Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-25T18:37:30.190Z Has data issue: false hasContentIssue false
  • English
  • Français

Mating system, bottlenecks and genetic polymorphism in hermaphroditic animals

Published online by Cambridge University Press:  14 April 2009

Philippe Jarne
Philippe Jarne
Affiliation:
Génétique et Environnement-CC065, Institut des Sciences de l'Evolution, Université Montpellier II, Place E. Bataillon, 34095 Montpellier Cedex 5, France, Phone (33) 67 14 46 29, Fax (33) 67 14 36 22, Email [email protected]
Rights & Permissions [Opens in a new window]

Summary

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

A loss of neutral genetic polymorphism is theoretically expected for many reasons in inbreeding organisms when compared to outbreeders. The first reason derives from the decrease of the effective population size, down to a halving, in purely selfing species. Other genetical reasons include hitchhiking and background selection. A loss can also be caused by ecological processes, that is by any kind of process provoking a genetic bottleneck. These theoretical expectations have been empirically confirmed in hermaphroditic plants for which selfing species exhibit both a lower gene diversity and number of alleles per population. Here I extend the analysis to hermaphroditic animals, mainly terrestrial and freshwater snails. The decrease of variability in selfers is far greater than what is expected under the halving of the effective size of populations only. Hitchhiking and background selection certainly cannot be rejected as causes of this extra loss. Bottlenecks can clearly be invoked in tropical freshwater snails. However a crude theoretical analysis using Ewens's sampling formulae shows that the relative loss of variability estimated by the number of alleles is smaller in inbreeders than in outbreeders assuming populations with the same number of individuals. This suggests that bottlenecks contribute less to the loss in selfers than in outcrossers. Variability lost within selfing populations of hermaphroditic animals is also lost at the level of a group of populations (metapopulation). This is theoretically not always expected. Indeed, I calculate the ratio of the effective size of a selfing metapopulation to be greater than that of an outcrossing one using previously derived equations. The large variation of this ratio which depends on both migration and effective size of subpopulations prevents prediction of the relative amount of genetic variability stored by selfing and outcrossing metapopulations.

Type
Research Article
Information
Genetics Research , Volume 65 , Issue 3 , June 1995 , pp. 193 - 207
Copyright
Copyright © Cambridge University Press 1995

References

Adiyodi, K. G., & Adiyodi, R. G., (1983). Reproductive Biology of Invertebrates. Vol. 1. Chichester: John Wiley & Sons.Google Scholar
Agatsuma, T., & Habe, S., (1986). Genetic variability and differentiation of natural populations in three Japanese lung flukes, Paragonimus ohirai, Paragonimus iloktsuenensis and Paragonimus sadoensis (Digenea: Troglotrematidae). Journal of Parasitology 72, 417–433.Google Scholar
Agnese, J.-F., (1989). Differenciation génétique de plusieurs espèces de siluriformes ouest-africains ayant un intérêt pour la pêche et l'aquaculture. Thèse de Doctorat, Université de Montpellier, France.Google Scholar
Arter, H. E., (1990). Spatial relationship and gene flow paths between populations of the alpine snail Arianta arbustorum (Pulmonata: Helicidae). Evolution 44, 966–980.CrossRefGoogle Scholar
Bandoni, S. M., Mulvey, M., Koech, D. K., & Locker, E. S., (1990). Genetic structure of Kenyan populations of Biomphalaria pfeifferi (Gastropoda: Planorbidae). Journal of Molluscan Studies 56, 383–391.Google Scholar
Barrett, S. C. H., & Kohn, J. R., (1991). Genetic and evolutionary consequences of small population size in plants: implications for conservation. In Genetics and Conservation of Rare Plants (ed. Falk, D. A. and Holsinger, K. E.), pp. 3–30. New York: Oxford University Press.Google Scholar
Baur, B., & Klemm, M., (1989). Absence of isozyme variation in geographically isolated populations of the land snail Chondrina clienta. Heredity 63, 239–244.Google Scholar
Beckwitt, R., (1980). Genetic structure of Pileolaria pseudomilitaris (Polychaeta: Spirobidae). Genetics 96, 711–726.Google Scholar
Brown, D. S., (1994). Freshwater Snails of Africa and their Medical Importance, 2nd ed.London: Taylor & Francis Ltd.Google Scholar
Brown, K. M., & Richardson, T. D., (1988). Genetic polymorphism in gastropods: A comparison of methods and habitat scales. American Malacological Bulletin 6, 9–17.Google Scholar
Brussard, P. F., (1975). Geographic variation in North American colonies of Cepaea nemoralis. Evolution 29, 402–410.Google Scholar
Chakraborty, R., & Neel, J. V., (1989). Description and validation of a method for simultaneous estimation of effective population size and mutation rate from human population data. Proceedings of the National Academy of Science, USA 86, 9407–9411.Google Scholar
Charlesworth, B., Morgan, M. T., & Charlesworth, D., (1993). The effect of deleterious mutations on neutral molecular variation. Genetics 134, 1289–1303.Google Scholar
Charlesworth, D., Morgan, M. T. & Charlesworth, B., (1993). Mutation accumulation in finite outbreeding and inbreeding populations. Genetical Research 61, 39–56.Google Scholar
Chiba, S., (1993). Modern and historical evidence for natural hybridization between sympatric species in Mandarina (Pulmonata: Camaenidae). Evolution, 47 1539–1556.Google Scholar
Cook, L. M., & Lace, L. A., (1993). Sex and genetic variation in a helicid snail. Heredity 70, 376–384.Google Scholar
Coutellec-Vreto, M.-A., Guiller, A., & Daguzan, J., (1994). Allozyme variation in some populations of the freshwater snails Lymnaea peregra, L. auricularia and L. stagnalis (Gastropoda: Pulmonata). Journal of Molluscan Studies 60, 393–403.Google Scholar
Crow, J. F., (1993). Mutation, mean fitness, and genetic load. Oxford Surveys in Evolutionary Biology 9, 3–42.Google Scholar
Crow, J. F., & Kimura, M., (1970). An Introduction to Population Genetics Theory. Minneapolis: Burgess Publishing Company.Google Scholar
Ellstrand, N. C., & Elam, D. R., (1993). Population genetic consequences of small population size: implications for plant conservation. Annual Review of Ecology and Systematics 24, 217–242.Google Scholar
Ewens, W. J., (1972). The sampling theory of selectively neutral alleles. Theoretical Population Biology 3, 87–112.Google Scholar
Falniowski, A., Kozik, A., Szarowska, M., Rapala-Kozik, M., & Turyna, I., (1993). Morphological and allozymic polymorphism and differences among local populations in Bradybaena fruticum (O. F. Müller, 1777) (Gastropoda: Stylommatophora: Helicoidea). Malacologia 35, 371–388.Google Scholar
Foltz, D. W., Ochman, H., Jones, J. S., Evangelisti, S. M., & Selander, R. K., (1982). Genetic population structure and breeding systems in arionid slugs (Mollusca: Pulmonata). Biological Journal of the Linnaean Society 17, 225–241.CrossRefGoogle Scholar
Foltz, D. W., Ochman, H., & Selander, R. K., (1984). Genetic diversity and breeding systems variation in terrestrial slugs of the families Limacidae and Arionidae. Malacologia 25, 593–605.Google Scholar
Fong, P. P., & Garthwaite, R. L., (1994). Allozyme electrophoretic analysis of the Hedite limnicola— H. diversicolor — H. japonica complex (Polychaeta: Nereidadae). Marine Biology 118, 463–470.Google Scholar
Gabriel, W., Lynch, M., & Bürger, M., (1993). Muller's ratchet and mutational meltdowns. Evolution 47, 1744–1757.Google Scholar
Gaffney, P. M., Scott, T. M., Koehn, R. K., & Diehl, W. J., (1990). Interrelationships of heterozygosity, growth rate and heterozygote deficiencies in the coot clam, Mulinia lateralis. Genetics 124, 687–699.Google Scholar
Gillespie, J. H., (1991). The Causes of Molecular Evolution. Oxford: Oxford University Press.Google Scholar
Govindaraju, D. R., (1988). A note on the relationship between outcrossing rate and gene flow in plants. Heredity 61, 401–404.Google Scholar
Guiller, A., (1994). Aspects géographique de la différenciation génétique des populations de l'escargot terrestre Helix Aspersa Müller (Gastéropode Pulmoné). Thése de Doctorat, Université de Rennes I, France.Google Scholar
Guiller, A., & Madec, L., (1993). A contribution to the study of morphological and biochemical differentiation of French and Iberian populations of Cepaea nemoralis. Biochemical Systematics and Ecology 21, 323–339.Google Scholar
Hamrick, J. L., & Godt, J. W., (1989). Allozymes diversity in plant species. In Plant Population Genetics, Breeding, and Genetic Resources (ed. Brown, A. H. D., Clegg, M. T., Kahler, A. L. and Weir, B. S.), pp. 43–63. Sunderland: Sinauer Associates Inc.Google Scholar
Hartl, D. L., & Clark, A. G., (1989). Principles of Population Genetics, 2nd ed.Sunderland: Sinauer Associates Inc.Google Scholar
Hebert, P. D. N., & Payne, W. J., (1985). Genetic variation in populations of the hermaphroditic flatworm Mesostoma lingua (Turbellaria, Rhabdocoela). Biological Bulletin 169, 143–151.Google Scholar
Hebert, P. D. N., & Beaton, M. J., (1990). Breeding system and genome size of the rhabdocoel turbellarian Mesostoma ehrenbergii. Genome 33, 719–724.Google Scholar
Hebert, P. D. N., Schwartz, S. S., Ward, R. D., & Finston, T. L., (1993). Macrogeographic patterns of breeding system diversity in the Daphnia pulex group. I. Breeding systems of Canadian populations. Heredity 70, 148–161.Google Scholar
Hedrick, P. W., (1980). Hitch-hiking: a comparison of linkage and partial selfing. Genetics 94, 791–808.Google Scholar
Hedrick, P. W., (1994). Purging inbreeding depression and the probability of extinction. Heredity 73, 363–372.Google Scholar
Hillis, D. M., Rosenfeld, D. S., & Sanchez, M., (1987). Allozymic variability and heterozygote deficiency within and among morphologically polymorphic populations of Liguus fasciatus (Mollusca: Pulmonata: Bulimulidae). American Malacological Bulletin 5, 153–157.Google Scholar
Houle, D., (1989). Allozyme-associated heterosis in Drosophila melanogaster. Genetics 123, 789–801.Google Scholar
Jarne, P., & Delay, B., (1990). Population genetics of Lymnaea peregra (Müller) (Gastropoda: Pulmonata) in lake Geneva. Journal of Molluscan Studies 56, 317–321.Google Scholar
Jarne, P., & Charlesworth, D., (1993). The evolution of the selfing rate in functionally hermaphrodite plants and animals. Annual Review of Ecology and Systematics 24, 441–466.Google Scholar
Jarne, P., Vianey-Liaud, M., & Delay, B., (1993). Selfing and outcrossing in hermaphrodite freshwater gastropods (Basommatophora): where, when and why. Biological Journal of the Linnaean Society 49, 99–125.Google Scholar
Jelnes, J. E., (1986). Experimental taxonomy of Bulinus (Gastropoda: Planorbidae): the West and North African species reconsidered based on an electrophoretic study of several enzymes per individual. Zoological Journal of the Linnaean Society 87, 1–26.Google Scholar
Johnson, M. S., (1988). Founder effects and geographic variation in the land snail Theba pisana. Heredity 61, 133–42.Google Scholar
Johnson, M. S., Murray, J., & Clarke, B. C., (1986). High genetic similarities and low heterozygosities in land snails of the genus Samoana from the Society islands. Malacologia 27, 97–106.Google Scholar
Kat, P. W., & Davis, G. M., (1984). Molecular genetics of peripheral populations of Nova Scotian Unionidae (Mollusca: Bivalvia). Biological Journal of the Linnaean Society 22, 157N–185.Google Scholar
Kimura, M., & Ohta, T., (1971). Theoretical Aspects of Population Genetics. Princeton: Princeton University Press.Google Scholar
Leberg, P. L., (1992). Effects of population bottlenecks on genetic diversity as measured by allozyme electrophoresis. Evolution 46, 477–494.Google Scholar
Maruyama, T., & Kimura, M., (1980). Genetic variability and effective population size when local extinction and recolonization of subpopulations are frequent. Proceedings of the National Academy of Science, USA 77, 6710–6714.Google Scholar
Maruyama, K., & Tachida, H., (1992). Genetic variability and geographic structure in partially selfing populations. Japanese Journal of Genetics 67: 39–51.Google Scholar
McCracken, G. F., & Brussard, P. F., (1980). The population biology of the white-lipped land snail, Triodopsis albolabris: genetic variability. Evolution 34, 92–104.Google Scholar
McCracken, G. F., & Selander, R. K., (1980). Selffertilization and monogenic strains in natural populations of terrestrial slugs. Proceedings of the National Academy of Science, USA 77, 684–688.Google Scholar
McLeod, M. J., Hornbach, D. J., Guttman, S. I., Way, C. M., & Burky, A. J., (1980). Environmental heterogeneity, genetic polymorphism and reproductive strategies. American Naturalist 118, 129–134.Google Scholar
Mimpfoundi, R., & Greer, G. J., (1989). Allozyme comparisons among species of the Bulinus forskalii group (Gastropoda: Planorbidae) in Cameroon. Journal of Molluscan Studies 55, 405–410.Google Scholar
Mimpfoundi, R., & Greer, G. J. (1990 a). Allozyme variation among populations of Bulinus forskalii (Ehrenberg, 1831) (Gastropoda: Planorbidae) in Cameroon. Journal of Molluscan Studies 56, 363–371.Google Scholar
Mimpfoundi, R., & Greer, G. J. (1990 b). Allozyme variation among populations of Biomphalaria pfeifferi (Krauss, 1848) (Gastropoda: Planorbidae) in Cameroon. Journal of Molluscan Studies 56, 461–467.Google Scholar
Mimpfoundi, R., & Greer, G. J., (1990 c). Allozyme variation among populations of Biomphalaria camerounensis (Boettger, 1941) (Gastropoda: Planorbidae) in Cameroon. Journal of Molluscan Studies 56, 373–381.Google Scholar
Mimpfoundi, R., & Greer, G. J. (1990 d). Allozyme comparison and ploidy levels among species of the Bulinus truncatus/tropicus complex (Gastropoda: Planorbidae). Journal of Molluscan Studies 56, 63–68.Google Scholar
Mulvey, M., & Vrijenhoek, R. C., (1982). Population structure in Biomphalaria glabrata: examination of an hypothesis for the patchy distribution of susceptibility to schistosomes. American Journal of Tropical Medicine and Hygiene 31, 1195–1200.Google Scholar
Mulvey, M., Newman, M. C., & Woodruff, D. S., (1988). Genetic differentiation among West Indian populations of the schistosome-transmitting snail Biomphalaria glabrata. Malacologia 29, 309–317.Google Scholar
Mulvey, M., Goater, T. M., Esch, G. W., & Crews, A. E., (1987). Genotype frequency differences in Halipegus occidualis-infected and uninfected Helisoma anceps. Journal of Parasitology 73, 757–761.Google Scholar
Mulvey, M., Aho, J. M., Lydeard, C, Leberg, P. L., & Smith, M. H., (1991). Comparative population genetic structure of a parasite (Fascioloides magna) and its definitive host. Evolution 45, 1628–1640.Google Scholar
Nei, M., (1987). Molecular Evolutionary Genetics. New York: Columbia University Press.Google Scholar
Nei, M., Maruyama, T., & Chakraborty, R., (1975). The bottleneck effect and genetic variability in populations. Evolution 29, 1–10.Google Scholar
Nevo, E., Bar-El, C., Bar, Z., & Beiles, A., (1981). Genetic structure and climatic correlates of desert landsnails. Oecologia 48, 199–208.Google Scholar
Nevo, E., Bar-El, C., & Bar, Z., (1983). Genetic diversity, climatic selection and speciation in Sphincterochila landsnails in Israel. Biological Journal of the Linnaean Society 19, 339–373.Google Scholar
Nevo, E., Beiles, A., & Ben-Schlomo, R., (1984). The evolutionary significance of genetic diversity: ecological, demographic and life history correlates. In Evolutionary Dynamics of Genetic Diversity. Lecture Notes in Biomathematics, vol. 53, (ed. Mani, G. S.), pp. 13–213. New York: Springer-Verlag.Google Scholar
Njiokou, F., Bellec, C., Berrebi, P., Delay, & Jarne, P., (1993). Do self-fertilization and genetic drift promote a very low variability in the allotetraploid Bulinus truncatus (Gastropoda: Planorbidae) populations? Genetical Research 62, 89–100.Google Scholar
Njiokou, F., Delay, B., Bellec, C., N'Goran, E. K., Yapi Yapi, G., & Jarne, P., (1994). Population genetic structure of the schistosome-vector snail Bulinus globosus: examining the role of genetic drift, migration and human activities. Heredity 72, 488–497.Google Scholar
Pollak, E., (1987). On the theory of partially inbreeding finite populations. I. Partial selfing. Genetics 117, 353–360.Google Scholar
Ritland, C., Ritland, K., & Straus, N. A., (1993). Variation in the ribosomal internal transcribed spacers (ITS1 and ITS2) among eight taxa of the Mimulus guttatus species complex. Molecular Biology and Evolution 10, 1273–1288.Google Scholar
Rollinson, D., & Wright, C. A., (1984). Population studies on Bulinus cernicus from Mauritius. Malacologia 25,447–463.Google Scholar
Rollinson, D., Kane, R. A., Warlow, A., Southgate, V. R., & Gopaul, A. R., (1990). Observations on genetic diversity of Bulinus cernicus (Gastropoda: Planorbidae) from Mauritius. Journal of Zoology, London 222, 19–26.Google Scholar
Schoen, D. J., & Brown, A. H. D., (1991). Intraspecific variation in population gene diversity and effective population size correlates with the mating system in plants. Proceedings of the National Academy of Science, USA 88, 4494–4497.Google Scholar
Selander, R. K., & Kaufman, D. W., (1973). Self-fertilization and genetic population structure in a colonizing land snail. Proceedings of the National Academy of Science, USA 70, 1186–1190.Google Scholar
Selander, R. K., & Kaufman, D. W., (1975). Genetic structure of the brown snail (Helix aspersa). I. Microgeographic variation. Evolution 29, 385–401.Google Scholar
Selander, R. K., & Hudson, R. O., (1976). Animal population structure under close inbreeding: the land snail Rumina in Southern France. American Naturalist 110, 695–718.Google Scholar
Selander, R. K., & Ochman, H., (1983). The genetic structure of populations as illustrated by molluscs. Isozymes 10, 93–123.Google Scholar
Skibinski, D. O. F., Woodmark, M., & Ward, R. D., (1993). A quantitative test of the neutral theory using pooled allozyme data. Genetics 135, 233–248.Google Scholar
Sokal, R. R., & Rohlf, F. J., (1981). Biometry, 2nd ed.New York: Freeman & Co.Google Scholar
Tajima, F., (1989). The effect of change in population size on DNA polymorphism. Genetics 123, 597–601.Google Scholar
Taylor, A.C., Sherwin, W. B., & Wayne, R. K., (1994). Genetic variation of microsatellite loci in a bottlenecked species: the northern hairy-nosed wombat Lasiorhinus kreftii. Molecular Ecology 3, 277–290.Google Scholar
Turner, B. J., Elder, J. F., Laughlin, T. F., Davis, W. P., & Taylor, D. S., (1992). Extreme clonal diversity and divergence in populations of a selfing hermaphroditic fish. Proceedings of the National Academy of Science, USA 89, 10643–10647.Google Scholar
Vrijenhoek, R. C., (1979). Genetics of a sexually reproducing fish in a highly fluctuating environment. American Naturalist 113, 17–29.Google Scholar
Vrijenhoek, R. C., (1985). Homozygosity and interstrain variation in the self-fertilizing hermaphroditic fish, Rivulus marmoratus. Journal of Heredity 76, 82–84.Google Scholar
Vrijenhoek, R. C., & Graven, M. A., (1992). Population genetics of Egyptian Biomphalaria alexandrina (Gastropoda, Planorbidae). Journal of Heredity 83, 255–261.Google Scholar
Waples, R. S., (1989). Temporal variation in allele frequencies: testing the right hypothesis. Evolution 43, 1236–1251.Google Scholar
Weir, B. S., (1989). Sampling properties of gene diversity. In Plant Population Genetics, Breeding, and Genetic Ressources (ed. Brown, A. H. D., Clegg, M. T., Kahler, A. L. and Weir, B. S.), pp. 23–42. Sunderland: Sinauer Associates Inc.Google Scholar
Woodruff, D. S., (1975). Allozyme variation and genie heterozygosity in the Bahaman Pulmonate snail Cerion bendalli. Malacological Review 8, 47–55.Google Scholar
Woodruff, D. S., Mulvey, M., & Yipp, M. W., (1985). Population genetics of Biomphalaria snails in Hong Kong. Journal of Heredity 76, 355–360.Google Scholar
Zimmerman, E. G., Merritt, R. L., & Wooten, M. C., (1980). Genetic variation and ecology of stoneroller minnows. Biochemical Systematics and Ecology 8, 447–453.Google Scholar