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Population genetic structure and mating system evolution in freshwater pulmonates


Freshwater gastropods (Basommatophora and Prosobranchia) harbor a variety of mating systems. In particular, apomictic parthenogenesis in prosobranchs and self-fertilization in the hermaphrodite pulmonates may be viable alternatives to outcrossing sexuality in a number of species. The coexistence of different mating systems in extant populations provides opportunities to examine the forces directing their evolution. We review the models analyzing and predicting genetic variability in subdivided populations, with an emphasis on the effects of inbreeding. Population genetic data on freshwater pulmonates are examined in the context of selfing rates and the loss of variability under selfing. Furthermore, the genetic and demographic factors thought to influence mating system evolution are considered, and we highlight the different approaches available to estimate mating system parameters, in particular the selfing rate. Recent population biological studies on polyploid species (Bulinus truncatus, Ancylus fluviatilis) indicate that selfing is the predominant mating system. These studies have contributed to a deeper understanding of conceptual issues in the evolution of selfing rates. Throughout, we emphasize the need for further carefully designed studies.

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  1. 1

    Adams, W. T., and Allard, R. W., Effect of polyploidy on phosphoglucose isomerase diversity inFestuca microstachys. Proc. natl Acad. Sci. U.S.A.74 (1977) 1652–1656.

  2. 2

    Baker, H. G., Characteristics and modes of origin of weeds, in: The Genetics of Colonizing Species, pp. 147–172. Eds H. G. Baker and G. L. Stebbins. Academic Press, New York 1965.

  3. 3

    Bandoni, S. M., Mulvey, M., Koech, D. K., and Loker, E. S., Genetic structure of Kenyan populations ofBiomphalaria pfeifferi (Gastropoda: Planorbidae). J. mollusc. Stud.56 (1990) 383–391.

  4. 4

    Barrett, S. C. H., and Kohn, J. R., Genetic and evolutionary consequences of small population size in plants: implications for conservation, in: Genetics and Conservation of Rare Plants, pp. 3–30. Eds D. A. Falk and K. E. Holsinger. Oxford University Press, New York 1991.

  5. 5

    Baur, B., and Baur, A., Reduced reproductive compatibility inArianta arbustorum (Gastropoda) from distant populations. Heredity69 (1992) 65–72.

  6. 6

    Begun, D. J., and Aquadro, C. F., African and North American populations ofDrosophila melanogaster are very different at the DNA level. Nature365 (1993) 548–550.

  7. 7

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

  8. 8

    Bierzychudek, P., Patterns in plant parthenogenesis. Experientia41 (1985) 1255–1264.

  9. 9

    Boag, D. A., Dispersal in pond snails: potential role of waterfowl. Can. J. Zool.64 (1986) 904–909.

  10. 10

    Brown, A. H. D., Enzyme polymorphism in plant populations. Theor. Popul. Biol.15 (1979) 1–42.

  11. 11

    Brown, A. H. D., Genetic characterization of plant mating systems, in: Plant Population Genetics, Breeding, and Genetic Resources, pp. 145–162. Eds A. H. D. Brown, M. T. Clegg, A. L. Kahler and B. S. Weir. Sinauer Associates, Sunderland 1990.

  12. 12

    Brown, D. S., Freshwater Snails of Africa and their Medical Importance. 2nd edn. Taylor & Francis Ltd., London 1994.

  13. 13

    Brown, K. M., and Richardson, T. D., Genetic polymorphism in gastropods: a comparison of methods and habitat scales. Am. malac. Bull.6 (1988) 9–17.

  14. 14

    Carvalho, G. R., Evolutionary genetics of aquatic clonal invertebrates: concepts, problems and prospects, in: Genetics and Evolution of Aquatic Organisms, pp. 291–323. Ed. A. R. Beaumont. Chapman and Hall, London 1994.

  15. 15

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

  16. 16

    Charlesworth, B., Morgan, M. T., and Charlesworth, D., The effect of deleterious mutations on neutral molecular variation. Genetics134 (1993) 1289–1303.

  17. 17

    Charlesworth, D., and Charlesworth, B., Inbreeding depression and its evolutionary consequences. A. Rev. Ecol. Syst.18 (1987) 237–268.

  18. 18

    Charlesworth, D., Morgan, M. T., and Charlesworth, B., Mutation accumulation in finite outbreeding and inbreeding populations. Genet. Res. (Camb.)61 (1993) 39–56.

  19. 19

    Charnov, E. L., The Theory of Sex Allocation. Princeton University Press, Princeton 1982.

  20. 20

    Coutellec-Vreto, M.-A., Guiller, A., and Daguzan, J., Allozyme variation in some populations of the freshwater snailsLymnaea peregra, L. auricularia andL. stagnalis (Gastropoda: Pulmonata). J. mollusc. Stud.60 (1994) 393–403.

  21. 21

    Dillon, R. T. Jr., The influence of minor human disturbance on biochemical variation in a population of freshwater snails. Biol. Conserv.43 (1988) 137–144.

  22. 22

    Dillon, R. T. Jr., Evolution from transplants between genetically distinct populations of freshwater snails. Genetica76 (1988) 111–119.

  23. 23

    Dillon, R. T. Jr., and Wethington, A. R., The inheritance of albinism in a freshwater snail,Physa heterostropha. J. Hered.83 (1992) 208–210.

  24. 24

    Doums, C., Delay, B., and Jarne, P., A problem with the estimate of self-fertilization depression in the hermaphrodite freshwater snailBulinus truncatus: the effect of grouping. Evolution48 (1994) 498–504.

  25. 25

    Duncan, C. J., Reproduction, in: Pulmonates, vol. 1, Functional Anatomy and Physiology, pp. 309–365. Eds V. Fretter and J. Peake. Academic Press, London 1975.

  26. 26

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

  27. 27

    Ellstrand, N. C., and Roose, M. L., Patterns of genotypic diversity in clonal plant species. Am. J. Bot.74 (1987) 123–131.

  28. 28

    Fisher, R. A., Average excess and average effect of a gene subsitution. Ann. Eugen.11 (1941) 53–63.

  29. 29

    Frank, S. A., Coevolutionary genetics of plants and pathogens. Evol. Ecol.7 (1993) 45–75.

  30. 30

    Gaffney, P. M., Scott, T. M., Koehn, R. K., and Diehl, W. J., Interrelationships of heterozygosity, growth rate and heterozygote deficiencies in the coot clam,Mulinia lateralis. Genetics124 (1990) 687–699.

  31. 31

    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.

  32. 32

    Gillespie, J. H., The Causes of Molecular Evolution. Oxford University Press, New York 1991.

  33. 33

    Goldman, M. A., LoVerde, P. T., and Chrisman, C. L., Hybrid origin of polyploidy in freshwater snails of the genusBulinus (Mollusca: Planorbidae). Evolution37 (1983) 592–600.

  34. 34

    Hamrick, J. L., and Godt, M. J. W., Allozyme diversity in plant species, in: Plant Population Genetics, Breeding, and Genetic Resources, pp. 43–63. Eds A. H. D. Brown, M. T. Clegg, A. L. Kahler and B. S. Weir. Sinauer Associates, Sunderland 1990.

  35. 35

    Hartl, D. L., and Clark, A. G., Principles of Population Genetics. 2nd edn. Sinauer Associates, Sunderland 1989.

  36. 36

    Hauser, L., Carvalho, G. R., Hughes, R. N., and Carter, R. E., Clonal structure of the introduced freshwater snailPotamopyrgus antipodarum (Prosobranchia: Hydrobiidae), as revealed by DNA fingerprinting. Proc. R. Soc., Lond. B249 (1992) 19–25.

  37. 37

    Hebert, P. D. N., Genotypic characteristics of cyclic parthenogens and their obligately asexual derivatives, in: The Evolution of Sex and its Consequences, pp. 175–195. Ed. S. C. Stearns. Birkhäuser, Basel 1987.

  38. 38

    Hedrick, P. W., Hitchhiking: a comparison of linkage and partial selfing. Genetics94 (1980) 791–808.

  39. 39

    Hedrick, P. W., Genetic load and the mating system in homosporous ferns. Evolution41 (1987) 1282–1289.

  40. 40

    Hedrick, P. W., and Cockerham, C. C., Partial inbreeding: equilibrium heterozygosity and the heterozygosity paradox. Evolution40 (1986) 856–861.

  41. 41

    Heller, J., Hermaphroditism in molluscs. Biol. J. Linn. Soc.48 (1993) 19–42.

  42. 42

    Hughes, R. N., A Functional Biology of Clonal Animals. Chapman and Hall, London 1989.

  43. 43

    Jarne, P., and Charlesworth, D., The evolution of the selfing rate in functionally hermaphrodite plants and animals. A. Rev. Ecol. Syst.24 (1993) 441–466.

  44. 44

    Jarne, P., and Delay, B., Inbreeding depression and self-fertilization inLymnaea peregra (Gastropoda: Pulmonata). Heredity64 (1990) 169–175.

  45. 45

    Jarne, P., and Delay, B., Population genetics ofLymnaea peregra (Müller) (Gastropoda: Pulmonata) in Lake Geneva. J. mollusc. Stud.56 (1990) 317–322.

  46. 46

    Jarne, P., Delay, B., Bellec, C., Roizes, G., and Cuny, G., Analysis of mating systems in the schistosome-vector hermaphrodite snailBulinus globosus by DNA fingerprinting. Heredity68 (1992) 141–146.

  47. 47

    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.

  48. 48

    Jarne, P., Finot, L., Delay, B., and Thaler, L., Self-fertilization versus cross-fertilization in the hermaphroditic freshwater snailBulinus globosus. Evolution45 (1991) 1136–1146.

  49. 49

    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.

  50. 50

    Jarne, P., Viard, F., Delay, B., and Cuny, G., Variable microsatellites in the highly selfing snailBulinus truncatus (Basommatophora: Planorbidae). Molec. Ecol.3 (1994) 527–528.

  51. 51

    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.

  52. 52

    Johnson, M. S., Stine, O. C., and Murray, J., Reproductive compatibility despite large-scale genetic divergence inCepaea nemoralis. Heredity53 (1984) 655–665.

  53. 53

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

  54. 54

    Karl, S. A., and Avise, J. C., Balancing selection at allozyme loci in oysters: implications from nuclear RFLPs. Science256 (1992) 100–102.

  55. 55

    Kimura, M., “Stepping stone” model of population. A. Rep. natl Inst. Genet. Japan3 (1953) 62–63.

  56. 56

    Lande, R., and Schemske, D. W., The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution39 (1985) 24–40.

  57. 57

    Larambergue, M. de, Étude de l'autofécondation chez les gastéropodes pulmonés. Recherche sur l'aphallie et la fécondation chezBulinus (Isidora) contortus Michaud. Bull. biol. Fr. Belg.73 (1939) 19–231.

  58. 58

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

  59. 59

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

  60. 60

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

  61. 61

    Madsen, H., and Frandsen, F., The spread of freshwater snails including those of medical and veterinary importance. Acta trop.46 (1989) 139–146.

  62. 62

    Marti, H. P., and Tanner, M., Field observations on the influence of low water velocities on drifting ofBulinus globosus. Hydrobiologia157 (1988) 119–123.

  63. 63

    Maruyama, K., and Tachida, H., Genetic variability and geographical structure in partially selfing populations. Jap. J. Genet.67 (1992) 39–51.

  64. 64

    Maruyama, T., and Kimura, M., Genetic variability and effective population size when local extinction and recolonization of subpopulations are frequent. Proc. natl Acad. Sci. U.S.A.77 (1980) 6710–6714.

  65. 65

    McCauley, D. E., Genetic consequences of local population extinction and recolonization. Trends Ecol. Evol.6 (1991) 5–8.

  66. 66

    McCracken, G. F., and Selander, R. K., Self-fertilization and monogenic strains in natural populations of terrestrial slugs. Proc. natl Acad. Sci. U.S.A.77 (1980) 684–688.

  67. 67

    McMahon, R. F., Physiological ecology of freshwater pulmonates, in: The Mollusca, vol. 6, Ecology, pp. 359–430. Ed. W. D. Russell-Hunter. Academic Press, Orlando 1983.

  68. 68

    Michod, R. E., and Levin, B. R. (eds), The Evolution of Sex. An Examination of Current Ideas. Sinauer Associates, Sunderland 1988.

  69. 69

    Mimpfoundi, R., and Greer, G. J., Allozyme comparisons among species of theBulinus forskalii group (Gastropoda Planorbidae) in Cameroon. J. mollusc. Stud.55 (1989) 405–410.

  70. 70

    Mimpfoundi, R., and Greer, G. J., Allozyme comparisons and ploidy levels among species of theBulinus truncatus/tropicus complex (Gastropoda: Planorbidae) in Cameroon. J. mollusc. Stud.56 (1990) 63–68.

  71. 71

    Mimpfoundi, R., and Greer, G. J., Allozyme variation among populations ofBulinus forskalii (Ehrenberg, 1831) (Gastropoda: Planorbidae) in Cameroon. J. mollusc. Stud.56 (1990) 363–371.

  72. 72

    Mimpfoundi, R., and Greer, G. J., Allozyme variation among populations ofBiomphalaria camerunensis (Boettger, 1941) (Gastropoda: Planorbidae) in Cameroon. J. mollusc. Stud.56 (1990) 373–381.

  73. 73

    Mimpfoundi, R., and Greer, G. J., Allozyme variation among populations ofBiomphalaria pfeifferi (Krauss, 1848) (Gastropoda: Planorbidae) in Cameroon. J. mollusc. Stud.56 (1990) 461–467.

  74. 74

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

  75. 75

    Mulvey, M., Goater, T. M., Esch, G. W., and Crews, A. E., Genotype frequency differences inHalipegus occidualis-infected and uninfectedHelisoma anceps. J. Parasit.73 (1987) 757–761.

  76. 76

    Mulvey, M., Newman, M. C., and Woodruff, D. S., Genetic differentiation among West Indian populations of the schistosome-transmitting snailBiomphalaria glabrata. Malacologia29 (1988) 309–317.

  77. 77

    Mulvey, M., and Vrijenhoek, R. C., Multiple paternity in the hermaphroditic snail,Biomphalaria obstructa. J. Hered.72 (1981) 308–312.

  78. 78

    Mulvey, M., and Vrijenhoek, R. C., Population structure inBiomphalaria glabrata: examination of an hypothesis for the patchy distribution of susceptibility to schistosomes. Am. J. trop. Med. Hyg.31 (1982) 1195–1200.

  79. 79

    Nei, M., Analysis of gene diversity in subdivided populations. Proc. natl Acad. Sci. U.S.A.70 (1973) 3321–3323.

  80. 80

    Nei, M., Maruyama, T., and Chakraborty, R., The bottleneck effect and genetic variability in populations. Evolution29 (1975) 1–10.

  81. 81

    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. (Camb.)62 (1993) 89–100.

  82. 82

    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. mollusc. Stud.59 (1993) 125–133.

  83. 83

    Njiokou, F., Bellec, C., N'Goran, E. K., Yapi Yapi, G., Delay, B., and Jarne, P., Comparative fitness and reproductive isolation between twoBulinus globosus (Gastropoda: Planorbidae) populations. J. mollusc. Stud.58 (1992) 367–376.

  84. 84

    Njiokou, F., Delay, B., Bellec, C., N'Goran, E. K., Yapi Yapi, G., and Jarne, P., Population genetic structure of the schistosome-vector snailBulinus globosus: examining the role of genetic drift, migration and human activities. Heredity72 (1994) 488–497.

  85. 85

    Orive, M. E., Effective population size in organisms with complex life-histories. Theor. Popul. Biol.44 (1993) 316–340.

  86. 86

    Paraense, W. L., Self and cross-fertilization inAustralorbis glabratus. Mem. Inst. Oswaldo Cruz53 (1955) 285–291.

  87. 87

    Paraense, W. L., A genetic approach to the systematics of planorbid molluscs. Evolution10 (1956) 403–407.

  88. 88

    Paraense, W. L., One-sided reproductive isolation between geographically remote populations of a planorbid snail. Am. Nat.93 (1959) 93–101.

  89. 89

    Patterson, C. M., and Burch, J. B., Chromosomes of pulmonate molluscs, in: Pulmonates, vol. 2A, Systematics, Evolution and Ecology, pp. 171–217. Eds V. Fretter and J. Peake. Academic Press, London 1978.

  90. 90

    Pointier, J. P., Delay, B., Toffart, J. L., Lefèvre, M., and Romero-Alvarez, R., Life history traits of three morphs ofMelanoides tuberculata (Gastropoda: Thiaridae), an invading snail in the French West Indies. J. mollusc. Stud.58 (1992) 415–423.

  91. 91

    Pointier, J.-P., and McCullough, F., Biological control of the snail hosts ofSchistosoma mansoni in the Caribbean area usingThiara spp. Acta trop.46 (1989) 147–155.

  92. 92

    Pointier, J. P., Thaler, L., Pernot, A. F., and Delay, B., Invasion of the Martinique island by the parthenogenetic snailMelanoides tuberculata and the succession of morphs. Acta oecol.14 (1993) 33–42.

  93. 93

    Pollak, E., On the theory of partially inbreeding finite populations. I. Partial selfing. Genetics117 (1987) 353–360.

  94. 94

    Ponder, W. F.,Potamopyrgus antipodarum — a molluscan coloniser of Europe and Australia. J. mollusc. Stud.54 (1988) 271–285.

  95. 95

    Price, S. C., and Jain, S. K., Are inbreeders better colonizers? Oecologia (Berl.)49 (1981) 283–286.

  96. 96

    Quattro, J. M., Avise, J. C., and Vrijenhoek, R. C., Mode of origin and sources of genotypic diversity in triploid gynogenetic fish clones (Poeciliopsis: Poeciliidae). Genetics130 (1992) 621–628.

  97. 97

    Rees, W. J., The aerial dispersal of Mollusca. Proc. malac. Soc. Lond.36 (1965) 269–282.

  98. 98

    Ritland, K., Joint maximum likelihood estimation of genetic and mating structure using open-pollinated progenies. Biometrics42 (1986) 25–43.

  99. 99

    Ritland, K., and Jain, S., A model for the estimation of outcrossing rate and gene frequencies usingn independent loci. Heredity47 (1981) 35–52.

  100. 100

    Rollinson, D., Kane, R. A., Warlow, A., Southgate, V. R., and Gopaul, A. R., Observations on genetic diversity ofBulinus cernicus (Gastropoda: Planorbidae) from Mauritius. J. Zool. (Lond.)222 (1990) 19–26.

  101. 101

    Rollinson, D., and Wright, C. A., Population studies onBulinus cernicus from Mauritius. Malacologia25 (1984) 447–463.

  102. 102

    Russell-Hunter, W. D., Ecology of freshwater pulmonates, in: Pulmonates, vol. 2A, Systematics, Evolution and Ecology, pp. 335–383. Eds V. Fretter and J. Peake. Academic Press, London 1978.

  103. 103

    Schoen, D. J., and Brown, A. H. D., Intraspecific variation in population gene diversity and effective population size correlates with the mating system in plants. Proc. natl Acad. Sci. U.S.A.88 (1991) 4494–4497.

  104. 104

    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.

  105. 105

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

  106. 106

    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.

  107. 107

    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.

  108. 108

    Selander, R. K., and Hudson, R. O., Animal population structure under close inbreeding: the land snailRumina in southern France. Am. Nat.110 (1976) 695–718.

  109. 109

    Selander, R. K., and Kaufman, D. W., Self-fertilization and genetic population structure in a colonizing land snail. Proc. natl Acad. Sci. U.S.A.70 (1973) 1186–1190.

  110. 110

    Selander, R. K., and Ochman, H., The genetic structure of populations as illustrated by molluscs. Isozymes 10 (1983) 93–123.

  111. 111

    Slatkin, M., Gene flow and genetic drift in a species subject to frequent local extinctions. Theor. popul. Biol.12 (1977) 253–262.

  112. 112

    Slatkin, M., Gene flow in natural populations. A. Rev. Ecol. Syst.16 (1985) 393–430.

  113. 113

    Slatkin, M., Gene flow and the geographic structure of natural populations. Science236 (1987) 787–792.

  114. 114

    Städler, T., Self-fertilization versus cross-fertilization in polyploid hermaphrodites: gene silencing as a new evolutionary mechanism. Verh. dt. zool. Ges.87.1 (1994) 60.

  115. 115

    Städler, T., Loew, M., and Streit, B., Genetic evidence for low outcrossing rates in polyploid freshwater snails (Ancylus fluviatilis). Proc. R. Soc. Lond. B251 (1993) 207–213.

  116. 116

    Stearns, S. C. (ed.), The Evolution of Sex and its Consequences. Birkhäuser, Basel 1987.

  117. 117

    Streit, B., Energy partitioning and ecological plasticity in populations ofAncylus fluviatilis (Gastropoda: Basommatophora). Am. malac. Bull.3 (1985) 151–168.

  118. 118

    Streit, B., Städler, T., Kuhn, K., Loew, M., Brauer, M., and Schierwater, B., Molecular markers and evolutionary processes in hermaphrodite freshwater snails, in: Molecular Ecology and Evolution: Approaches and Applications, pp. 247–260. Eds B. Schierwater, B. Streit, G. P. Wagner and R. DeSalle. Birkhäuser, Basel 1994.

  119. 119

    Uyenoyama, M. K., Holsinger, K. E., and Waller, D. M., Ecological and genetic factors directing the evolution of self-fertilization. Oxf. Surv. evol. Biol.9 (1993) 327–381.

  120. 120

    Vrijenhoek, R. C., Ecological differentiation among clones: the frozen niche-variation model, in: Population Biology and Evolution, pp. 217–231. Eds K. Wöhrmann and V. Loeschcke. Springer Verlag, Berlin 1984.

  121. 121

    Vrijenhoek, R. C., and Graven, M. A., Population genetics of EgyptianBiomphalaria alexandrina (Gastropoda, Planorbidae). J. Hered.83 (1992) 255–261.

  122. 122

    Wade, M. J., and McCauley, D. E., Extinction and recolonization: their effects on the genetic differentiation of local populations. Evolution42 (1988) 995–1005.

  123. 123

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

  124. 124

    Waples, R. S., Temporal variation in allele frequencies: testing the right hypothesis. Evolution43 (1989) 1236–1251.

  125. 125

    Waser, N. M., Population structure, optimal outbreeding, and assortative mating in angiosperms, in: The Natural History of Inbreeding and Outbreeding, pp. 173–199. Ed. N. W. Thornhill. University of Chicago Press, Chicago and London 1993.

  126. 126

    Weir, B. S., and Cockerham, C. C., EstimatingF-statistics for the analysis of population structure. Evolution38 (1984) 1358–1370.

  127. 127

    Werth, C. R., Guttman, S. I., and Eshbaugh, W. H., Recurring origins of allopolyploid species inAsplenium. Science228 (1985) 731–733.

  128. 128

    Wethington, A. R., and Dillon, R. T. Jr., Reproductive development in the hermaphroditic freshwater snailPhysa monitored with complementing albino lines. Proc. R. Soc. Lond. B252 (1993) 109–114.

  129. 129

    Whitlock, M. C., and McCauley, D. E., Some population genetic consequences of colony formation and extinction: genetic correlations within founding groups. Evolution44 (1990) 1717–1724.

  130. 130

    Woodruff, D. S., Mulvey, M., and Yipp, M. W., Population genetics ofBiomphalaria straminea in Hong Kong. J. Hered.76 (1985) 355–360.

  131. 131

    Woolhouse, M. E. J., Passive dispersal ofBulinus globosus. Ann. Trop. Med. Parasit.82 (1988) 315–317.

  132. 132

    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.

  133. 133

    Wright, S., Evolution in Mendelian populations. Genetics16 (1931) 97–159.

  134. 134

    Wright, S., Isolation by distance. Genetics28 (1943) 114–138.

  135. 135

    Wright, S., The genetical structure of populations. Ann. Eugen.15 (1951) 323–354.

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Jarne, P., Städler, T. Population genetic structure and mating system evolution in freshwater pulmonates. Experientia 51, 482–497 (1995). https://doi.org/10.1007/BF02143200

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Key words

  • Freshwater pulmonates
  • population genetics
  • mating systems
  • selfing
  • phally
  • polyploidy
  • population structure
  • colonization
  • allozymes
  • genetic markers