Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-28T05:14:49.021Z Has data issue: false hasContentIssue false
  • English
  • Français

Stability and genetic basis of variability of phally polymorphism in natural populations of the self-fertile freshwater snail Bulinus truncatus

Published online by Cambridge University Press:  14 April 2009

Claudie Doums ,
Rabiou Labbo  and
Philippe Jarne
Claudie Doums*
Affiliation:
Génétique et Environnement CC065, Institut des Sciences de l'Evolution, Université Montpellier II, Place Eugéne Bataillon, 34095, Montpellier cedex 5, France
Rabiou Labbo
Affiliation:
OCCGE, Niamey, Niger
Philippe Jarne
Affiliation:
Génétique et Environnement CC065, Institut des Sciences de l'Evolution, Université Montpellier II, Place Eugéne Bataillon, 34095, Montpellier cedex 5, France
*
* Corresponding author.
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.

We investigated the genetic variability for phally polymorphism within and between natural populations of the hermaphrodite self-fertile freshwater snail Bulinus truncatus. Phally polymorphism is characterized by the co-occurrence in natural populations of regular hermaphrodite individuals (euphallic) and individuals deprived of the male copulatory organ (aphallic). The two morphs can both self-fertilize and outcross. However, aphallic individuals cannot outcross as males. We examined the variation of the aphally ratio in 22 natural populations from Niger over two successive years. During the second years, populations were sampled three times at 3 week intervals. The aphally ratio was highly variable among populations at a given sampling data and remained relatively stable over time. For 10 of these populations, one population from Corsica and two from Sardinia, we also estimated the between- and within- population variability, analysing the aphally ratio of 346 families under laboratory conditions. The aphally ratio varied significantly among populations and was highly correlated with the aphally ratio of the natural populations. Some within-population variability, associated with a high value of the broad sense heritability, was observed in four populations out of 13. In these populations, aphallic individuals produced significantly more aphallic offspring than euphallic individuals. Our results indicate a strong genetic basis for aphally, with large genetic differences among populations and some genetic variability for aphally within populations. We discuss the adaptive and stochastic factors that may shape the distribution of the genetic variability for aphally.

Type
Research Article
Information
Genetics Research , Volume 68 , Issue 1 , August 1996 , pp. 23 - 33
Copyright
Copyright © Cambridge University Press 1996

References

Baker, R. J. & Nelder, J. A. (1985). The GLIM system, release 3·77, Manual. Oxford: Numerical Algorithms Group.Google Scholar
Bell, G. (1982). The Masterpiece of Nature: The Evolution and Genetics of Sexuality. Berkeley and Los Angeles: University of California Press.Google Scholar
Brown, D. S. (1994). Freshwater Snails of Africa and their Medical Importance, 2nd edn. London: Taylor & Francis.CrossRefGoogle Scholar
Charlesworth, D. & Charlesworth, B. (1987). Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18, 237–268.CrossRefGoogle Scholar
Charlesworth, B., Morgan, M. T. & Charlesworth, D. (1993). The effect of deleterious mutations on neutral molecular variation. Genetics 134, 1289–1303.CrossRefGoogle ScholarPubMed
Crawley, M. J. (1993). GLIM for Ecologists. Oxford: Blackwell Scientific.Google Scholar
Dempster, E. R. & Lerner, I. M. (1950). Heritability of threshold characters. Genetics 35, 212–236.CrossRefGoogle ScholarPubMed
Doums, C. & Jarne, P., (1996 a). The evolution of phally polymorphism in Bulinus truncatus (Planorbidae, Gastropoda): the cost of the male function analysed through life-history traits and sex allocation. Oecologia (in the Press).CrossRefGoogle ScholarPubMed
Doums, C. & Jarne, P., (1996 b). The evolution of phally polymorphism in Bulinus truncatus: is the male copulatory organ costly? Submitted to Ecology.Google Scholar
Doums, C., Bremond, P., Delay, B. & Jarne, P., (1996 a). The genetical and environmental determination of phally polymorphism in the freshwater snail Bulinus truncatus. Genetics 142, 217–225.Google Scholar
Doums, C., Viard, F., Pernot, A. F., Delay, B. & Jarne, P., (1996 b). Inbreeding depression, neutral polymorphism and copulatory behavior in freshwater snails: a selffertilization syndrome. Evolution (in the Press).Google Scholar
Falconer, D. S. (1989). Introduction to Quantitative Genetics, 3rd edn. New York: Longman Scientific & Technical.Google Scholar
Fenster, C. B. & Ritland, K. (1994). Evidence for natural selection on mating system in Mimulus (Scrophulariaceae). International Journal of Plant Science 155, 588–596.CrossRefGoogle Scholar
Hamilton, W. D., Axelrod, R. & Tanese, R. (1990). Sexual reproduction as an adaptation to resist parasites (a review). Proceeding of the National Academy of Sciences of the USA 87, 3566–3573.Google Scholar
Hazel, W. N. & West, D. A. (1982). Pupal colour dimorphism in swallowtail butterflies as a threshold trait: selection in Eurytides marcellus (Cramer). Heredity 49, 295–301.Google Scholar
Hill, W. G. & Smith, C. (1977). Estimating ‘heritability’ of a dichotomous trait. Biometrics 33, 234–236.Google Scholar
Jarne, P. (1995). Mating system, bottlenecks and genetic polymorphism in hermaphroditic animals. Genetical Research 65, 193–207.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.CrossRefGoogle Scholar
Jarne, P., Finot, L., Bellec, C. & Delay, B. (1992). Aphally versus euphally in self-fertile hermaphrodite snails from the species Bulinus truncatus (Pulmonata: Planorbidae). American Naturalist 139, 424–432.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 Linnean Society 48, 99–125.Google Scholar
Jarne, P., Viard, F., Delay, B. & Cuny, G. (1994). Variable microsatellites in the highly selfing snail Bulinus truncatus (Planorbidae: Basommatophora). Molecular Ecology 3, 527–528.Google Scholar
Jelnes, J. E. (1986). Experimental taxonomy of Bulinus (Gastropoda: Planorbidae): the West and North African species reconsidered, based upon an electrophoretic study of several enzymes per individual. Zoological Journal of the Linnean Society 87, 1–26.Google Scholar
de, Larambergue M. (1939). Etude de l'autofécondation chez les gastéropodes pulmonés: recherches sur l'aphallie et la fécondation chez Bulinus (Isidora) contortus Michaud. Bulletin Biologique de France & Belgique 73, 19–231.Google Scholar
Lively, C. M. & Howard, R. S. (1994). Selection by parasites for clonal diversity and mixed mating. Philosophical Transactions of the Royal Society of London, Series B 346, 271–281.Google ScholarPubMed
McCullagh, H. P. & Nelder, J. A. (1983). Generalized Linear Models. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Nei, M., Maruyama, T. & Chakraborty, R. (1975). The bottleneck effect and genetic variability in populations. Evolution 29, 1–10.CrossRefGoogle ScholarPubMed
Njiokou, F., Bellec, C., Berrebi, P., Delay, B. & Jarne, P. (1993). Do self-fertilization and genetic drift promote a very low genetic variability in the allotetraploid Bulinus truncatus (Gastropoda: Planorbidae) populations? Genetical Research 62, 89–100.CrossRefGoogle Scholar
Raymond, M. & Rousset, F. (1995). An exact test for population differentiation. Evolution 49, 1280–83.Google Scholar
Roff, D. A. (1986). The genetic basis of wing dimorphism in the sand cricket, Gryllus firmus and its relevance to the evolution of wing dimorphisms in insects. Heredity 57, 221–231.CrossRefGoogle Scholar
Schmitt, J. & Ehrhardt, D. W. (1987). A test of the sibcompetition hypothesis for outcrossing advantage in Impatiens capensis. Evolution 41, 579–590.Google Scholar
Schoen, D. J. (1982). The breeding system of Gilia achileifolia: variation in floral characteristics and outcrossing rate. Evolution 36, 352–360.Google Scholar
Schrag, S. J. & Read, A. F. (1992). Temperature determination of male outcrossing ability in a simultaneous hermaphrodite. Evolution 46, 1698–1707.Google Scholar
Schrag, S. J. & Rollinson, D. (1994). Effects of Schistosoma haematobium infection on reproductive success and male outcrossing ability in the simultaneous hermaphrodite, Bulinus truncatus (Gastropoda: Planorbidae). Parasitology 108, 27–34.CrossRefGoogle Scholar
Schrag, S. J., Rollinson, D., Keymer, A. E. & Read, A. F. (1992). Heritability of male outcrossing ability in the simultaneous hermaphrodite, Bulinus truncatus (Gastropoda: Planorbidae). Journal of Zoology, London 216, 311–319.CrossRefGoogle Scholar
Schrag, S. J., Mooers, A. O., Ndifon, G. T. & Read, A. F., (1994 a). Ecological correlates of male outcrossing ability in a simultaneous hermaphrodite snail. American Naturalist 143, 636–655.CrossRefGoogle Scholar
Schrag, S. J., Ndifon, G. T. & Read, A. F. (1994 b). Temperature-determined outcrossing ability in wild populations of a simultaneous hermaphrodite snail. Ecology 75, 2066–2077.CrossRefGoogle Scholar
Sokal, R. R. & Rohlf, F. J. (1995). Biometry, 3rd edn. New York: Freeman.Google Scholar
Stebbins, G. L. (1957). Self-fertilization and population variability in the higher plants. American Naturalist 91, 337–354.Google Scholar
Uyenoyama, M. K., Holsinger, K. E. & Waller, D. M. (1993). Ecological and genetic factors directing the evolution of self-fertilization. Oxford Surveys in Evolutionary Biology 9, 327–381.Google Scholar
Vera, C., Bremond, P., Labbo, R., Mouchet, F., Sellin, E., Boulanger, D., Pointier, J. P., Delay, B. & Sellin, B. (1995). Seasonal fluctuations in population densities of Bulinus senegalensis and B. truncatus (Planorbidae) in temporary pools in a focus of Schistosoma haematobium in Niger: implications for control. Journal of Molluscan Studies 61, 79–88.Google Scholar
Viard, F., Bremond, P., Labbo, R., Justy, F., Delay, B. & Jarne, P. (1996). Microsatellites and the genetics of highly selfing populations in the freshwater snail Bulinus truncatus. Genetics (in the Press).CrossRefGoogle ScholarPubMed
Wyatt, R. (1984). The evolution of self-pollination in granite outcrop species of Arenaria (Caryophyllaceae). I. Morphological correlates. Evolution 38, 804–816.Google Scholar