Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-28T01:00:40.567Z Has data issue: false hasContentIssue false

Selection response in traits with maternal inheritance

Published online by Cambridge University Press:  14 April 2009

Russell Lande*
Affiliation:
Department of Ecology and Evolution, University of Chicago, Chicago, IL 60637, USA
Mark Kirkpatrick
Affiliation:
Department of Zoology, University of Texas, Austin, TX 78712, USA
*
* 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.

Maternal inheritance is the non-Mendelian transmission of traits, from mothers to their offspring. Despite its presence in virtually all organisms, acting through a variety of mechanisms, the evolutionary consequences of maternal inheritance are not well understood. Here we review and extend a model of the inheritance and evolution of multiple quantitative characters with complex pathways of maternal effects. Extensions of the earlier model include common family environmental effects not associated with maternal phenotype, sexual dimorphism, and paternal effects (non-Mendelian influence of the father on offspring traits). We find that, in contrast to simple Mendelian inheritance, maternal inheritance produces qualitatively different evolutionary dynamics for two reasons: (1) the response to selection on a set of characters depends not only on their additive genetic variances and covariances, but also on maternal characters that influence them, and (2) time lags in the response to selection create a form of evolutionary momentum. These results have important implications for evolution in natural populations and practical applications in the economic improvement of domesticated species. We derive selection indices that maximize either the economic improvement in a single generation of artificial selection or the asymptotic rate of improvement in long-term selection programmes, based on individual merit or a combination of individual and family merit. Numerical examples show that accounting for maternal inheritance can lead to considerable increases in the efficiency of artificial selection.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1990

References

Bondari, K., Willham, R. & Freeman, A. (1978). Estimates of direct and maternal genetic correlations for pupa weight and family size of Tribolium. Journal of Animal Science 47, 358365.CrossRefGoogle Scholar
Boycott, A. E., Diver, C., Garstang, S. L. & Turner, F. M. (1930). The inheritance of sinistrality in Limnea peregra (Mollusca, Pulmonata). Proceedings of the Royal Society of London B219, 51131.Google Scholar
Bulmer, M. (1985). The Mathematical Theory of Quantitative Genetics. Oxford: Oxford University Press.Google Scholar
Cheverud, J. M., Leamy, L. J., Atchley, W. R. & Rutledge, J. J. (1983). Quantitative genetics and the evolution of ontogeny. I. Ontogenetic changes in quantitative genetic variance components in randombred mice. Genetical Research 42, 6575.CrossRefGoogle Scholar
Cundiff, L. (1972). The role of maternal effects in animal breeding. VIII. Comparative aspects of maternal effects. Journal of Animal Science 35, 13351337.CrossRefGoogle Scholar
Dickerson, G. E. (1947). Composition of hog carcasses as influenced by heritable differences in rate and economy of gain. Iowa Agricultural Experiment Station Research Bulletin 354, 492524.Google Scholar
Eisen, E. J. (1967). Mating designs for estimating direct and maternal genetic variances and direct-maternal covariances. Canadian Journal of Genetics and Cytology 9, 1322.CrossRefGoogle ScholarPubMed
Falconer, D. S. (1965). Maternal effects and selection response. Genetics Today. Proceedings, XI International Congress of Genetics, vol. 3 (ed. Geerts, S. J.), pp. 763774. Oxford: Pergamon Press.Google Scholar
Falconer, D. S. (1981). Introduction to Quantitative Genetics, 2nd edn.New York: Longman.Google Scholar
Grun, P. (1976). Cytoplasmic Inheritance and Evolution. New York: Columbia University Press.Google Scholar
Hanrahan, J. P. (1976). Maternal effects and selection response with an application to sheep data. Animal Production 22, 359369.Google Scholar
Hanrahan, J. P. & Eisen, E. J. (1973). Sexual dimorphism and direct and maternal genetic effects on body weight in mice. Theoretical and Applied Genetics 43, 3945.CrossRefGoogle ScholarPubMed
Harris, D. L. (1963). Influence of errors of parameter estimation upon index selection. Statistical Genetics and Plant Breeding (ed. Hanson, W. D. and Robinson, H. F.), pp. 491500. Washington, D. C.: National Academy of Sciences, National Research Council, Publication 982.Google Scholar
Hayes, J. F. & Hill, W. G. (1981). Modification of estimates of parameters in the construction of genetic selection indices (‘Bending’). Biometrics 37, 483493.CrossRefGoogle Scholar
Hill, W. G. & Thompson, R. (1978). Probabilities of non-positive definite between-group or genetic covariance matrices. Biometrics 34, 429439.CrossRefGoogle Scholar
Janssen, G. M., de Jong, G.Joose, E. N. G. & Scharloo, W. (1988). A negative maternal effect in springtails. Evolution 42, 828834.Google Scholar
Kirkpatrick, M. & Lande, R. (1989). The evolution of maternal characters. Evolution 43, 485503.CrossRefGoogle ScholarPubMed
Lande, R. (1979). Quantitative genetic analysis of multivariate evolution, applied to brain:body size allometry. Evolution 33, 402416.Google ScholarPubMed
Lande, R. (1980). Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34, 292305.CrossRefGoogle ScholarPubMed
Lande, R. & Arnold, S. J. (1983). The measurement of selection on correlated characters. Evolution 37, 12101226.CrossRefGoogle ScholarPubMed
Lande, R. & Price, T. (1989). Genetic correlations and maternal effect coefficients obtained from offspring-parent regression. Genetics 122, 915922.CrossRefGoogle ScholarPubMed
Price, T. D. & Grant, P. R. (1985). The evolution of ontogeny in Darwin's finches: a quantitative genetic approach. American Naturalist 125, 169188.CrossRefGoogle Scholar
Reznick, D. (1981). ‘Grandfather effects’: the genetics of interpopulational differences in offspring size in the mosquito fish. Evolution 35, 941953.Google ScholarPubMed
Riska, B., Rutledge, J. J. & Atchley, W. R. (1985). Covariance between direct and maternal genetic effects in mice, with a model of persistent environmental influences. Genetical Research 45, 287297.CrossRefGoogle Scholar
Roach, D. A. & Wulff, R. D. (1987). Maternal effects in plants. Annual Review of Ecology and Systematics 18, 209236.CrossRefGoogle Scholar
Roberston, A. (1955). Prediction equations in quantitative genetics. Biometrics 11, 9598.Google Scholar
Rutledge, J. J., Robison, O. W., Eisen, E. J. & Legates, J. E. (1972). Dynamics of genetic and maternal effects in mice. Journal of Animal Science 35, 911918.CrossRefGoogle ScholarPubMed
Schaal, B. A. (1984). Life history variation, natural selection, and maternal effects in plant populations. Perspectives in Plant Population Ecology (ed. Dirzo, R. and Sarukahn, J.), pp. 188206. Sunderland, MA: Sinauer.Google Scholar
Van der Steen, H. A. M. (1985). The implication of maternal effects for genetic improvement of litter size in pigs. Livestock Production Science 13, 159168.CrossRefGoogle Scholar
Van Vleck, L. D. (1970). Index selection for direct and maternal genetic components of economic traits. Biometrics 26, 477483.CrossRefGoogle ScholarPubMed
Van Vleck, L. D. (1976). Selection for direct, maternal and grandmaternal genetic components of economic traits. Biometrics 32, 173181.CrossRefGoogle Scholar
Van Vleck, L. D., St Louis, D. & Miller, J. I. (1977). Expected phenotypic response in weaning weight of beef calves from selection for direct and maternal genetic effects. Journal of Animal Science 44, 360367.CrossRefGoogle Scholar
Willham, R. L. (1963). The covariance between relatives for characters composed of components contributed by related individuals. Biometrics 19, 1827.CrossRefGoogle Scholar
Willham, R. L. (1972). The role of maternal effects in animal breeding. III. Biometrical aspects of maternal effects in animals. Journal of Animal Science 35, 12881293.CrossRefGoogle Scholar