Abstract
A positive relationship between heterozygosity and growth rate, or less frequently, between heterozygosity and fitness components, has been found in many species. A particularly important component of net fitness is sexual selection. However, no studies have been made of the relationship between this character and multilocus heterozygosity in natural populations. In this study, a natural population of the intertidal flat periwinkle Littorina mariae was used to investigate the heterozygosity-sexual fitness relationship. A positive heterozygosity-sexual fitness relationship was found in male L. mariae, but not in females. The selective coefficients acting on the different heterozygosity classes of males ranged between 0.21 and 0.57 (average 0.39), and are similar to those found in previous studies on correlations between heterozygosity and other fitness components. This relationship accounted for approximately 1 per cent of the variance in matings. Furthermore, the contribution of each locus was associated with its homozygosity excess across loci. The positive heterozygosity-sexual fitness relationship showed the same characteristics as the heterozygosity-growth rate correlation. Finally, relationships between sexual selection and size of snail, and heterozygosity and size were found, although they did not account for the heterozygosity-sexual selection relationship.
Similar content being viewed by others
Article PDF
References
Alvarez, G, Zapata, C, Amaro, R, and Guerra, A. 1989. Multi-locus heterozygosity and fitness in the European oyster, Ostrea edulis L. Heredity, 63, 359–372.
Alvarez, G, Santos, M, and Zapata, C. 1984. Frequency-dependent selection arising from inappropriate fitness estimation. Evolution, 38, 696–699.
Anderson, W W, and McGuire, P R. 1978. Mating pattern and mating success of Drosophila pseudoobscura karyotypes in large experimental populations. Evolution, 32, 416–423.
Arnold, S J, and Wade, M J. 1983a. On the measurement of natural and sexual selection: theory. Evolution, 38, 709–719.
Arnold, S J, and Wade, M J. 1983b. On the measurement of natural and sexual selection: applications. Evolution, 38, 720–734.
Chakraborty, R. 1987. Biochemical heterozygosity and phenotypic variability of polygenic traits. Heredity, 59, 19–28.
Diehl, W I, and Koehn, R K. 1985. Multiple locus heterozygosity, mortality, and growth in a cohort of Mytilus edulis. Mar Biol, 88, 265–271.
Endler, J A. 1986. Natural Selection in the Wild. Princeton University Press, Princeton, NJ.
Falconer, D S. 1981. Introduction to Quantitative Genetics, 2nd edn. Longman, London.
Fretter, V, and Graham, A. 1980. The prosobranch molluscs of Britain and Denmark. Part 5. Marine Littorinaceae. J Moll Stud, Suppl 7, 243–284.
Gaffney, P M, Scott, T M, Koehn, R K, and Diehl, W J. 1990. Interrelationships of heterozygosity, growth rate and heterozygote deficiencies in the coot clam, Mulinia lateralis. Genetics, 124, 687–699.
Gajardo, G M, and Beardmore, J A. 1989. Ability to Switch reproductive mode in Artemia is related to maternal heterozygosity. Mar Ecol Prog Ser, 55, 191–195.
Goodwin, B J, and Fish, J D. 1977. Inter and intra specific variation in L. obtusata and L. mariae. J Moll Stud, 43, 241–254.
Janson, K. 1982. Genetic and environmental effects on the growth rate of Littorina saxatilis Olivi. Mar Biol, 69, 73–78.
Johannesson, K, Rolán-Alvarez, E, and Ekendahl, A. (in press). Incipient reproductive isolation between two sympatric morphs of the intertidal snail Littorina saxatilis. Evolution
Knoppien, P. 1985. Rare male mating advantage: a review. Biol Rev, 60, 81–117.
Koehn, R K. 1990. Heterozygosity and growth in marine bivalves, comments on the paper by Zouros, RomeroDorey and Mallet (1988). Evolution, 44, 213–216.
Koehn, R K, and Gaffney, P M. 1984. Genetic heterozygosity and growth rate in Mytilus edulis. Mar Biol, 82, 1–7.
Linhart, Y B, and Mitton, J B. 1985. Relationships among reproduction, growth rates, and protein heterozygosity in Ponderosa pine. Am J Bot, 11, 181–184.
McAlpine, S. 1993. Genetic heterozygosity and reproductive success in the green treefrog, Hyla cinerea. Heredity, 70, 553–558.
Merrell, D J. 1950. Measurement of sexual isolation and selective mating. Evolution, 4, 326–331.
Mitton, J B, and Grant, M C. 1984. Associations among protein heterozygosity, growth rate, and developmental homeostasis. Ann Rev Ecol Syst, 15, 479–499.
Nei, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 89, 583–590.
O'Donald, P. 1980. Genetic Models of Sexual Selection. Cambridge University Press, London.
Pogson, G H, and Zouros, E. 1994. Auozyme and RFLP heterozygosities as correlates of growth rate in the scallop Placopecten magellanicus, a test of the associative over-dominance hypothesis. Genetics, 137, 221–231.
Prout, T. 1965. The estimation of fitnesses from genotypic frequencies. Evolution, 19, 546–551.
Reid, D G. 1990. Note on the discrimination of females of Littorina mariae Sacchi and Rastelli and L. obtusata (Linnaeus). J Moll Stud, 56, 113–114.
Rice, W R. 1989. Analyzing tables of statistical tests. Evolution, 43, 223–225.
Rodhouse, P G, McDonald, J H, Newell, R I E, and Koehn, R K. 1986. Gamete production, somatic growth and multiple-locus enzyme heterozygosity in Mytilus edulis. Mar Biol, 90, 209–214.
Rolán-Alvarez, E. 1992. A method of breeding Littorina obtusata (L.) and L. mariae Sacchi and Rastelli: preliminary results. In: Grahame, J., Mill, P. J. and Reid, D. G. (eds) Proceedings of the Third International Symposium on Littorinid Biology, pp. 163–167. The Malacological Society of London, London.
Rolán-Alvarez, E. 1993. Estructura Genética y Seleccion Sexual en Poblaciones Naturales de dos Especies Gemelas del Genero Littorina. Ph.D. Thesis, Universidad de Santiago de Compostela.
Rolán-Alvarez, E, Zapata, C, and Alvarez, G. 1995. Distinct genetic subdivision in sympatric and sibling species of the genus Littorina (Gastropoda: Littorinidae). Heredity, 74, 1–9.
Santos, M, Tarrio, R, Zapata, C, and Alvarez, G. 1990. Sexual selection on chromosomal polymorphism in Drosophila subobscura. Heredity, 57, 161–169.
Siegel, S, and Castellan, N J. 1988. Non-parametric Statistics for the Behavioral Sciences. Mcgraw-Hill, New York.
Singh, S M, and Zouros, E. 1978. Genetic variation associated with growth rate in the American oyster (Crassostrea virginica). Evolution, 32, 342–353.
Sokal, R R, and Rohlf, F J. 1981. Biometry, 2nd edn. W. H. Freeman, San Francisco.
Spieth, H T, and Ringo, J M. 1983. Mating behavior and sexual isolation in Drosophila. In: Ashburner, M., Carson, H. L. and Thompson, J. N., Jr (eds) The Genetics and Biology of Drosophila, 3c, pp. 223–284. Academic Press, London.
Ward, R D, Warwick, T, and Knight, A J. 1986. Genetic analysis of ten polymorphic enzyme loci in Littorina saxatilis (Prosobranchia, Mollusca). Heredity, 57, 223–241.
Ward, R D, Warwick, T, and Knight, A J. 1991. Further genetic analysis of polymorphic enzyme loci in Littorina saxatilis (Prosobranchia, Mollusca). Heredity, 66, 151–158.
Williams, G A. 1992. The effect of predation on the life histories of Littorina obtusata and L. mariae. J Mar Biol Ass UK, 72, 403–416.
Zapata, C, Gajardo, G, and Beardmore, J A. 1990. Multilocus heterozygosity and sexual selection in the brine shrimp Artemiafranciscana. Mar Ecol Prog Ser, 62, 211–217.
Zaslavskaya, N I, Sergievsky, S O, and Tatarenkov, A N. 1992. Allozyme similarity of Atlantic and Pacific species of Littorina (Gastropoda, Littorinidae). J Moll Stud, 58, 377–384.
Zaykin, D V, and Pudovkin, A I. 1993. Two programs to estimate significance of X2 values using pseudo-probability tests. J Hered, 84, 152.
Zouros, E. 1987. On the relation between heterozygosity and heterosis, an evaluation of evidence from marine mollusks. Isozymes Curr Top Biol Med Res, 15, 255–270.
Zouros, E. 1993. Associative overdominance: evaluating the effects of inbreeding and linkage disequilibrium. Genetica, 89, 35–46.
Zouros, E, and Foltz, D W. 1987. The use of allelic isozyme variation for the study of heterosis. Isozymes Curr Top Biol Med Res, 13, 1–59.
Zouros, E, and Mallet, A L. 1989. Genetic explanations of the growth/heterozygosity correlation in marine mollusks. In: Ryland, J. S. and Tyler, P. A. (eds) Reproduction, Genetics and Distributions of Marine Organisms, pp. 317–324. Olsen and Olsen, Fredensborg, Denmark.
Zouros, E, and Pogson, G H. 1994. The present status of the relationship between heterozygosity and heterosis. In: Beaumont, A. R. (ed.) Genetics and Evolution of Aquatic Organisms, pp. 135–146. Chapman and Hall, London.
Zouros, E, Singh, S M, Foltz, D W, and Mallet, A L. 1983. Post-settlement viability in the American oyster (Crassostrea virginica): an overdominant phenotype. Genet Res, 41, 259–270.
Acknowledgements
One of us (E. R.-A.) thanks D. Mayo and H. Quesada for help during sampling, H. Quesada and C. Saavedra for general discussions of K. Johannesson and two anonymous referees for improving a version of the manuscript. Philip Mason improved the English of a later version. E. R.-A. was suported by a fellowship from the XUNTA DE GAUCIA and the University of Santiago.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Rolán-Alvarez, E., Zapata, C. & Alvarez, G. Multilocus heterozygosity and sexual selection in a natural population of the marine snail Littorina mariae (Gastropoda: Prosobranchia). Heredity 75, 17–25 (1995). https://doi.org/10.1038/hdy.1995.99
Received:
Issue date:
DOI: https://doi.org/10.1038/hdy.1995.99
