The chastity of amoebae: Re-evaluating evidence for sex in amoeboid organisms

Proceedings of the Royal Society B: Biological Sciences

Volumn 278, Issue 1715, 2011, Pages 2081-2090

  Lahr, Daniel J G ^a   Parfrey, Laura Wegener ^a   Mitchell, Edward A D ^b   Katz, Laura A ^a,c   Lara, Enrique ^b  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b UNIVERSITY OF NEUCHÂTEL   (Switzerland)

^c SMITH COLLEGE   (United States)

Author keywords

Amoebozoa; Asexual; Evolution of sex; Karyogamy; Meiosis; Rhizaria

Indexed keywords

EVOLUTIONARY BIOLOGY; GENOMICS; LIFE CYCLE; PHYLOGENETICS; POLYPLOIDY; PROTOZOAN; SEXUALITY;

AMOEBA (LIFE CYCLE STAGE); ASEXUAL REPRODUCTION; CLASSIFICATION; EVOLUTION; GENETICS; GENOME; PHYLOGENY; PHYSIOLOGY; REPRODUCTION; REVIEW;

AMOEBA; BIOLOGICAL EVOLUTION; GENOME, PROTOZOAN; PHYLOGENY; REPRODUCTION; REPRODUCTION, ASEXUAL;

AMOEBOZOA; ANIMALIA; EMBRYOPHYTA; EUKARYOTA; FUNGI; PROTOZOA; RHIZARIA;

EID: 79959240229     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.0289     Document Type: Review

References (132)

1. Calkins, G. N. 1916 General biology of the protozoan life cycle. Am. Nat. 50, 257-270. (doi:10.1086/279539)
2. Haeckel, E. H. P. A. 1866 Generelle morphologie der organismen. Allgemeine grundzüge der organischen formen-wissenschaft, mechanisch begründet durch die von charles Darwin reformirte descendenztheorie. Berlin, Germany: G. Reimer.
3. Margulis, L. & Schwartz, K. 1988 Five Kingdoms: an illustrated guide to the phyla of life on earth, 2nd edn. New York, NY, W. H.: Freeman and Company.
4. Whittaker, R. H. 1969 New concepts of Kingdoms of organisms. Science 163, 150-160. (doi:10.1126/science.163.3863.150)
5. Corliss, J. O. 1984 The Kingdom Protista and its 45 phyla. Biosystems 17, 87-126. (doi:10.1016/0303-2647(84)90003-0)
6. Mayr, E. 1964 Systematics and the origin of species: from the viewpoint of a zoologist (with a new introduction by the author). New York, NY: Dover Publications, Inc.
7. Maynard Smith, J. 1978 The evolution of sex. Cambridge, UK: Cambridge University Press.
8. Bell, G. 1988 Sex and death in protozoa: the history of an obsession. Cambridge, UK: Cambridge University Press.
9. Adl, S. M. et al. 2005 The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 52, 399-451. (doi:10.1111/j.1550-7408.2005.00053.x)
10. Baldauf, S. L. 2003 The deep roots of eukaryotes. Science 300, 1703-1706. (doi:10.1126/science.1085544)
11. Cavalier-Smith, T. 1998 A revised six-kingdom system of life. Biol. Rev. Camb. Phil. Soc. 73, 203-266. (doi:10.1017/S0006323198005167)
12. Keeling, P. J., Burger, G., Durnford, D. G., Lang, B. F., Lee, R. W., Pearlman, R. E., Roger, A. J. & Gray, M. W. 2005 The tree of eukaryotes. Trends Ecol. Evol. 20, 670-676. (doi:10.1016/j.tree.2005.09.005)
13. Parfrey, L. W., Grant, J., Tekle, Y. I., Lasek-Nesselquist, E., Morrison, H. G., Sogin, M. L., Patterson, D. J. & Katz, L. A. 2010 Broadly sampled multigene analyses yield a well-resolved eukaryotic tree of life. Syst. Biol. 59, 518-533. (doi:10.1093/sysbio/syq037)
14. Bonner, J. T. 1998 The origins of multicellularity. Integr. Biol. Issues News Rev. 1, 27-36. (doi:10.1002/(SICI)1520-6602(1998)1:1,27::AID-INBI4.3.0.CO;2-6)
15. Dacks, J. & Roger, A. J. 1999 The first sexual lineage and the relevance of facultative sex. J. Mol. Evol. 48, 779-783. (doi:10.1007/PL00013156)
16. Schwander, T. & Crespi, B. J. 2009 Twigs on the tree of life? Neutral and selective models for integrating macro-evolutionary patterns and microevolutionary processes in the analysis of asexuality. Mol. Ecol. 18, 28-42. (doi:10.1111/j.1365-294X.2008.03992.x)
17. Kondrashov, A. S. 1997 Evolutionary genetics of life cycles. Annu. Rev. Ecol. Syst. [Review] 28, 391-435.
18. Weismann, A. 1889 Essays on heredity and kindred biological subjects. Oxford, UK: Oxford University Press.
19. Muller, H. J. 1932 Some genetic aspects of sex. Am. Nat. 66, 118-138. (doi:10.1086/280418)
20. Muller, H. J. 1964 The relation of recombination to mutational advance. Mutat. Res. Fundam. Mol. Mech. Mutagen. 1, 2-9. (doi:10.1016/0027-5107(64)90047-8)
21. Judson, O. P. & Normark, B. B. 1996 Ancient asexual scandals. Trends Ecol. Evol. 11, A41-A46. (doi:10.1016/0169-5347(96)81040-8)
22. Otto, S. P. 2009 The evolutionary enigma of sex. Am. Nat. 174(Suppl. 1), S1-S14. (doi:10.1086/599084)
23. Ross, L., Pen, I. & Shuker, D. M. 2010 Genomic conflict in scale insects: the causes and consequences of bizarre genetic systems. Biol. Rev. Camb. Phil. Soc. 85, 807-828. (doi:10.1111/j.1469-185x.2010.00127.x)
24. Parfrey, L. W., Lahr, D. J. G. & Katz, L. A. 2008 The dynamic nature of eukaryotic genomes. Mol. Biol. Evol. 25, 787-794. (doi:10.1093/molbev/msn032)
25. Dunthorn, M. & Katz, L. A. 2010 Secretive ciliates and putative asexuality in microbial eukaryotes. Trends Microbiol. 18, 183-188. (doi:10.1016/j.tim.2010.02.005)
26. Anderson, O. R. 1981 Radiolaria. Berlin, Germany: Springer Verlag.
27. Smith, R. J., Kamiya, T. & Horne, D. J. 2006 Living males of the 'ancient asexual' Darwinulidae (Ostracoda: Crustacea). Proc. R. Soc. Lond. B 273, 1569-1578. (doi:10.1098/rspb.2005.3452)
28. Croll, D. & Sanders, I. R. 2009 Recombination in Glomus intraradices, a supposed ancient asexual arbuscular mycorrhizal fungus. BMC Evol. Biol. 9, 13.
29. O'Gorman, C. M., Fuller, H. T. & Dyer, P. S. 2009 Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus. Nature 457, 471-474. (doi:10.1038/nature07528)
30. Pontecorvo, G. 1956 The parasexual cycle in Fungi. Annu. Rev. Microbiol. 10, 393-400. (doi:10.1146/annurev.mi.10.100156.002141)
31. Birky, C. W. 2010 Giardia sex? Yes, but how and how much? Trends Parasitol. 26, 70-74. (doi:10.1016/j.pt.2009.11.007)
32. Pawlowski, J. & Burki, F. 2009 Untangling the phylogeny of amoeboid protists. J. Eukaryot. Microbiol. 56, 16-25.
33. Patterson, D. J. 1999 The diversity of eukaryotes. Am. Nat. [Review]. 154, S96-S124.
34. Hurst, L. D., Hamilton, W. D. & Ladle, R. J. 1992 Covert sex. Trends Ecol. Evol. 7, 144-145.
35. Cavalier-Smith, T. 2002 The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int. J. Syst. Evol. Microbiol. 52, 297-354.
36. Bonner, J. T. 1944 A descriptive study of the development of the slime mold Dictyostelium discoideum. Am. J. Bot. 31, 175-182.
37. Bonner, J.T. 1947 Evidence for the formation of cell aggregates by chemotaxis in the development of the slime mold Dictyostelium discoideum. J. Exp. Zool. 106, 1-26.
38. Tekle, Y. T., Grant, J., Anderson, O. R., Nerad, T. A., Cole, C. C., Patterson, D. J. & Katz, L. A. 2008 Phylogenetic placement of diverse amoebae inferred from multigene analyses and assessment of clade stability within 'Amoebozoa' upon removal of varying rate classes of SSU-rDNA. Mol. Phyl. Evol. 47, 339-352.
39. Shadwick, L. L., Spiegel, F. W., Shadwick, J. D. L., Brown, M. W. & Silberman, J. D. 2009 Eumycetozoa = Amoebozoa? SSU-rDNA phylogeny of protosteloid slime molds and its significance for the amoebozoan supergroup. PLoS ONE 4, e6754.
40. Erdos, G.W., Raper, K. B. & Vogen, L. K. 1973 Mating types and macrocyst formation in Dictyostelium discoideum. Proc. Natl Acad. Sci. USA 70, 1828-1830.
41. Erdos, G. W., Raper, K. B. & Vogen, L. K. 1975 Sexuality in cellular slime mold Dictyostelium giganteum. Proc. Natl Acad. Sci. USA 72, 970-973.
42. Macinnes, M. A. & Francis, D. 1974 Meiosis in Dictyostelium mucoroides. Nature 251, 321-324. (doi:10.1038/251321a0)
43. Fiore-Donno, A. M., Berney, C., Pawlowski, J. & Baldauf, S. A. 2005 Higher-order phylogeny of plasmodial slime molds (Myxogastria) based on elongation factor 1-a and small subunit rRNA gene sequences. J. Euk. Microbiol. 52, 201-210.
44. Martin, G. W. & Alexopoulos, C. J. 1969 The myxomycetes. Iowa City, IA: University of Iowa Press.
45. Collins, O. R. & Tang, H. C. 1977 New mating types in Physarum polycephalum. Mycologia 69, 421-423.
46. Michel, R., Wylezich, C., Hauroder, B. & Smirnov, A. 2006 Phylogenetic position and notes on the ultrastructure of Sappinia diploidea (Thecamoebidae). Protistology 4, 319-325.
47. Goodfellow, L. P., Belcher, J. H. & Page, F. C. 1974 A light- and electron-microscopical study of Sappinia diploidea, a sexual amoeba. Protistologica 2, 207-216.
48. Wenrich, D. H. 1954 Sex in Protozoa: a comparative review. In Sex in microorganisms: a symposium (ed. D. H. Wenrich), p. 362. Washington, DC: AAAS.
49. Brown, M. W., Spiegel, F. W. & Silberman, J. D. 2007 Amoeba at attention: phylogenetic affinity of Sappinia pedata. J. Eukaryot. Microbiol. 54, 511-519.
50. Brown, M. W., Spiegel, F. W. & Silberman, J. D. 2009 Phylogeny of the 'forgotten' cellular slime mold, Fonticula alba, reveals a key evolutionary branch within Opisthokonta. Mol. Biol. Evol. 26, 2699-2709.
51. Spiegel, F. W. & Olive, L. S. 1978 New evidence for validity of Copromyxa protea. Mycologia 70, 843-847.
52. Mignot, J.-P. & Raikov, I. B. 1992 Evidence for meiosis in the testate amoeba Arcella. J. Eurkaryot. Microbiol. 39, 287-289.
53. Moses, M. J. 1969 Structure and function of the synaptonemal complex. Genetics 61(Suppl. 1), 41-51.
54. Lahr, D. J., Nguyen, T. B., Barbero, E. & Katz, L. A. 2011 Evolution of the actin gene family in testate lobose amoebae (Arcellinida) is characterized by 2 distinct clades of paralogs and recent independent expansions. Mol. Biol. Evol. 28, 223-236. (doi:10.1093/molbev/msq200)
55. Lüftenegger, G. & Foissner, W. 1991 Morphology and biometry of twelve soil testate amoebae (Protozoa, Rhizopoda) from Australia, Africa, and Austria. Bull. Br. Mus. Nat. Hist. (Zoology) 57, 1-16.
56. Meisterfeld, R. 2002 Order Arcellinida Kent, 1880. In The illustrated guide to the Protozoa (eds J. J. Lee, G. F. Leedale & P. Bradbury), pp. 827-860, 2nd edn. Lawrence, KS: Allen Press.
57. Dangeard, L. 1937 Memoirs sur le Difflugia globulosa Dujardin. Le Botaniste 28, 229-274.
58. Rhumbler, H. 1898 Zelleib-, schalen-, und kernverschmelzungen bei den rhizopoden und deren wahrscheinliche beziehungen zu phylogenetischen vorstufen der metazoenbefruchtung. 2. Biologisches Centralblatt 18, 33-38.
59. Heger, T. J., Mitchell, E. A. D., Ledeganck, P., Vincke, S., Van de Vijver, B. & Beyens, L. 2009 The curse of taxonomic uncertainty in biogeographical studies of free-living terrestrial protists: a case study of testate amoebae from Amsterdam island. J. Biogeogr. 36, 1551-1560.
60. Lahr, D. J. G. & Lopes, S. 2009 Evaluating the taxonomic identity in four species of the lobose testate amoebae genus Arcella Ehrenberg, 1832. Acta Protozoolog. 48, 127-142.
61. Seravin, L. N. & Goodkov, A. V. 1984 Possible forms of agamic genetic interactions in protists andways of establishment of the sexual process. Tsitologiya 26, 1224-1236.
62. Seravin, L. N. & Goodkov, A. V. 1984 The main types and forms of agamic cell fusion in Protozoa. Tsitologiya 26, 123-131.
63. Smirnov, A. V. & Goodkov, A. V. 1999 An illustrated list of basic morphotypes of Gymnamoebia (Rhizopoda, Lobosea). Protistology 1, 20-29.
64. Dykova, I., Fiala, I., Peckova, H. & Dvorakova, H. 2008 Phylogeny of Flabellulidae (Amoebozoa: Leptomyxida) inferred from SSU rDNA sequences of the type strain of Flabellula citata Schaeffer, 1926 and newly isolated strains of marine amoebae. Folia Parasitol. 55, 256-264.
65. Sargeaunt, P. G., Jackson, T. F., Wiffen, S. R. & Bhojnani, R. 1988 Biological evidence of genetic exchange in Entamoeba histolytica. Trans. R. Soc. Trop. Med. Hyg. 82, 862-867.
66. Blanc, D., Nicholls, R. & Sargeaunt, P. G. 1989 Experimental production of new zymodemes of Entamoeba histolytica supports the hypothesis of genetic exchange. Trans. R. Soc. Trop. Med. Hyg. 83, 787-790.
67. Loftus, B. et al. 2005 The genome of the protist parasite Entamoeba histolytica. Nature 433, 865-868.
68. Ramesh, M. A., Malik, S.-B. & Longsdon, J. M. 2005 A phylogenomic inventory of meiotic genes: evidence for sex in Giardia and an early eukaryotic origin of meiosis. Curr. Biol. 15, 185-191.
69. Stanley, J. S. L. 2005 The Entamoeba histolytica genome: something old, something new, something borrowed and sex too? Trends Parasitol. 21, 451.
70. Angell, R.W. 1976 Observations on Trichosphaerium platyxyrum sp. n. J. Protozool. 23, 357-364.
71. Schuster, F. L. 1976 Fine structure of the schizont stage of the testate marine amoeba, Trichosphaerium sp. J. Euk. Microbiol. 23, 86-93.
72. Schaudinn, F. R. 1899 Untersuchungen uber den generationswechsel von Trichosphaerium sieboldi. Sch. Abh. Konigl. Preuss. Akd. Wiss. Berlin 1(Suppl.), 1-93.
73. Whatley, J. & Chapman-Andresen, C. 1990 Phylum Karyoblastea. In Handbook of Protoctista (eds L. Margulis, J. O. Corliss, M. Melkonian & D. Chapman), pp. 167-185. Boston, MA: Jones and Bartlett Publishers.
74. Ekelund, F. & Patterson, D. J. 1997 Some heterotrophic flagellates from a cultivated soil in Australia. Arch. Protistenk. 148, 461-478.
75. Foissner, W. 1991 Diversity and ecology of soil flagellates. In The biology of free-living heterotrophic flagellates (eds D. J. Patterson & J. Larsen), pp. 93-112. Oxford, UK: Clarendon Press.
76. Bass, D., Chao, E. E. Y., Nikolaev, S., Yabuki, A., Ishida, K. I., Berney, C., Pakzad, U., Wylezich, C. & Cavalier-Smith, T. 2009 Phylogeny of novel naked filose and reticulose Cercozoa: Granofilosea cl. n. and Proteomyxidea revised. Protist 160, 75-109.
77. Bowser, S. S. & Travis, J. L. 2002 Reticulopodia: structural and behavioral basis for the suprageneric placement of granuloreticulosan protists. J. Foraminiferal Res. 32, 440-447.
78. Goldstein, S. T. 1999 Foraminifera: a biological overview. In Modern foraminifera (ed. B. K. Sen Gupta), pp. 37-56. Dordrecht, The Netherlands: Kluwer.
79. Arnold, Z. M. 1972 Observations on the biology of the protozoan Gromia oviformis Dujardin. Berkley, CA: University of California Press.
80. Matz, M. V., Frank, T. M., Marshall, N. J., Widder, E. A. & Johnsen, S. 2008 Giant deep-sea protist produces bilaterian-like traces. Curr. Biol. 18, 1849-1854. (doi:10.1016/j.cub.2008.10.028)
81. Pina-Ochoa, E. et al. 2010 Widespread occurrence of nitrate storage and denitrification among Foraminifera and Gromiida. Proc. Natl Acad. Sci. USA 107, 1148-1153. (doi:10.1073/pnas.0908440107)
82. Tolonen, K., Warner, B. G. & Vasander, H. 1992 Ecology of testaceans (Protozoa, Rhizopoda) in mires in southern Finland. I. Autecology. Arch. Protistenk. 142, 119-138.
83. Mitchell, E. A. D., Charman, D. J. & Warner, B. G. 2008 Testate amoebae analysis in ecological and paleoecological studies of wetlands: past, present and future. Biodivers. Conserv. 17, 2115-2137. (doi:10.1007/s10531-007-9221-3)
84. Wylezich, C., Meisterfeld, R., Meisterfeld, S. & Schlegel, M. 2002 Phylogenetic analyses of small subunit ribosomal RNA coding regions reveal a monophyletic lineage of euglyphid testate amoebae (Order Euglyphida). J. Eukaryot. Microbiol. 49, 108-118. (doi:10.1111/j.1550-7408.2002.tb00352.x)
85. Lara, E., Heger, T. J., Mitchell, E. A. D., Meisterfeld, R. & Ekelund, F. 2007 SSU rRNA reveals a sequential increase in shell complexity among the euglyphid testate amoebae (Rhizaria: Euglyphida). Protist 158, 229-237. (doi:10.1016/j.protis.2006.11.006)
86. Heger, T. J., Mitchell, E. A. D., Todorov, M., Golemansky, V., Lara, E., Leander, B. S. & Pawlowski, J. 2010 Molecular phylogeny of euglyphid testate amoebae (Cercozoa: Euglyphida) suggests transitions between marine supralittoral and freshwater/terrestrial environments are infrequent. Mol. Phylogenet. Evol. 55, 113-122. (doi:10.1016/j.ympev.2009.11.023)
87. Reukauf, E. 1912 Zur encystierung von Euglypha alveolata. Zoolog. Anzeiger 39, 372-375.
88. Penard, E. 1902 Faune rhizopodique du bassin du léman. Geneva, Switzerland: Henry Kündig.
89. Awerintzew, S. 1906 Die süsswasser Rhizopoden. I and II. Trudui S.-Peter. Oscch 36, 351.
90. Blochmann, F. 1887 Zur kenntniss der fortpflanzung von Euglypha alveolata Dujardin. Morphologische Jahrbuch 13, 173-183.
91. Cash, J., Wailes, G. H. & Hopkinson, J. 1915 The British freshwater Rhizopoda and Heliozoa: Rhizopoda part 3. London, UK: The Ray Society.
92. Chardez, D. 1965 On the particular mode and little understood reproduction in aquatic thecamoebae (Rhizopoda; Testacea.). Bull. Inst. Agron. Sta. Rech. Gembloux 33, 26-34.
93. Valkanov, A. 1962 Euglyphella delicatula n. g., n. sp. (Rhizopoda Testacea) und ihre kopulation. Dokl. Bolgarkoi Akad. Nauk 15, 207-209.
94. Schonborn, W. & Peschke, T. 1990 Evolutionary studies on the Assulina-Valkanovia complex (Rhizopoda, Testaceafilosia) in sphagnum and soil. Biol. Fertil. Soils 9, 95-100. (doi:10.1007/BF00335790)
95. Valkanov, A. 1962 Über die kopulation der testaceen (Rhizopoda Testacea). Dokl. Bolgarskoi Akad. Nauk 15, 305-308.
96. Iudina, T. A. & Sukhanova, K. M. 2000 The testate amoeba Corythion delamarei: cell biology and life cycle. Tsitologiya 42, 613-623.
97. Sukhanova, I. N. & Cheban, E. A. 1990 Heterotrophic phytoplankton of the Black-Sea in the early spring period of the phytocen development. Okeanologiya 30, 979-986.
98. Cavalier-Smith, T. & Chao, E. E. Y. 2003 Phylogeny and classification of phylum Cercozoa (protozoa). Protist 154, 341-358. (doi:10.1078/143446103322454112)
99. Archibald, J. M. 2009 The puzzle of plastid evolution. Curr. Biol. CB 19, R81-R88. (doi:10.1016/j.cub.2008.11.067)
100. Grell, K. G. 1990 Indications of sexual reproduction in the plasmodial protist Chlorarachnion reptans Geitler. Zeitsch. Naturforsch. C J. Biosci. 45, 112-114.
101. Beutlich, A. & Schnetter, R. 1993 The life-cycle of Cryptochlora perforans (Chlorarachniophyta). Bot. Acta 106, 441-447.
102. Braselton, J. P. 2002 Phylum Plasmodiophora (Plasmodiophoromycota). In The illustrated guide to the Protozoa (eds J. J. Lee, G. F. Leedale & P. C. Bradbury), 2nd edn, pp. 1342-1345. Lawrence, KS: Society of Protozoologists.
103. Raikov, I. B. 1982 The protozoan nucleus: morphology and evolution. Wien, Austria: Springer-Verlag.
104. Grell, K. G. & Ruthmann, A. 1964 Uber die karyologie des radiolars Aulacantha scolymantha und die feinstruktur seiner chromosomen. Chromosoma 15, 185-211 (doi:10.1007/BF00285729)
105. Febvre, C., Febvre, J. & Michaels, A. F. 2002 Class Acantharea. In The illustrated guide to the Protozoa (eds J. J. Lee, G. F. Leedale & P. C. Bradbury), 2nd edn, pp. 1055-1084. Lawrence, KS: Society of Protozoologists.
106. Anderson, O. R., Nigrini, C., Boltovskoy, D., Takahashi, K. & Swanberg, N. R. 2002 Class Polycystina. In The illustrated guide to the protozoa (eds J. J. Lee, G. F. Leedale & P. C. Bradbury), 2nd edn, pp. 994-1022. Lawrence, KS: Society of Protozoologists.
107. Woodcock, H. M. & Lapage, G. 1915 Observations on the life-cycle of a new flagellate, Helkesimastix faecicola, n. g., n. sp.: together with remarks on the question of syngamy in the trypanosomes. Proc. R. Soc. Lond. B 88, 353-370. (doi:10.1098/rspb.1915.0001)
108. Woodcock, H. M. 1916 Observations on coprozoic flagellates. Phil. Trans. R. Soc. Lond. B 207, 375-412. (doi:10.1098/rstb.1916.0008)
109. Shirkina, N. I. 1987 Biological features in some flagellates of the genus Cercomonas (Rhizomastigida, Cercomonadidae). Zoolog. Z. 66, 485-489.
110. Karpov, S. A. 1997 Cercomonads and their relationship to the myxomycetes. Arch. Protistenkunde 148, 297-307.
111. Hulsmann, N. 1993 Lateromyxa gallica n. g. n. sp. (Vampyrellidae)-a filopodial ameboid protist with a novel life-cycle and conspicuous ultrastructural characters. J. Eukaryot. Microbiol. 40, 141-149. (doi:10.1111/j.1550-7408.1993.tb04894.x)
112. Ropstorf, P., Hulsmann, N. & Hausmann, K. 1993 Karyological investigations on the vampyrellid filose amoeba Lateromyxa gallica Hulsmann 1993. Eur. J. Protistol. 29, 302-310.
113. Nikolaev, S. I., Berney, C., Fahrni, J. F., Bolivar, I., Polet, S., Mylnikov, A. P., Aleshin, V. V., Petrov, N. B. & Pawlowski, J. 2004 The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes. Proc. Natl Acad. Sci. USA 101, 8066-8071. (doi:10.1073/pnas.0308602101)
114. Mikrjukov, K. A. & Patterson, D. J. 2001 Taxonomy and phylogeny of Heliozoa. III. Actinophryids. Acta Protozoolog. 40, 3-25.
115. Simpson, A. G. B. 2003 Cytoskeletal organization, phylogenetic affinities and systematics in the contentious taxon Excavata (Eukaryota). Int. J. Syst. Evol. Microbiol. 53, 1759-1777. (doi:10.1099/ijs.0.02578-0)
116. Droop, M. R. 1961 Evidence for a sexual phase in lifecycle of an amoeba. Nature 192, 281. (doi:10.1038/192281a0)
117. Fritz-Laylin, L. K. et al. 2010 The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140, 631-642. (doi:10.1016/j.cell.2010.01.032)
118. Perkins, F. O. & Amon, J. P. 1969 Zoosporulation in Labyrinthula sp.-an electron microscope study. J. Protozoolog. 16, 235-257.
119. Moens, P. B. & Perkins, F. O. 1969 Chromosome number of a small protist-accurate determination. Science 166, 1289-1291.
120. Sumbali, G. 2005 The fungi (ed. B. M. Johri). Middlesex, UK: Alpha Science International.
121. Hamilton, W. D. 2001 Narrow roads of gene land, vol. 2: the evolution of sex. Oxford, UK: Oxford University Press.
122. Felsenstein, J. 1974 The evolutionary advantage of recombination. Genetics 78, 737-756.
123. Porter, S. M. & Knoll, A. H. 2000 Testate amoebae in the neoproterozoic era: evidence from vase-shaped microfossils in the Chuar group, Grand Canyon. Paleobiology 26, 360-385. (doi:10.1666/0094-8373(2000)026,0360:TAITNE.2.0.CO;2)
124. Sen Gupta, B. K. 1999 Introduction to modern Foraminifera. In Modern Foraminifera (ed. B. K. Sen Gupta), pp. 1-6. Dordrecht, The Netherlands: Kluwer.
125. Gladyshev, E. A. & Arkhipova, I. R. 2010 Genome structure of bdelloid rotifers: shaped by asexuality or desiccation? J. Hered. 101(Suppl. 1), S85-S93. (doi:10.1093/jhered/esq008)
126. Lohia, A. 2003 The cell cycle of Entamoeba histolytica. Mol. Cell. Biochem. 253, 217-222. (doi:10.1023/A:1026055631421)
127. Török, J. K., Pollák, B., Heéger, Z., Csikós, G. & Márialigeti, K. 2008 First evidence of bacterial endocytobionts in the lobose testate amoeba Arcella (Amoebozoa, Arcellinida). Protistology 5, 303-312.
128. Corsaro, D. & Venditti, D. 2009 Detection of chlamydiae from freshwater environments by PCR, amoeba coculture and mixed coculture. Res. Microbiol. 160, 547-552. (doi:10.1016/j.resmic.2009.08.001)
129. Jeon, K. W. 2004 Genetic and physiological interactions in the amoeba-bacteria symbiosis. J. Eukaryot. Microbiol. 51, 502-508. (doi:10.1111/j.1550-7408.2004.tb00277.x)
130. Greub, G. & Raoult, D. 2004 Microorganisms resistant to free-living amoebae. Clin. Microbiol. Rev. 17, 413-433. (doi:10.1128/CMR.17.2.413-433.2004)
131. Boyer, M. et al. 2009 Giant marseillevirus highlights the role of amoebae as a melting pot in emergence of chimeric microorganisms. Proc. Natl Acad. Sci. USA 106, 21848-21853. (doi:10.1073/pnas.0911354106)
132. Moreira, D. & Brochier-Armanet, C. 2008 Giant viruses, giant chimeras: the multiple evolutionary histories of mimivirus genes. BMC Evol. Biol. 8, 12. (doi:10.1186/1471-2148-8-12)