  PubMed  Google Scholar 

  18. Gilbert OM, Foster KR, Mehdiabadi NJ, Strassmann JE, Queller DC (2007) High relatedness maintains multicellular cooperation in a social amoeba by controlling cheater mutants. Proc Natl Acad Sci U S A 104:8913–8917

    Article  CAS  PubMed  Google Scholar 

  19. Gilbert OM, Queller DC, Strassmann JE (2009) Discovery of a large clonal patch of a social amoeba: implications for social evolution. Mol Ecol 18:1273–1281

    Article  CAS  PubMed  Google Scholar 

  20. Hagiwara H (1990) Altitudinal distribution of Dictyostelid cellular slime molds in the Langtang Valley of the central Himalayas. Reports Tottori Mycol Inst 28:191–198

    Google Scholar 

  21. Haldane JBS (1932) Causes of evolution. Longmans, Green and Co., London

    Google Scholar 

  22. Haldane JBS (1955) New Biology 19:7–26

    Google Scholar 

  23. Hamilton WD (1964) The genetical evolution of social behaviour (I and II). J Theor Biol 7:1–52

    Article  CAS  PubMed  Google Scholar 

  24. Huang HJ, Takagawa D, Weeks G, Pears C (1997) Cells at the center of Dictyostelium aggregates become spores. Dev Biol 192:564–571

    Article  CAS  PubMed  Google Scholar 

  25. Huss MJ (1989) Dispersal of cellular slime molds by two soil invertebrates. Mycologia 81:677–682

    Article  Google Scholar 

  26. Kawli TS, Kaushik S (2001) Cell fate choice and social evolution in Dictyostelium discoideum: interplay of morphogens and heterogeneities. J Biosci 26:130–133

    Article  CAS  PubMed  Google Scholar 

  27. Kaushik S, Nanjundiah V (2003) Evolutionary questions raised by cellular slime mold development. Proc Indian Natl Sci Acad B69:825–852

    Google Scholar 

  28. Kaushik S, Katoch B, Nanjundiah V (2006) Social behaviour in genetically heterogeneous groups of Dictyostelium giganteum. Behav Ecol Sociol 59:521–530

    Article  Google Scholar 

  29. Kessin RH, Gundersen GG, Zaydfudim V, Grimson M (1996) How cellular slime molds evade nematodes. Proc Natl Acad Sci U S A 93:4857–4861

    Article  CAS  PubMed  Google Scholar 

  30. Ketcham RB, Eisenberg RM (1989) Clonal diversity in populations of Polysphondylium pallidum, a cellular slime mold. Ecology 70:1425–1433

    Article  Google Scholar 

  31. Khare A, Santorelli LA, Strassmann JE, Queller DC, Kuspa A, Shaulsky G (2009) Cheater-resistance is not futile. Nature 461:980–982

    Article  CAS  PubMed  Google Scholar 

  32. Lam KM, Yamamoto R, DaMassa AJ (1995) DNA diversity among isolates of Campylobacter jejuni detected by PCR-based RAPD fingerprinting. Vet Microbiol 45:269–274

    Article  CAS  PubMed  Google Scholar 

  33. Mehdiabadi NJ, Jack CN, Farnham TT, Platt TG, Kalla SE, Shaulsky G, Queller DC, Strassmann JE (2006) Kin preference in a social microbe. Nature 442:881–882

    Article  CAS  PubMed  Google Scholar 

  34. Nanjundiah V, Saran S (1992) The determination of spatial pattern in Dictyostelium discoideum. J Biosci 17:353–394

    Article  Google Scholar 

  35. Olive LS (1975) The mycetozoans. Academic, New York

    Google Scholar 

  36. O’Malley MA (2008) ‘Everything is everywhere: but the environment selects’: ubiquitous distribution and ecological determinism in microbial biogeography. Stud Hist Phil Biol Biomed Sci 39:314–325

    Google Scholar 

  37. 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

    Article  PubMed  Google Scholar 

  38. Ozbey G, Kilic A, Ertas HB, Muz A (2004) Random amplified polymorphic DNA (RAPD) analysis of Pasteurella multocida and Manheimia haemolytica strains isolated from cattle, sheep and goats. VetMed–Czech 49:65–69

    CAS  Google Scholar 

  39. Pilcher KE, Fey P, Gaudet P, Kowal AS, Chisholm RL (2007) A reliable general purpose method for extracting genomic DNA from Dictyostelium cells. Nat Protoc 2:1325–1328

    Article  CAS  PubMed  Google Scholar 

  40. Puill-Stephan E, Willis BL, van Herwerden L, van Oppen MJ (2009) Chimerism in wild adult populations of the broadcast spawning coral Acropora millepora on the Great Barrier Reef. PLoS ONE 4:e7751

    Article  PubMed  Google Scholar 

  41. Queller DC, Ponte E, Bozzaro S, Strassmann JE (2003) Single-gene greenbeard effects in the social amoeba Dictyostelium discoideum. Science 299:105–106

    Article  CAS  PubMed  Google Scholar 

  42. Rai JN, Tewari JP (1961) Studies in cellular slime moulds from Indian soils. I. On the occurrence of Dictyostelium mucoroides Bref. and Polysphondylium violaceum. Proc Indian Acad Sci 53:1–9

    Google Scholar 

  43. Rai JN, Tewari JP (1963) Studies in cellular slime moulds from Indian soils. II. On the occurrence of an aberrant strain of Polysphondylium violaceum Bref with a discussion on the relevance of mode of branching of the sorocarp as a criterion for classifying members of Dictyosteliaceae. Proc Indian Acad Sci 58:201–206

    Google Scholar 

  44. Rai JN, Tewari JP (1963) Studies in cellular slime moulds from Indian soils. III. On the occurrence of two strains of Dictyostelium mucoroides complex, conforming to the species Dictyostelium sphaerocephalum (Oud). Saccardo and March. Proc Indian Acad Sci 58:263–266

    Google Scholar 

  45. Raper KB (1984) The Dictyostelids. Princeton University Press, Princeton

    Google Scholar 

  46. Rinkevich B (2000) A critical approach to the definition of Darwinian units of selection. Biol Bull 199:231–240

    Article  CAS  PubMed  Google Scholar 

  47. Schaap P, Winckler T, Nelson M, Alvarez-Curto E, Elgie B, Hagiwara H, Cavender J, Milano-Curto A, Rozen DE, Dingermann T, Mutzel R, Baldauf SL (2006) Molecular phylogeny and evolution of morphology in the social amoebas. Science 314:661–663

    Article  CAS  PubMed  Google Scholar 

  48. Stephenson SL, Landolt JC (1992) Vertebrates as vectors of cellular slime molds in temperate forests. Mycol Res 96:670–672

    Article  Google Scholar 

  49. Stephenson SL, Slay ME, Slay CA, Tuggle AE (2007) Cave crickets (Orthoptera: Rhaphidophoridae) as vectors of Dictyostelids (Protista: Dictyosteliida). Entomol News 118:292–295

    Article  Google Scholar 

  50. Strassmann JE, Zhu Y, Queller DC (2000) Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature 408:965–967

    Article  CAS  PubMed  Google Scholar 

  51. Sussman M (1987) Cultivation and synchronous morphogenesis of Dictyostelium under controlled experimental conditions. Methods Cell Biol 28:9–29

    Article  CAS  PubMed  Google Scholar 

  52. Suthers HB (1985) Ground-feeding migratory songbirds as cellular slime mold distribution vectors. Oecologia (Berlin) 65:526–530

    Article  Google Scholar 

  53. Swanson AR, Vadell E, Cavender JC (1999) Global distribution of forest soil dictyostelids. J Biogeography 26:133–148

    Article  Google Scholar 

  54. Vos M, Velicer GJ (2006) Genetic population structure of the soil bacterium Myxococcus xanthus at the centimeter scale. Appl Environ Microbiol 72:3615–3625

    Article  CAS  PubMed  Google Scholar 

  55. Waddell D (1982) A predatory slime mould. Nature 298:464–466

    Article  Google Scholar 

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Acknowledgments

Suggestions made by the anonymous reviewers added significantly to the analysis; we wish to express our thanks to them. We are grateful to CM Bharanaiah for his help in sample collection; R Sukumar and N Mandal for information regarding animal home ranges and feeding habits; the CES field station in Masinagudi for practical assistance at the collection site; the Director, CCMB, for extending the facilities for molecular analysis; and C. Nizak, R. Sawarkar, and J. T. Bonner for comments on the manuscript. S.S. acknowledges the award of a Senior Research Fellowship from the Council of Scientific and Industrial Research, India.

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Correspondence to Santosh Sathe or Vidyanand Nanjundiah.

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Sathe, S., Kaushik, S., Lalremruata, A. et al. Genetic Heterogeneity in Wild Isolates of Cellular Slime Mold Social Groups. Microb Ecol 60, 137–148 (2010). https://doi.org/10.1007/s00248-010-9635-4

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  • DOI: https://doi.org/10.1007/s00248-010-9635-4

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