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Evolutionary Biology

, Volume 38, Issue 4, pp 434–440 | Cite as

Genetic and Maternal Effects on Offspring Mortality in Mice

  • Joseph Gyekis
  • David A. Blizard
  • Joseph T. Stout
  • David J. Vandenbergh
  • Gerald E. McClearn
  • Reinmar Hager
Research Article

Abstract

Trade-offs occur when two traits have opposing fitness effects such that positive selection on one trait is constrained by the negative fitness consequences of the other trait. To understand why trade-off may arise we need to study the genetic and non-genetic factors that influence associated traits because these may respond differently to selective pressure. Research into trade-offs has largely focused on the genetic basis of associated traits, yet both maternal effects and epigenetic effects have recently been shown to affect life history traits that play a role in trade-offs. In this study, we analyze genetic, epigenetic and life-history predictors of one of the most important trade-offs, that between offspring number and offspring mortality. Using a large-scale 3-generational intercross between two divergent mouse lines C57BL/6J and DBA/2J, we show that litter size differences between these lines, although significant, are surprisingly not the most important predictors of mortality. Offspring genotype, maternal effects and their interactions are the most influential factors determining mortality. We found significant paternal effects suggesting an important influence of paternal care or potentially the role of imprinted genes. Perhaps contrary to expectations our results further show that the trade-off between offspring number and mortality is not just a simple function of the two factors yielding, on average, an ‘optimal’ litter size at weaning. Indeed if one focused on litter size and mortality alone, the slope of relationship is the same for the two lines, yet they differ in the number of young at weaning. Our study reveals that a perceived trade-off between two traits is governed by a more complex set of interactions between genetic and non-genetic effects.

Keywords

Offspring mortality Litter size Trade-off Parent of origin Maternal effects 

Notes

Acknowledgments

This research was supported by NIH grants P01 AG14731 and T32 AG00276. Joseph Gyekis is supported by a Kligman Graduate Fellowship; Reinmar Hager is supported by a NERC Research Fellowship.

References

  1. Barnett, S. A. (1964). Heterozygosis and the survival of young mice in two temperatures. Quarterly Journal of Experimental Physiology and Cognate Medical Sciences, 49, 290–296.PubMedGoogle Scholar
  2. Brockelman, W. Y. (1975). Competition, the fitness of offspring, and optimal clutch size. The American Naturalist, 109, 677–699.CrossRefGoogle Scholar
  3. Brown, R. E., Mathieson, W. B., Stapleton, J., & Neumann, P. E. (1999). Maternal behavior in female C57BL/6 J and DBA/2 J inbred mice. Physiological Behaviour, 67(4), 599–605.CrossRefGoogle Scholar
  4. Bruce, H. M., & East, J. (1956). Number and viability of young from pregnancies concurrent with lactation in the mouse. Journal of Endocrinology, 14(1), 19–27.PubMedCrossRefGoogle Scholar
  5. Carola, V., Frazzetto, G., & Gross, C. (2006). Identifying interactions between genes and early environment in the mouse. Genes, Brain, and Behaviour 5(2), 189–199.Google Scholar
  6. Cheverud, J. M. (1988). A comparison of genetic and phenotypic correlations. Evolution, 42, 958–968.CrossRefGoogle Scholar
  7. Cheverud, J. M., & Leamy, L. J. (1985). Quantitative genetics and the evolution of ontogeny. III. Ontogenetic changes in correlation structure among live-body traits in random-bred mice. Genetics Research, 46(3), 325–335.Google Scholar
  8. Cheverud, J. M., Leamy, L. J., Atchley, W. R., & Rutledge, J. J. (1983). Quantitative genetics and the evolution of ontogeny I. Genetics Research, 42, 65–75.CrossRefGoogle Scholar
  9. Cheverud, J. M., & Wolf, J. B. (2009). The genetics and evolutionary consequences of maternal effects. In D. Maestripieri (Ed.), Maternal effects in mammals (pp. 11–36). Chicago: Chicago University Press.Google Scholar
  10. Curley, J. P., & Mashoodh, R. (2010). Parent-of-origin and trans-generational germline influences on behavioral development: The interacting roles of mothers, fathers, and grandparents. Developmental Psychobiology, 52(4), 312–330.PubMedCrossRefGoogle Scholar
  11. Falconer, D. S. (1960). The genetics of litter size in mice. Journal of Cell and Comparative Physiology, 56, 153–167.CrossRefGoogle Scholar
  12. Falconer, D. S. (1965). Maternal effects and selection response. In: Genetics today: Proceedings of XIth international congress genetics, Vol 3 (pp. 763–774). Oxford, UK: Pergamon.Google Scholar
  13. Gabriel, K. I., & Cunningham, C. L. (2008). Effects of maternal strain on ethanol responses in reciprocal F1 C57BL/6 J and DBA/2 J hybrid mice. Genes Brain and Behaviour, 7(3), 276–287.CrossRefGoogle Scholar
  14. Gratten, J., Wilson, A. J., McRae, A. F., Beraldi, D., Visscher, P. M., Pemberton, J. M., et al. (2008). A localized negative genetic correlation constrains microevolution of coat color in wild sheep. Science, 319(5861), 318–320.PubMedCrossRefGoogle Scholar
  15. Hager, R., Cheverud, J. M., & Wolf, J. B. (2008). Maternal effects as the cause of parent-of-origin-dependent effects that mimic genomic imprinting. Genetics, 178, 1755–1762.PubMedCrossRefGoogle Scholar
  16. Hager, R., Cheverud, J. M., & Wolf, J. B. (2009). Relative contribution of additive, dominance and imprinting effects to phenotypic variation in body size and growth between divergent selection lines of mice. Evolution, 65, 1118–1128.CrossRefGoogle Scholar
  17. Hager, R., & Johnstone, R. A. (2003). The genetic basis of family conflict resolution in mice. Nature, 421, 533–535.PubMedCrossRefGoogle Scholar
  18. Hager, R., & Johnstone, R. A. (2006). The influence of phenotypic and genetic effects on maternal provisioning and offspring weight gain in mice. Biology Letters, 2, 81–84.PubMedCrossRefGoogle Scholar
  19. Holinka, C. F., Tseng, Y. C., & Finch, C. E. (1978). Prolonged gestation, elevated preparturitional plasma progesterone and reproductive aging in C57BL/6 J mice. Biology Reproductive, 19(4), 807–816.CrossRefGoogle Scholar
  20. Krackow, S. (1990). Sex-specific embryonic mortality during concurrent pregnancy and lactation in house mice. Journal of Experimental Zoology, 256(1), 106–112.PubMedCrossRefGoogle Scholar
  21. Lack, D. (1947). The significance of clutch size. Pts. I and II. Ibis, 87, 302–352.Google Scholar
  22. Lack, D. (1948). The significance of litter size. Journal of Animal Ecology, 17, 45–50.CrossRefGoogle Scholar
  23. Maestripieri, D., & Mateo, J. M. (2009). Maternal effects in mammals. Chicago, IL: University of Chicago Press.Google Scholar
  24. Meaney, M. J. (2001). Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annual Review of Neuroscience, 24, 1161–1192.PubMedCrossRefGoogle Scholar
  25. Mineur, Y. S., Belzung, C., & Crusio, W. E. (2006). Effects of unpredictable chronic mild stress on anxiety and depression-like behavior in mice. Behaviour Brain Research, 175(1), 43–50.CrossRefGoogle Scholar
  26. Priestnall, R. (1972). Effects of litter size on the behaviour of lactating female mice (Mus musculus). Animal Behaviour, 20, 386–394.CrossRefGoogle Scholar
  27. Pritchett, K. R., & Taft, R. A. (2007). Reproductive biology of the laboratory mouse. In J. G. Fox, et al. (Eds.), The mouse in biomedical research: Normative biology, husbandry, and models (2nd ed., Vol. 3, pp. 91–122). Boston: Academic Press.Google Scholar
  28. Ralls, K., & Ballou, J. (1982). Effect of inbreeding on juvenile mortality in some small mammal species. Laboratory Animal, 16(2), 159–166.CrossRefGoogle Scholar
  29. Rauw, W. M., Knap, P. W., Verstegen, M. W., & Luiting, P. (2002). Food resource allocation patterns in lactating females in a long-term selection experiment for litter size in mice. Genetics Selection Evolution, 34(1), 83–104.CrossRefGoogle Scholar
  30. Ressler, R. H. (1962). Parental handling in two strains of mice reared by foster parents. Science, 137, 129–130.PubMedCrossRefGoogle Scholar
  31. Roff, D. A. (1997). Evolutionary quantitative genetics. New York: Chapman and Hall.CrossRefGoogle Scholar
  32. Roff, D. A., & Fairbairn, D. J. (2007). The evolution of trade-offs: Where are we? Journal of Evolutionary Biology, 20(2), 433–447.PubMedCrossRefGoogle Scholar
  33. Sheldon, B. C. (2000). Differential allocation: Tests, mechanisms and implications. Trends in Ecology & Evolution, 15, 397–402.CrossRefGoogle Scholar
  34. Shoji, H., & Kato, K. (2006). Maternal behavior of primiparous females in inbred strains of mice: A detailed descriptive analysis. Physiological Behaviour, 89(3), 320–328.CrossRefGoogle Scholar
  35. Shoji, H., & Kato, K. (2009). Maternal care affects the development of maternal behavior in inbred mice. Developmental Psychobiology, 51(4), 345–357.PubMedCrossRefGoogle Scholar
  36. Stearns, S. C. (1989). Trade-offs in life-history evolution. Functional Ecology, 3, 259–268.CrossRefGoogle Scholar
  37. van der Veen, R., Abrous, D. N., de Kloet, E. R., Piazza, P. V., & Koehl, M. (2008). Impact of intra- and interstrain cross-fostering on mouse maternal care. Genes Brain and Behaviours, 7(2), 184–192.CrossRefGoogle Scholar
  38. Ward, R. (1980). Some effects of strain differences in the maternal behavior of inbred mice. Developmental Psychobiology, 13(2), 181–190.PubMedCrossRefGoogle Scholar
  39. Wilkins, J. F., & Haig, D. (2003). What good is genomic imprinting: The function of parent-specific gene expression. Nature Genetics Review, 4, 1–19.Google Scholar
  40. Williams, G. C. (1966). Adaptation and natural selection: A critique of some current evolutionary thought. Princeton, N.J: Princeton University Press.Google Scholar
  41. Wolf, J. B., Brodie, E. D., III, Cheverud, J. M., Moore, A. J., & Wade, M. J. (1998). Evolutionary consequences of indirect genetic effects. Trends in Ecology & Evolution, 13, 64–69.CrossRefGoogle Scholar
  42. Wolf, J. B., Cheverud, J. M., Roseman, C., & Hager, R. (2008a). Genome-wide analysis reveals a complex pattern of genomic imprinting in mice. PLoS Genetics, 4(6), e1000091.PubMedCrossRefGoogle Scholar
  43. Wolf, J. B., & Hager, R. (2006). A maternal-offspring coadaptation theory for the evolution of genomic imprinting. PLoS Biology, 4, 380.CrossRefGoogle Scholar
  44. Wolf, J. B., Hager, R., & Cheverud, J. M. (2008b). Genomic imprinting effects on complex traits: A phenotype based perspective. Epigenetics, 3(6), 295–299.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Joseph Gyekis
    • 1
  • David A. Blizard
    • 1
  • Joseph T. Stout
    • 1
  • David J. Vandenbergh
    • 1
  • Gerald E. McClearn
    • 1
  • Reinmar Hager
    • 2
  1. 1.Department of Biobehavioral Health, College of Health and Human DevelopmentPennsylvania State UniversityUniversity ParkUSA
  2. 2.Computational and Evolutionary Biology, Faculty of Life SciencesUniversity of ManchesterManchesterUK

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