Evolutionary implications of a high selfing rate in the freshwater snail Lymnaea truncatula

Evolution

Volumn 57, Issue 10, 2003, Pages 2303-2314

  Trouve S ^a   Degen, L ^a   Renaud, F ^b   Goudet, J ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

Gastropoda; Habitat quality; Inbreeding depression; Mating system; Microsatellites; Parasitism; Selfing

Indexed keywords

AUTOGAMY; EVOLUTION; HERMAPHRODITE; INBREEDING DEPRESSION; REPRODUCTIVE STRATEGY;

ANIMALIA; BASOMMATOPHORA; FOSSARIA TRUNCATULA; GASTROPODA; INVERTEBRATA; LYMNAEA; LYMNAEA TRUNCATULA; LYMNAEIDAE;

EID: 0242416059     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1554/02-452     Document Type: Article

References (111)

1. Agrawal, A. F., and C. M. Lively. 2001. Parasites and the evolution of self-fertilization. Evolution 55:869-879.
2. Ågren, J., and D. W. Schemske. 1993. Outcrossing rate and inbreeding depression in two annual monoecious herbs, Begonia hirsuta and Begonia semiovata. Evolution 47:125-135.
3. Ayala, F. J. 1998. Is sex better? Parasites say "no." Proc. Natl. Acad. Sci. USA 95:3346-3348.
4. Berry, A. J., J. W. Ajioka, and M. Kreitman. 1991. Lack of polymorphism on the Drosophila fourth chromosome resulting from selection. Genetics 129:1111-1118.
5. Bilton, D. T., J. R. Freeland, and B. Okamura. 2001. Dispersal in freshwater invertebrates. Annu. Rev. Ecol. Syst. 32:159-181.
6. Bishop, J. D. D., and J. S. Ryland. 1993. Enzyme electrophoretic evidence for the prevalence of outcrossing in the hermaphroditic brooding ascidian Dendrodoa grossularia (Chordata, Urochordata). J. Exp. Mar. Biol. Ecol. 168:149-165.
7. Boag, D. A. 1986. Dispersal in pond snails: potential role of waterfowl. Can. J. Zool. 64:904-909.
8. Bonnell, M. L., and R. K. Selander. 1974. Elephant seals: genetic variation and near extinction. Science 184:908-909.
9. Byers, D. L., and D. M. Waller. 1999. Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annu. Rev. Ecol. Syst. 30:479-513.
10. Cassinello, J., M. Gomendio, and E. R. S. Roldan. 2001. Relationship between coefficient of inbreeding and parasite burden in endangered gazelles. Conserv. Biol. 15:1171-1174.
11. Charlesworth, B. 1980. The cost of sex in relation to mating system. J. Theor. Biol. 84:655-671.
12. Charlesworth, B., and D. Charlesworth. 1999. The genetic basis of inbreeding depression. Genet. Res. 74:329-340.
13. Charlesworth, B., M. T. Morgan, and D. Charlesworth. 1993. The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289-1303.
14. Charlesworth, D., and B. Charlesworth. 1987. Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst. 18:237-268.
15. _. 1990. Inbreeding depression with heterozygote advantage and its effect on selection for modifiers changing the outcrossing rate. Evolution 44:870-888.
16. Cohen, C. S. 1996. The effects of contrasting modes of fertilization on levels of inbreeding in the marine invertebrate genus Corella. Evolution 50:1896-1907.
17. Coltman, D. W., J. G. Pilkington, J. A. Smith, and J. M. Pemberton. 1999. Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evolution 53:1259-1267.
18. Coutellec-Vreto, M. A., A. Guiller, and J. Daguzan. 1994. Allozyme variation in some populations of the freshwater snails Lymnaea peregra, L. auricularia and L. stagnalis (Gastropoda: Pulmonata). J. Molluscan Stud. 60:393-403.
19. Coutellec-Vreto, M. A., L. Madec, and A. Guiller. 1997. Selfing and biparental inbreeding: a mating system analysis in Lymnaea peregra (Gastropoda: Lymnaeidae). Heredity 79:277-285.
20. Coutellec-Vreto, M.-A., P. Jarne, A. Guiller, L. Madec, and J. Daguzan. 1998. Inbreeding and fitness in the freshwater snail Lymnaea peregra: an evaluation over two generations of self-fertilization. Evolution 52:1635-1647.
21. Crow, J. F. 1999a. Dominance and overdominance. Pp. 49-58 in J. G. Coors and S. Pandey, eds. Genetics and exploitation of heterosis in crops. American Soceity of Agronomy, Madison, WI.
22. _. 1999b. The rise and fall of overdominance. Plant Breed. Rev. 17:225-257.
23. Darwin, C. 1876. The effects of cross and self-fertilization in the vegetable kingdom. J. Murray, London.
24. Dillon, R. T., Jr. 2000. The ecology of freshwater molluscs. Cambridge Univ. Press, Cambridge, U.K.
25. Doums, C., F. Viard, A.-F. Pernot, B. Delay, and P. Jarne. 1996. Inbreeding depression, neutral polymorphism, and copulatory behavior in freshwater snails: a self-fertilization syndrome. Evolution 50:1908-1918.
26. El Mousadik, A., and R. J. Petit. 1996. High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor. Appl. Genet. 92:832-839.
27. Fisher, R. A. 1941. Average excess and average effect of a gene substitution. Ann. Eugen. 11:53-63.
28. Flor, H. H. 1956. The complementary genetic system in flax and flax rust. Adv. Genet. 8:29-54.
29. Franceschinelli, E. V., and K. S. Bawa. 2000. The effect of ecological factors on the mating system of a South American shrub species (Helicteres brevispira). Heredity 84:116-123.
30. Frank, S. A. 1993. Specificity versus detectable polymorphism in host-parasite genetics. Proc. R. Soc. Lond. B 254:191-197.
31. _. 1994. Recognition and polymorphism in host-parasite genetics. Philos. Trans. R. Soc. B 346:283-293.
32. Ghiselin, M. T. 1969. The evolution of hermaphroditism among animals. Q. Rev. Biol. 44:189-208.
33. _. 1974. The economy of nature and the evolution of sex. Univ. of California Press, Berkeley, CA.
34. Giles, B. E., and J. Goudet. 1997. Genetic differentiation in Silene dioica metapopulations: estimation of spatiotemporal effects in a successional plant species. Am. Nat. 149:507-526.
35. Goudet, J. 2001. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available via http: //www.unil.ch/izea/ softwares/fstat.html.
36. Goudet, J., M. Raymond, T. De Meeus, and F. Rousset. 1996. Testing differentiation in diploid populations. Genetics 144:1933-1940.
37. Hamilton, W. D., R. Axelrod, and R. Tanese. 1990. Sexual reproduction as an adaptation to resist parasites (a review). Proc. Natl. Acad. Sci. USA 87:3566-3573.
38. Hamrick, J. L., and M. J. Godt. 1990. Allozyme diversity in plant species. Pp. 43-63 in A. H. D. Brown, M. T. Clegg, A. L. Kahler, and B. S. Weir, eds. Plant population genetics, breeding and genetic resources. Sinauer Associates, Sunderland, MA.
39. Hartl, D. L., and A. G. Clark. 1997. Principles of population genetics. Sinauer Associates, Sunderland, MA.
40. He, T. H., G. Y. Rao, R. L. You, and S. Ge. 1998. Mating system of Ophiopogon xylorrhizus (Liliaceae), an endangered species in southwest China. Int. J. Plant Sci. 159:440-445.
41. Hedrick, P. W. 1980. Hitchhiking: a comparison of linkage and partial selfing. Genetics. 94:791-808.
42. Herlihy, C. R., and C. G. Eckert. 2002. Genetic cost of reproductive assurance in a self-fertilizing plant. Nature 416:320-323.
43. Holtsford, T. P., and N. C. Ellstrand. 1990. Inbreeding effects in Clarkia tembloriensis (Onagraceae) populations with different natural outcrossing rates. Evolution 44:2031-2046.
44. Hurst, L. D., and J. R. Peck. 1996. Recent advances in understanding of the evolution and maintenance of sex. Trends Ecol. Evol. 11:46-52.
45. Jaenike, J. 1978. An hypothesis to account for the maintenance of sex within populations. Evol. Theor. 3:191-194.
46. Jain, S. K. 1976. The evolution of inbreeding in plants. Annu. Rev. Ecol. Syst. 7:469-495.
47. Jarne, P. 1995. Mating system, bottlenecks and genetic polymorphism in hermaphroditic animals. Genet. Res. 65:193-207.
48. Jarne, P., and D. Charlesworth. 1993. The evolution of the selfing rate in functionally hermaphrodite plants and animals. Annu. Rev. Ecol. Syst. 24:441-466.
49. Jarne, P., and B. Delay. 1990. Inbreeding depression and self-fertilization in Lymnaea peregra (Gastropoda: Pulmonata). Heredity 64:169-175.
50. Jarne, P., and P. J. L. Lagoda. 1996. Microsatellites, from molecules to populations and back. Trends Ecol Evol. 11:424-429.
51. Jarne, P., and T. Städler. 1995. Population genetic structure and mating system evolution in freshwater pulmonates. Experientia 51:482-497.
52. Jarne, P., and A. Théron. 2001. Genetic structure in natural populations of flukes and snails: a practical approach and review. Parasitology 123:S27-S40.
53. Jarne, P., L. Finot, B. Delay, and L. Thaler. 1991. Self-fertilization versus cross-fertilization in the hermaphroditic freshwater snail Bulinus globosus. Evolution 45:1136-1146.
54. Jarne, P., M. Vianey-Liaud, and B. Delay. 1993. Selfing and outcrossing in hermaphrodite freshwater gastropods (Basommatophora): where, when and why. Biol. J. Linn. Soc. 49:99-125.
55. Jarne, P., M.-A. Perdieu, A.-F. Pernot, B. Delay, and P. David. 2000. The influence of self-fertilization and grouping on fitness attributes in the freshwater snail Physa acuta: population and individual inbreeding depression. J. Evol. Biol. 13:645-655.
56. Jokela, J., C. M. Lively, M. F. Dybdahl, and J. A. Fox. 1997. Evidence for a cost of sex in the freshwater snail Potamopyrgus antipodarum. Ecology 78:452-460.
57. Kaplan, N. L., R. R. Hudson, and C. H. Langley. 1989. The hitchhiking effect revisited. Genetics 123:887-899.
58. Keller, L. F., and D. M. Waller. 2002. Inbreeding effects in wild populations. Trends Ecol. Evol. 17:230-241.
59. Kendall, S. B. 1949. Bionomics of Limnaea truncatula and the parthenitae of Fasciola hepatica under drought conditions. J. Helminth. 23:57-68.
60. _. 1953. The life-history of Limnaea truncatula under laboratory conditions. J. Helminth. 27:17-28.
61. Kirkpatrick, M., and P. Jarne. 2000. The effects of a bottleneck on inbreeding depression and the genetic load. Am. Nat. 155:154-167.
62. Ladle, R. J., R. A. Johnstone, and O. P. Judson. 1993. Coevolutionary dynamics of sex in a metapopulation: escaping the Red Queen. Proc. R. Soc. Lond. B 253:155-160.
63. Lande, R., and D. W. Schemske. 1985. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39:24-40.
64. Leberg, P. 1992. Effects of population bottlenecks on genetic diversity as measured by allozyme electrophoresis. Evolution 46:477-494.
65. Liu, F., L. Zhang, and D. Charlesworth. 1998. Genetic diversity in Leavenworthia populations with different inbreeding levels. Proc. R. Soc. Lond. B 265:293-301.
66. Lively, C. M., and R. S. Howard. 1994. Selection by parasites for clonal diversity and mixed mating. Phil. Trans. R. Soc. Lond. B 346:271-281.
67. Malek, E. A. 1980. Snail-transmitted diseases. Vol. I and II. CRC Press, Inc., Boca Raton, FL.
68. Malone, C. R. 1965. Killdeer (Charadrius vociferus Linnaeus) as a means of dispersal for aquatic gastropods. Ecology 46:551-552.
69. Manly, B. F. J. 1997. Randomization, bootstrap and Monte Carlo methods in biology. 2d ed. Chapman and Hall, London.
70. Maynard Smith, J. 1978. The evolution of sex. Cambridge Univ. Press, Cambridge, U.K.
71. Meagher, S. 1999. Genetic diversity and Capillaria hepatica (Nematoda) prevalence in Michigan deer mouse populations. Evolution 53:1318-1324.
72. Meunier, C., C. Tirard, S. Hurtrez-Bousses, P. Durand, M. D. Bargues, S. Mas-Coma, J. P. Pointier, J. Jourdane, and F. Renaud. 2001. Lack of molluscan host diversity and the transmission of an emerging parasitic disease in Bolivia. Mol. Ecol. 10:1333-1340.
73. Nei, M. 1987. Molecular evolutionary genetics. Columbia Univ. Press, New York.
74. Nei, M., T. Maruyama, and R. Chakraborty. 1975. The bottleneck effect and genetic variability in populations. Evolution 29:1-10.
75. Otto, S. P., and Y. Michalakis. 1998. The evolution of recombination in changing environments. Trends Ecol. Evol. 13:145-151.
76. Pannell, J. R., and S. C. H. Barrett. 1998. Baker's law revisited: reproductive assurance in a metapopulation. Evolution 52:657-668.
77. _. 2001. Effects of population size and metapopulation dynamics on a mating-system polymorphism. Theor. Popul. Biol. 59:145-155.
78. Petit, E., F. Balloux, and J. Goudet. 2001. Sex-biased dispersal in a migratory bat: a characterization using sex-specific demographic parameters. Evolution 55:635-640.
79. Petit, R. J., A. El Mousadik, and O. Pons. 1998. Identifying populations for conservation on the basis of genetic markers. Conserv. Biol. 12:844-855.
80. Pollak, E. 1987. On the theory of partially inbreeding finite populations I. Partial selfing. Genetics 117:353-360.
81. Purchon, R. D. 1968. The biology of the mollusca. Pergamon Press, Oxford, U.K.
82. Rice, W. R. 1989. Analysing tables of statistical tests. Evolution 43:223-225.
83. Ritland, K. 1986. Joint maximum likelihood estimation of genetic and mating structure using open-pollinated progenies. Biometrics 42:25-43.
84. _. 1990. Inferences about inbreeding depression based on changes of the inbreeding coefficient. Evolution 44:1230-1241.
85. Ritland, K., and S. Jain. 1981. A model for the estimation of outcrossing rate and gene frequencies using n independent loci. Heredity 47:35-52.
86. Roberts, E. W. 1950. Studies on the life-cycle of Fasciola hepatica (Linnaeus) and of its snail host, Limnaea (Galba) truncatula (Müller), in the field and under controlled conditions in the laboratory. Ann. Trop. Med. Parasitol. 44:187-206.
87. Rondelaud, D., and C. Mage. 1992. Lymnaea truncatula Müller: les consequences d'une seule génération annuelle sur les caractérístiques de l'infestation par Fasciola hepatica. Rev. Méd. Vét. 143:843-846.
88. Rousset, F. 1997. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219-1228.
89. Slate, J., and J. M. Pemberton. 2002. Comparing molecular measures for detecting inbreeding depression. J. Evol. Biol. 15:20-31.
90. Slatkin, M. 1977. Gene flow and genetic drift in a species subject to frequent local extinctions. Theor. Popul. Biol. 12:253-262.
91. _. 1985. Gene flow in natural populations. Annu. Rev. Ecol. Syst. 16:393-430.
92. Smith, G. 1981. Copulation and oviposition in Lymnaea truncatula (Müller). J. Molluscan Stud. 47:108-111.
93. Sorensen, R. E., and D. J. Minchella. 1998. Parasite influences on host life history: Echinostoma revolutum parasitism of Lymnaea elodes snails. Oecologia 115:188-195.
94. Städler, T., and P. Jarne. 1997. Population biology, genetic structure, and mating system parameters in freshwater snails. Pp. 231-262 in B. Streit, T. Städler, C. M. Lively, eds. Evolutionary ecology of freshwater animals. Birkhäuser, Basel.
95. Tomlinson, J. 1966. The advantages of hermaphroditism and parthenogenesis. J. Theor. Biol. 11:54-58.
96. Trouvé, S., F. Renaud, P. Durand, and J. Jourdane. 1996. Selfing and outcrossing in a parasitic hermaphrodite helminth (Trematoda, Echinostomatidae). Heredity 77:1-8.
97. _. 1999a. Reproductive and mate choice strategies in the hermaphroditic flatworm Echinostoma caproni. J. Hered. 90:582-585.
98. Trouvé, S., J. Jourdane, F. Renaud, P. Durand, and S. Morand. 1999b. Adaptive sex allocation in a simultaneous hermaphrodite. Evolution 53:1599-1604.
99. Trouvé, S., L. Degen, C. Meunier, C. Tirard, S. Hurtrez-Bousses, P. Durand, J. F. Guégan, J. Goudet, and F. Renaud. 2000. Microsatellites in the hermaphroditic snail, Lymnaea truncatula, intermediate host of the liver fluke, Fasciola hepatica. Mol. Ecol. 9:1662-1664.
100. Uyenoyama, M. K., K. E. Holsinger, and D. M. Waller. 1993. Ecological and genetic factors directing the evolution of self-fertilization. Oxf. Surv. Evol. Biol. 9:327-381.
101. Van Treuren, R., R. Bijlsma., N. J. Ouborg, and W. Van Delden. 1993. The effects of population size and plant density on outcrossing rates in locally endangered Salvia pratensis, Evolution 47:1094-1104.
102. Van Valen, L. 1973. A new evolutionary law. Evol. Theor. 1:1-30.
103. Viard, F., F. Justy, and P. Jarne. 1997. The influence of self-fertilization and population dynamics on the genetic structure of subdivided populations: a case study using microsatellite markers in the freshwater snail Bulinus truncatus. Evolution 51:1518-1528.
104. Victoir, K., and J. C. Dujardin. 2002. How to succeed in parasitic life without sex? Asking Leishmania. Trends Parasitol. 18:81-85.
105. Wade, M. J., and D. E. McCauley. 1988. Extinction and recolonization: their effects on the genetic differentiation of local populations. Evolution 42:995-1005.
106. Waller, D. M., and S. E. Knight. 1989. Genetic consequences of outcrossing in the cleistogamous annual, Impatiens capensis. II. Outcrossing rates and genotypic correlations. Evolution 43:860-869.
107. Weir, B. S., and C. C. Cockerham. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38:1358-1370.
108. Wethington, A. R., and R. T. Dillon Jr. 1991. Sperm storage and evidence for multiple insemination in a natural population of the freshwater snail, Physa. Am. Malacol. Bull. 9:99-102.
109. Whitlock, M. C., and M. C. McCauley. 1990. Some population genetic consequences of colony formation and extinction: genetic correlations within founding groups. Evolution 44:1717-1724.
110. Whitlock, M. C., P. K. Ingvarsson, and T. Hatfield. 2000. Local drift load and the heterosis of interconnected populations. Heredity 84:452-457.
111. Wright, S. 1969. Evolution and the genetics of populations: the theory of gene frequencies. Vol. 2. Univ. of Chicago Press, Chicago, IL.