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Evolution and ecological correlates of uniparental reproduction in freshwater snails

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  • Population Biology of Freshwater Invertebrates
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Abstract

We review the spatial and temporal correlates of uniparental reproduction in freshwater snails as they pertain to the ecological hypotheses for the maintenance of biparental sex. The biogeographic evidence from two species (Potamopyrgus antipodarum andBulinus truncatus) presently supports the Red Queen hypothesis that biparental reproduction is selected as a way to reduce the risk to progeny of parasite attack. Uniparental reproduction in these species is associated with low levels of infection by parasites (castrating digenetic trematodes), suggesting that parthenogenesis or self-fertilization can replace cross-fertilization when the risk of infection is low. In addition, inB. truncatus, the opportunity for cross-fertilization coincides with the season in which parasite attack is highest. In a third species (Campeloma decisum), parthenogenetic reproduction is correlated with latitude and the presence of a non-castrating trematode that may prevent cross-fertilization; these patterns suggest that parthenogenesis has been selected as a mechanism to assure reproduction. Finally, we discuss the spotty taxonomic distribution of parthenogenetic species.

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References

  1. Anderson, R. M., and May, R. M., Population biology of infectious diseases: Part I. Nature280 (1979) 361–366.

    Article  CAS  PubMed  Google Scholar 

  2. Anderson, R. M., and May, R. M., Prevalence of schistosome infections within molluscan populations: observed patterns and theoretical predictions. Parasitology79 (1979) 63–94.

    Article  CAS  PubMed  Google Scholar 

  3. Antonovics, J., and Ellstrand, N. C., Experimental studies of the evolutionary significance of sexual reproduction. I. A test of the frequency-dependent selection hypothesis. Evolution38 (1984) 103–115.

    PubMed  Google Scholar 

  4. Beadle, L. C., The Inland Waters of Tropical Africa: An Introduction To Tropical Limnology. Longman, London 1974.

    Google Scholar 

  5. Bell, G., The Masterpiece of Nature: The Evolution and Genetics of Sexuality. University of California Press, Berkeley 1982.

    Google Scholar 

  6. Bernstein, H., Byerly, H. C., Hopf, F. A., and Michod, R. E., Genetic damage, mutation, and the evolution of sex. Science229 (1985) 1277–1281.

    Article  CAS  PubMed  Google Scholar 

  7. Betterton, C., Spatiotemporal distributional patterns ofBulinus rohlfsi (Clessin),Bulinus forskalii (Ehrenberg) andBulinus senegalensis (Muller) in newly-irrigated areas in northern Nigeria. J. moll. Stud.50 (1984) 137–152.

    Google Scholar 

  8. Bremermann, H. J., Sex and polymorphism as strategies in host-pathogen interactions. J. theor. Biol.87 (1980) 671–702.

    Article  CAS  PubMed  Google Scholar 

  9. Brown, D. S., Freshwater Snails of Africa and Their Medical Importance. Taylor and Francis, London 1980.

    Google Scholar 

  10. Brown, D. S., and Wright, C. A., On a polyploid complex of freshwater snails (Planorbidae:Bulinus) in Ethiopia. J. Zool., Lond.167 (1972) 97–132.

    Article  Google Scholar 

  11. Bull, J. J., and Charnov, E. L., Enigmatic reptilian sex ratios. Evolution43 (1989) 1561–1566.

    Article  CAS  PubMed  Google Scholar 

  12. Burt, A., and Bell, G., Mammalian chiasma frequencies as a test of two theories of recombination. Nature326 (1987) 803–805.

    Article  CAS  PubMed  Google Scholar 

  13. Burt, A., and Bell, G., Seed reproduction is associated with a transient escape from parasite damage in American beech. Oikos61 (1991) 145–148.

    Article  Google Scholar 

  14. Charlesworth, B., The cost of sex in relation to mating system. J. Theor. Biol.84 (1980) 655–671.

    Article  CAS  PubMed  Google Scholar 

  15. Charnov, E. L., and Bull, J. J., When is sex environmentally determined? Nature266 (1977) 828–830.

    Article  CAS  PubMed  Google Scholar 

  16. Clay, K., Differential establishment of seedlings from chasmogamous and cleistogamous flowers in the grass,Danthonia spicata. Oecologia36 (1983) 734–741.

    Google Scholar 

  17. Clay, K., and Antonovics, J., Demographic genetics of the grassDanthonia spicata: success of progeny from chasmogamous and cleistogamous flowers. Evolution39 (1985) 205–210.

    PubMed  Google Scholar 

  18. Conover, D. O., and Heins, S. W., Adaptive variation in environmental and genetic sex determination in a fish. Nature326 (1987) 496–498.

    Article  CAS  PubMed  Google Scholar 

  19. Dybdahl, M., and Lively, C. M., Diverse endemic clones in mixed populations of a freshwater snail (Potamopyrgus antipodarum). J. evol. Biol. (1995) in press.

  20. Eernisse, D. J., Reproductive patterns in six species of Lepidochitona (Mollusca: Polyplacophora) from the Pacific Coast of North America. Biol. Bull.174 (1988) 287–302.

    Article  Google Scholar 

  21. Fisher, R. A., The Genetical Theory of Natural Selection. Oxford University Press, Oxford 1930.

    Book  Google Scholar 

  22. Fryer, S. E., Oswald, R. C., Probert, A. J., and Runham, N. W., The effect ofSchistosoma haematobium infection on the growth and fecundity of three sympatric species of Bulinid snails. J. Parasit.76 (1990) 557–563.

    Article  CAS  PubMed  Google Scholar 

  23. Gadgil, M., and Bossert, W., Life history consequences of natural selection. Am. Nat.104 (1970) 1–24.

    Article  Google Scholar 

  24. Geraerts, W. P. M., and Joosse, J., Freshwater snails (Basommatophora), in: The Mollusca, vol. 7, Reproduction, pp. 141–207. Eds A. S. Tompa, N. H. Verdonk and J. A. M. van den Biggelaar. Academic Press, Orlando 1984.

    Google Scholar 

  25. Gerritsen, J., Sex and parthenogenesis in sparse populations. Am. Nat.115 (1980) 718–742.

    Article  Google Scholar 

  26. Ghiselin, M. T., The Economy of Nature and the Evolution of Sex. University of California Press, Berkeley 1974.

    Google Scholar 

  27. Hamilton, W. D., Sex versus non-sex versus parasite. Oikos35 (1980) 282–290.

    Article  Google Scholar 

  28. Hamilton, W. D., Axelrod, R., and Ranese, R., Sexual reproduction as an adaptation to resist parasites (A Review) Proc. natl Acad. Sci. USA87 (1990) 3566–3573.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Heller, J., and Farstey, V., Sexual and parthenogenetic populations of the freshwater snailMelanoides tuberculata in Israel. Israel J. Zool.37 (1990) 75–87.

    Google Scholar 

  30. Holtsford, T. P., and Ellstrand, N. C., Inbreeding effects inClarkia tembloriensis (Onagraceae) populations with different natural outcrossing rates. Evolution44 (1990) 2031–2046.

    Article  PubMed  Google Scholar 

  31. Howard, R. S., and Lively, C. M., Parasitism, mutation accumulation and the maintenance of sex. Nature367 (1994) 554–557.

    Article  CAS  PubMed  Google Scholar 

  32. Jaenike, J., An hypothesis to account for the maintenance of sex within populations. Evol. Theory3 (1978) 191–194.

    Google Scholar 

  33. Jain, S. K., The evolution of inbreeding in plants. A. Rev. Ecol. Syst.7 (1976) 469–495.

    Article  Google Scholar 

  34. Jarne, P., Finot, L., Bellec, C., and Delay, B., Aphally versus euphally in self-fertile hermaphrodite snails from the speciesBulinus truncatus (Pulmonata: Planorbidae). Am. Nat.139 (1992) 424–432.

    Article  Google Scholar 

  35. Jarne, P., Vianey-Liaud, M., and Delay, B., Selfing and outcrossing in hermaphrodite freshwater gastropods (Basommatophora): where, when and why. Biol. J. Linn. Soc.49 (1993) 99–125.

    Article  Google Scholar 

  36. Jelnes, J. E., Experimental taxonomy ofBulinus (Gastropoda: Planorbidae): the West and North African species reconsidered, based upon an electrophoretic study of several enzymes per individual. Zool. J. Linn. Soc.87 (1986) 1–26.

    Article  Google Scholar 

  37. Johnson, S. G., Spontaneous and hybrid origins of parthenogenesis inCampeloma decisum (freshwater prosobranch snail). Heredity68 (1992) 253–261.

    Article  Google Scholar 

  38. Johnson, S. G., Parasite-induced parthenogenesis in a freshwater snail: stable, persistent patterns of parasitism. Oecologia89 (1992) 533–541

    Article  PubMed  Google Scholar 

  39. Johnson, S. G., Parasitism, reproductive assurance and the evolution of reproductive mode in a freshwater snail. Proc. R. Soc. Lond. B255 (1994) 209–213.

    Article  Google Scholar 

  40. Jokela, J., and Lively, C. M., Parasites, sex and early reproduction in a mixed population of freshwater snails. Evolution (1995) in press.

  41. Jones, C. S., Okamura, B., and Noble, L. R., Parent and larval RAPD fingerprints reveal outcrossing in freshwater bryozoans. Molec. Ecol.3 (1994) 193–199.

    Article  CAS  Google Scholar 

  42. Jordan, P., and Webbe, G., Schistosomiasis: Epidemiology, Treatment and Control. William Heinemann Medical Books Ltd., London 1982.

    Google Scholar 

  43. Kondrashov, A. S., Deleterious mutations and the evolution of sexual reproduction. Nature336 (1988) 435–440.

    Article  CAS  PubMed  Google Scholar 

  44. Lafferty, K. D., The marine snail,Cerithidea californica, matures at smaller sizes where parasitism is high. Oikos68 (1993) 3–11.

    Article  Google Scholar 

  45. Larambergue, M. de, Etude de l'autofé condation chez les gastéropodes pulmoné/s: recherches sur l'aphallie et la fécondation chezBulinus (Isidora) contortus Michaud. Bull. biol. Fr. Belg.73 (1939) 19–231.

    Google Scholar 

  46. Law, R., Bradshaw, A. D., and Putwain, P. D., Optimal life histories under age-specific predation. Am. Nat.114 (1979) 339–417.

    Article  Google Scholar 

  47. Levin, D. A., Pest pressure and recombination systems in plants. Am. Nat.109 (1975) 437–451.

    Article  Google Scholar 

  48. Lively, C. M., Evidence from a New Zealand snail for the maintenance of sex by parasitism. Nature328 (1987) 519–521.

    Article  Google Scholar 

  49. Lively, C. M., Adaptation by a parasitic trematode to local populations of its snail host. Evolution43 (1989) 1663–1671.

    Article  PubMed  Google Scholar 

  50. Lively, C. M., Parthenogenesis in a freshwater snail: reproductive assurance versus parasitic release. Evolution46 (1992) 907–913.

    Article  PubMed  Google Scholar 

  51. Lively, C. M., Craddock, C., and Vrijenhoek, R. C., Red Queen hypothesis supported by parasitism in sexual and clonal fish. Nature344 (1990) 864–866.

    Article  Google Scholar 

  52. Lively, C. M., and Johnson, S. G., Brooding and the evolution of parthenogenesis: strategy models and evidence from aquatic invertebrates. Proc. R. Soc., Lond. B256 (1994) 89–95.

    Article  CAS  Google Scholar 

  53. Lively, C. M., and Howard, R. S., Selection by parasites for clonal diversity and mixed mating. Phil. Trans. R. Soc., Lond.346 (1994) 271–281.

    Article  CAS  Google Scholar 

  54. Lloyd, D. G., Some reproductive factors affecting the selection of self-fertilization in plants. Am. Nat.113 (1979) 67–79.

    Article  Google Scholar 

  55. Lloyd, D. G., Benefits and handicaps of sexual reproduction. Evol. Biol.13 (1980) 69–111.

    Article  Google Scholar 

  56. Lynch, M., Destabilizing hybridization, general-purpose genotypes and geographic parthenogenesis. Q. Rev. Biol.59 (1984) 257–290.

    Article  Google Scholar 

  57. May, R. M., and Anderson, R. M., Population biology of infectious diseases: Part II. Nature280 (1979) 455–460.

    Article  CAS  PubMed  Google Scholar 

  58. Maynard Smith, J., The origin and maintenance of sex, in: Group Selection, pp. 163–175. Ed. G. C. Williams. Aldine Atherton, Chicago 1971.

    Google Scholar 

  59. Maynard Smith, J., The Evolution of Sex. Cambridge University Press, Cambridge 1978.

    Google Scholar 

  60. Maynard Smith, J., Evolutionary Genetics. Oxford University Press, Oxford 1989.

    Google Scholar 

  61. Michod, R. E., Evolution of life histories in response to age-specific mortality factors. Am. Nat.113 (1979) 531–550.

    Article  Google Scholar 

  62. Mitchell-Olds, T., and Waller, D. M., Relative performance of selfed and outcrossed progeny inImpatiens capensis. Evolution39 (1985) 533–544.

    Article  PubMed  Google Scholar 

  63. Mitter, C., Futuyma, D. J., Schneider, J. C., and Hare, J. D., Genetic variation and host plant relations in a parthenogenetic moth. Evolution33 (1979) 777–790.

    Article  PubMed  Google Scholar 

  64. Moritz, C., McCallum, H., Donnellan, S., and Roberts, J. D., Parasite loads in parthenogenetic and sexual lizards (Heteronotia binoei): support for the Red Queen hypothesis. Proc. R. Soc. Lond. B244 (1991) 145–149.

    Article  Google Scholar 

  65. Muller, H. J., The relation of recombination to mutational advance. Mutat. Res.1 (1964) 2–9.

    Article  Google Scholar 

  66. Nagylaki, T., A model for the evolution of self-fertilization and vegetative reproduction. J. theor. Biol.58 (1976) 55–58.

    Article  CAS  PubMed  Google Scholar 

  67. Naylor, C., Adams, J., and Greenwood, P. J., Variation in sex determination in natural populations of a shrimp. J. evol. Biol.1 (1988) 355–368.

    Article  Google Scholar 

  68. Ndifon, G. T., and Umar-Yahaya, A., Cercariae of freshwater snails in Kano, Nigeria. Niger. J. Parasit.9–11 (1988-1990) 69–75.

    Google Scholar 

  69. Nicklas, N. L., and Hoffmann, R., Apomictic parthenogenesis in a hermaphroditic terrestrial slug,Deroceras laeve (Müller). Biol. Bull.160 (1981) 123–135.

    Article  Google Scholar 

  70. Njiokou, F., Bellec, C., Berrebi, P., Delay, B., and Jarne, P., Do self-fertilization and genetic drift promote a very low genetic variability in the allotetraploidBulinus truncatus (Gastropoda: Planorbidae) populations? Genet. Res.62 (1993a) 89–100.

    Article  Google Scholar 

  71. Njiokou, F., Bellec, C., Jarne, P., Finot, L., and Delay, B., Mating system analysis using protein electrophoresis in the self-fertile hermaphrodite speciesBulinus truncatus (Gastropoda: Planorbidae). J. moll. Stud.59 (1993) 125–133.

    Article  Google Scholar 

  72. Nunney, L., The maintenance of sex by group selection. Evolution43 (1989) 245–257.

    Article  PubMed  Google Scholar 

  73. Phillips, N. R., and Lambert, D. M., Genetics ofPotamopyrgus antipodarum (Gastropoda: Prosobranchia): evidence for reproductive modes. N. Z. J. Zool.16 (1989) 435–445.

    Article  Google Scholar 

  74. Pokryszko, B. M., On the aphally in the Vertiginidae (Gastropoda: Pulmonata: Orthurethra). J. Conch.32 (1987) 365–375.

    Google Scholar 

  75. Sage, R. D., Heyneman, D., Lim, K-C., and Wilson, A. C., Wormy mice in a hybrid zone. Nature324 (1986) 60–63.

    Article  CAS  PubMed  Google Scholar 

  76. Schmitt, J., and Antonovics, J., Experimental studies of the evolutionary significance of sexual reproduction. IV. Effect of neighbor relatedness and aphid infestation on seedling performance. Evolution40 (1986) 830–836.

    Article  PubMed  Google Scholar 

  77. Schmitt, J., and Ehrhardt, D. W., A test of the sib-competition hypothesis for outcrossing advantage inImpatients capensis. Evolution41 (1987) 579–590.

    PubMed  Google Scholar 

  78. Schmitt, J., and Gamble, S. E., The effect of distance from the parental site on offspring performance and inbreeding depression inImpatiens capensis: a test of the local adaptation hypothesis. Evolution44 (1990) 2022–2030.

    PubMed  Google Scholar 

  79. Schrag, S. J., Factors Influencing Selfing and Outcrossing in the hermaphrodite,Bulinus truncatus. D. Phil. Thesis, University of Oxford 1993.

  80. Schrag, S. J., and Read, A. F., Temperature determination of male outcrossing ability in a simultaneous hermaphrodite. Evolution46 (1992) 1698–1707.

    Article  PubMed  Google Scholar 

  81. Schrag, S. J., Rollinson, D., Keymer, A. E., and Read, A. F., Heritability of male outcrossing ability in the simultaneous hermaphrodite,Bulinus truncatus (Gastropoda: Planorbidae). J. Zool., Lond.226 (1992) 311–319.

    Article  Google Scholar 

  82. Schrag, S. J., and Rollinson, D., Effects ofSchistosoma haematobium infection on reproductive success and male outcrossing ability in the simultaneous hermaphrodite,Bulinus truncatus (Gastropoda: Planorbidae). Parasitology108 (1994) 27–34.

    Article  PubMed  Google Scholar 

  83. Schrag, S. J., Mooers, A. Ø., Ndifon, G. T., and Read, A. F., Ecological correlates of male outcrossing ability in a simultaneous hermaphrodite snail. Am. Nat.143 (1994) 636–655.

    Article  Google Scholar 

  84. Schrag, S. J., Ndifon, G. T., and Read, A. F., Temperature determination of male outcrossing ability in wild populations of a simultaneous hermaphrodite snail. Ecology75 (1994) 2066–2077.

    Article  Google Scholar 

  85. Schrag, S. J., and Read, A. F., Loss of male outcrossing ability in simultaneous hermaphrodites: phylogenetic analyses of pulmonate snails. J. Zool. (1995) in press.

  86. Stearns, S. C., The selection-arena hypothesis, in: The Evolution of Sex and Its Consequences, pp. 337–349. Ed. S. C. Stearns. Birkhäuser Verlag, Basel 1987.

    Chapter  Google Scholar 

  87. Strathmann, R. R., Strathmann, M. R., and Emson, R. H., Does limited brood capacity link adult size, brooding, and simultaneous hermaphroditism? A test with the starfishAsterina phylactica. Am. Nat.123 (1984) 796–818.

    Article  Google Scholar 

  88. Templeton, A. R., The prophecies of parthenogenesis, in: Evolution and Genetics of Life Histories, pp. 75–101. Eds H. Dingle and J. P. Hegmann. Springer Verlag, New York 1982.

    Google Scholar 

  89. Tingley, G. A., and Anderson, R. M., Environmental sex determination and density-dependent population regulation in the entomogenous nematodeRomanomermis culcivorax. Parasitology92 (1986) 431–449.

    Article  Google Scholar 

  90. Uyenoyama, M. K., On the evolution of parthenogenesis: a genetic representation of the “cost of meiosis” Evolution38 (1984) 87–102.

    PubMed  Google Scholar 

  91. Vail, V. A., Comparative reproductive anatomy of three viviparid gastropods. Malacologia16 (1977) 519–540.

    Google Scholar 

  92. Wallace, C., Parthenogenesis, sex and chromosomes inPotamopyrgus. J. moll. Stud.58 (1992) 93–107.

    Article  Google Scholar 

  93. Waller, D. M., Differences in fitness between seedlings derived from cleistogamous and chasmogamous flowers inImpatiens capensis. Evolution38 (1984) 427–440.

    Article  PubMed  Google Scholar 

  94. Watson, H., Genital dimorphism inZonitoides. J. Conch.20 (1934) 33–42.

    Google Scholar 

  95. Williams, G. C., Introduction, in: Group Selection, pp. 1–15. Ed. G. C. Williams. Aldine Atherton, Chicago 1971.

    Google Scholar 

  96. Williams, G. C., Sex and Evolution. Princeton University Press, Princeton 1975.

    Google Scholar 

  97. Winterbourn, M., Rounick, J. S., and Cowie, B., Are New Zealand stream ecosystems really different? N. Z. J. mar. Freshwat. Res.15 (1981) 321–328.

    Article  Google Scholar 

  98. Woolhouse, M. E. J., and Chandiwana, S. K., Spatial and temporal heterogeneity in the population dynamics ofBulinus globosus andBiomphalaria pfeifferi and in the epidemiology of their infection with schistosomes. Parasitology98 (1989) 21–34.

    Article  PubMed  Google Scholar 

  99. Wright, C. A., and Rollinson, D., Analysis of enzymes in theBulinus tropicus/truncatus complex (Mollusca: Planorbidae). J. nat. Hist.15 (1981) 873–885.

    Article  Google Scholar 

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Johnson, S.G., Lively, C.M. & Schrag, S.J. Evolution and ecological correlates of uniparental reproduction in freshwater snails. Experientia 51, 498–509 (1995). https://doi.org/10.1007/BF02143201

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