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.
Similar content being viewed by others
References
Agnihothrudu V (1956) Occurrence of Dictyosteliaceae in the rhizosphere of plants in Southern India. Experientia 12:149–150
Atzmony D, Zahavi A, Nanjundiah V (1997) Altruistic behaviour in Dictyostelium discoideum explained on the basis of individual selection. Curr Sci 72:142–145
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
Bonner JT (1967) The cellular slime molds. Princeton University Press, Princeton
Bonner JT (1982) Evolutionary strategies and developmental constraints in the cellular slime molds. Am Naturalist 119:530–552
Bonner JT (2009) The social amoebae. Princeton University Press, Princeton
Brefeld O (1869) Dictyostelium mucoroides. Ein neuer Organismus aus der Verwandtschaft der Myxomyceten. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft Frankfurt 7:85–107
Buss LW (1982) Somatic cell parasitism and the evolution of somatic tissue compatibility. Proc Natl Acad Sci USA 79:5337–5341
Cavender JC, Lakhanpal TN (1986) Distribution of dictyostelid cellular slime molds in forest soils of India. Mycologia 78:56–65
Chuang JS, Rivoire O, Leibler S (2009) Simpson’s paradox in a synthetic microbial system. Science 323:272–275
Crespi BJ (2001) The evolution of social behavior in microorganisms. Trends Ecol Evol 16:178–183
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
Fiegna F, Velicer GJ (2005) Exploitative and hierarchical antagonism in a cooperative bacterium. PLoS Biol 3:e370
Filosa MF (1962) Heterocytosis in cellular slime molds. Am Naturalist XCVI(no. 887):79–92
Fisher RA (1930) The genetical theory of natural selection. Clarendon, Oxford
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
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
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
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
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
Haldane JBS (1932) Causes of evolution. Longmans, Green and Co., London
Haldane JBS (1955) New Biology 19:7–26
Hamilton WD (1964) The genetical evolution of social behaviour (I and II). J Theor Biol 7:1–52
Huang HJ, Takagawa D, Weeks G, Pears C (1997) Cells at the center of Dictyostelium aggregates become spores. Dev Biol 192:564–571
Huss MJ (1989) Dispersal of cellular slime molds by two soil invertebrates. Mycologia 81:677–682
Kawli TS, Kaushik S (2001) Cell fate choice and social evolution in Dictyostelium discoideum: interplay of morphogens and heterogeneities. J Biosci 26:130–133
Kaushik S, Nanjundiah V (2003) Evolutionary questions raised by cellular slime mold development. Proc Indian Natl Sci Acad B69:825–852
Kaushik S, Katoch B, Nanjundiah V (2006) Social behaviour in genetically heterogeneous groups of Dictyostelium giganteum. Behav Ecol Sociol 59:521–530
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
Ketcham RB, Eisenberg RM (1989) Clonal diversity in populations of Polysphondylium pallidum, a cellular slime mold. Ecology 70:1425–1433
Khare A, Santorelli LA, Strassmann JE, Queller DC, Kuspa A, Shaulsky G (2009) Cheater-resistance is not futile. Nature 461:980–982
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
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
Nanjundiah V, Saran S (1992) The determination of spatial pattern in Dictyostelium discoideum. J Biosci 17:353–394
Olive LS (1975) The mycetozoans. Academic, New York
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
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
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
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
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
Queller DC, Ponte E, Bozzaro S, Strassmann JE (2003) Single-gene greenbeard effects in the social amoeba Dictyostelium discoideum. Science 299:105–106
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
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
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
Raper KB (1984) The Dictyostelids. Princeton University Press, Princeton
Rinkevich B (2000) A critical approach to the definition of Darwinian units of selection. Biol Bull 199:231–240
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
Stephenson SL, Landolt JC (1992) Vertebrates as vectors of cellular slime molds in temperate forests. Mycol Res 96:670–672
Stephenson SL, Slay ME, Slay CA, Tuggle AE (2007) Cave crickets (Orthoptera: Rhaphidophoridae) as vectors of Dictyostelids (Protista: Dictyosteliida). Entomol News 118:292–295
Strassmann JE, Zhu Y, Queller DC (2000) Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature 408:965–967
Sussman M (1987) Cultivation and synchronous morphogenesis of Dictyostelium under controlled experimental conditions. Methods Cell Biol 28:9–29
Suthers HB (1985) Ground-feeding migratory songbirds as cellular slime mold distribution vectors. Oecologia (Berlin) 65:526–530
Swanson AR, Vadell E, Cavender JC (1999) Global distribution of forest soil dictyostelids. J Biogeography 26:133–148
Vos M, Velicer GJ (2006) Genetic population structure of the soil bacterium Myxococcus xanthus at the centimeter scale. Appl Environ Microbiol 72:3615–3625
Waddell D (1982) A predatory slime mould. Nature 298:464–466
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.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-010-9635-4