Abstract
Mating between relatives generally results in reduced offspring viability or quality, suggesting that selection should favor behaviors that minimize inbreeding. However, in natural populations where searching is costly or variation among potential mates is limited, inbreeding is often common and may have important consequences for both offspring fitness and phenotypic variation. In particular, offspring morphological variation often increases with greater parental relatedness, yet the source of this variation, and thus its evolutionary significance, are poorly understood. One proposed explanation is that inbreeding influences a developing organism’s sensitivity to its environment and therefore the increased phenotypic variation observed in inbred progeny is due to greater inputs from environmental and maternal sources. Alternatively, changes in phenotypic variation with inbreeding may be due to additive genetic effects alone when heterozygotes are phenotypically intermediate to homozygotes, or effects of inbreeding depression on condition, which can itself affect sensitivity to environmental variation. Here we examine the effect of parental relatedness (as inferred from neutral genetic markers) on heritable and nonheritable components of developmental variation in a wild bird population in which mate choice is often constrained, thereby leading to inbreeding. We found greater morphological variation and distinct contributions of variance components in offspring from highly related parents: inbred offspring tended to have greater environmental and lesser additive genetic variance compared to outbred progeny. The magnitude of this difference was greatest in late-maturing traits, implicating the accumulation of environmental variation as the underlying mechanism. Further, parental relatedness influenced the effect of an important maternal trait (egg size) on offspring development. These results support the hypothesis that inbreeding leads to greater sensitivity of development to environmental variation and maternal effects, suggesting that the evolutionary response to selection will depend strongly on mate choice patterns and population structure.
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Alatalo, R. V., Gustaffson, L., & Lundberg, A. (1990). Phenotypic selection on heritable size traits: Environmental variance and genetic response. American Naturalist, 135, 464–471.
Altwegg, R., Ringsby, T., & Saether, B. (2000). Phenotypic correlates and consequences of dispersal in a metapopulation of house sparrows Passer domesticus. Journal of Animal Ecology, 69, 762–770.
Ardia, D. R. (2005). Super size me: An experimental test of the factors affecting lipid content and the ability of residual body mass to predict lipid stores in nestling European Starlings. Functional Ecology, 19, 414–420.
Atchley, W. R. (1984). Ontogeny, timing of development, and genetic variance-covariance structure. American Naturalist, 123, 519–540.
Badyaev, A. V. (2005a). Maternal inheritance and rapid evolution of sexual size dimorphism: Passive effects or active strategies? American Naturalist, 166, S17–S30.
Badyaev, A. V. (2005b). Stress-induced variation in evolution: From behavioural plasticity to genetic assimilation. Proceedings of the Royal Society of London, Series B: Biological Sciences, 272, 877–886.
Badyaev, A. V., Hill, G. E., & Whittingham, L. A. (2001a). The evolution of sexual size dimorphism in the house finch. IV. Population divergence in ontogeny. Evolution, 55, 2534–2549.
Badyaev, A. V., Whittingham, L. A., & Hill, G. E. (2001b). The evolution of sexual size dimorphism in the house finch. III. Developmental basis. Evolution, 55, 176–189.
Badyaev, A. V., Hill, G. E., Beck, M. L., Dervan, A. A., Duckworth, R. A., McGraw, K. J., Nolan, P. M., & Whittingham, L. A. (2002). Sex-biased hatching order and adaptive population divergence in a passerine bird. Science, 295, 316–318.
Badyaev, A. V., Oh, K. P., & Mui, R. (2005). Evolution of sex-biased maternal effects in birds: II. Contrasting sex-specific oocyte competition in native and recently established populations. Journal of Evolutionary Biology, 19, 909–921.
Badyaev, A. V., Hamstra, T. L., Oh, K. P., & Acevedo Seaman, D. (2006). Sex-biased maternal effects reduce ectoparasite-induced mortality in a passerine bird. Proceedings of the National Academy of Sciences of the United States of America, 103, 14406–14411.
Balloux, F., Amos, W., & Coulson, T. (2004). Does heterozygosity estimate inbreeding in real populations? Molecular Ecology, 13, 3021–3031.
Blouin, M. S. (2003). DNA-based methods for pedigree reconstruction and kinship analysis in natural populations. Trends in Ecology & Evolution, 18, 503–511.
Blouin, S. F., & Blouin, M. S. (1988). Inbreeding avoidance behaviors. Trends in Ecology & Evolution, 3, 230–233.
Brown, W., & Roth, R. (2004). Juvenile survival and recruitment of wood thrushes Hylocichla mustelina in a forest fragment. Journal of Avian Biology, 35, 316–326.
Chakraborty, R., & Ryman, N. (1983). Relationship of mean and variance of genotypic values with heterozygosity per individual in a natural population. Genetics, 103, 149–152.
Charlesworth, D., & Charlesworth, B. (1987). Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics, 18, 237–268.
Charmantier, A., Perrins, C., McCleery, R. H., & Sheldon, B. C. (2006). Age-dependent genetic variation in a life-history trait in the mute swan. Proceedings of the Royal Society of London, Series B: Biological Sciences, 273, 225–232.
Cheverud, J. M. (1996). Developmental integration and the evolution of pleitropy. American Zoologist, 36, 44–50.
Cleveland, W. S., & Devlin, S. J. (1988). Locally weighted regression: An approach to regression analysis by local fitting. Journal of the American Statistical Association, 83, 596–610.
Coellho, A. M. (1985). Baboon dimorphism: Growth in weight, length and adiposity from birth to eight years of age. Monographs in Primatology, 6, 125–129.
Cooper, W. S., & Kaplan, R. H. (1982). Adaptive “coin-flipping”: A decision-theoretic examination of natural selection for random individual variation. Journal of Theoretical Biology, 94, 135–151.
David, P. (1999). A quantitative model of the relationship between phenotypic variance and heterozygosity at marker loci under partial selfing. Genetics, 153, 1463–1474.
David, P., Delay, B., & Jarne, P. (1997). Heterozygosity and growth in the marine bivalve Spisula ovalis: Testing alternative hypotheses. Genetical Research, 70, 215–223.
Deng, H-W. (1997). Increase in developmental instability upon inbreeding in Daphnia. Heredity, 78, 182–189.
Falconer, D. S., & Mackay, T. F. C. (1996). Introduction to quantitative genetics. London: Longman.
Fisher, R. A. (1930). The genetical theory of natural selection. Oxford, U.K.: Clarendon Press.
Fleischer, R. C., Johnson, R. F., & Klitz, W. J. (1983). Allozymic heterozygosity and morphological variation in house sparrows. Nature, 304, 628–630.
Foerster, K., Delhey, K., Johnsen, A., Lifjeld, J. T., & Kempenaers, B. (2003). Females increase offspring heterozygosity and fitness through extra-pair matings. Nature, 425, 714–717.
Gilmour, A. R., Gogel, B. J., Cullis, B. R., & Thompson, R. (2006). ASReml User Guide Release 2.0. Hemel Hempstead, HP1 1ES, UK: VSN International Ltd.
Goudet, J. (2001). FSTAT, a program to estimate and test gene diversities and fixation indices. Version 2.9.3.
Green, A. J. (2001). Mass/length residuals: Measures of body condition or generators of spurious results? Ecology, 82, 1473–1483.
Griffiths, R., Daan, S., & Dijkstra, C. (1996). Sex identification in birds using two CHD genes. Proceedings of the Royal Society of London, Series B: Biological Sciences, 263, 1251–1256.
Hadany, L., & Beker, T. (2003). Fitness-associated recombination on rugged adaptive landscapes. Journal of Evolutionary Biology, 16, 862–870.
Hall, B. K. (2005). Fifty years later: I. Michael Lerner’s Genetic Homeostasis (1954)–a valiant attempt to integrate genes, organisms and environment. Journal of Experimental Zoology, 304B, 187–197.
Hawley, D. M., Hanley, D., Dhondt, A. A., & Lovette, I. J. (2006). Molecular evidence for a founder effect in invasive house finch (Carpodacus mexicanus) populations experiencing an emergent disease epidemic. Molecular Ecology, 15, 263–275.
Hipfner, J. M., & Gaston, A. J. (1999). The relationship between egg size and posthatching development in the thick-billed murre. Ecology, 80, 1289–1297.
Hoffman, A. A., & Merilä, J. (1999). Heritable variation and evolution under favourable and unfavourable conditions. Trends in Ecology & Evolution, 14, 96–101.
Hoffman, A. A., & Parsons, P. A. (1991). Evolutionary genetics and environmental stress. Oxford, U.K.: Oxford University Press.
Jamieson, A., & Taylor, S. C. S. (1997). Comparisons of three probability formulae for parentage exclusion. Animal Genetics, 28, 397–400.
Johnsen, A., Andersen, V., Sunding, C., & Lifjeld, J. T. (2000). Female bluethroates enhance offspring immunocompetence through extra-pair copulations. Nature, 406, 296–299.
Kaplan, R. H., & Cooper, W. S. (1984). The evolution of developmental plasticity in reproductive characteristics: An application of the “adaptive coin-flipping” principle. American Naturalist, 123, 393–410.
Keller, L. F., & Arcese, P. (1998). No evidence for inbreeding avoidance in a natural population of song sparrows (Melospiza melodia). American Naturalist, 152, 380–392.
Keller, L. F., & Waller, D. M. (2002). Inbreeding effects in wild populations. Trends in Ecology & Evolution, 17, 230–241.
King, D. P. F. (1985). Enzyme heterozygosity associated with anatomical character variance and growth in the herring (Clupea harengus L.). Heredity, 54, 289–296.
Kirkpatrick, M., & Lande, R. (1989). The evolution of maternal characters. Evolution, 43, 485–503.
Kristensen, T. N., Sørensen, A. C., Sorensen, D., Pedersen, K. S., Sørensen, J. G., & Loeschcke, V. (2005). A test of quantitative genetic theory using Drosophila—effects of inbreeding and rate of inbreeding on heritabilities and variance components. Journal of Evolutionary Biology, 18, 763–770.
Kruuk, L. E. B. (2004). Estimating genetic parameters in natural populations using the ‘animal model’. Proceedings of the Royal Society of London Series B-Biological Sciences, 359, 873–890.
Kruuk, L. E. B., Sheldon, B. C., & Merilä, J. (2002). Severe inbreeding depression in collared flycatchers (Ficedula albicollis). Proceedings of the Royal Society of London, Series B: Biological Sciences, 269, 1581–1589.
Leary, R. J., Allendorf, F. W., & Knudsen, K. L. (1983). Superior developmental stability of heterozygotes at enzyme loci in salmonid fishes. American Naturalist, 124, 540–551.
Lerner, I. M. (1954). Genetic homeostasis. London: Oliver and Boyd.
Lessells, C. M., & Boag, P. (1987). Unrepeatable repeatabilities: A common mistake. Auk, 104, 116–121.
Levene, H. (1960). Robust tests for equality of variances. In I Olkin, SG Ghurye, W Heoffding, WG Madow, & HB Mann (Eds.), Contributions to probability and statistics (pp. 278–292). Stanford, CA USA: Stanford University Press.
Lindstedt, E., Oh, K. P., & Badyaev, A. V. (2006). Ecological, social, and genetic contingency of extrapair behavior in a socially monogmous bird. Journal of Avian Biology, 38, 214–238.
Maddox, J. D., & Weatherhead, P. J. (2008). Egg size variation in birds with asynchronous hatching: Is bigger really better? American Naturalist, 171, 358–365.
McCleery, R. H., Pettifor, R. A., Armbruster, P., Meyer, K., Sheldon, B. C., Perrins, & C. M. (2004). Components of variance underlying fitness in a natural population of the great tit Parus major. American Naturalist, 164, E62–E72.
McGinley, M. A., Temme, D. H., & Geber, M. A. (1987). Parental investment in offspring in variable environments: Theoretical and empirical considerations. American Naturalist, 130, 370–198.
Merilä, J. (1997). Expression of genetic variation in body size of the collared flycatcher under different environmental conditions. Evolution, 51, 526–536.
Merilä, J., Kruuk, L. E. B., & Sheldon, B. C. (2001). Natural selection on the genetical component of variance in body condition in a wild bird population. Journal of Evolutionary Biology, 14, 918–929.
Merilä, J., & Sheldon, B. C. (1999). Genetic architecture of fitness and nonfitness traits: Empirical patterns and development of ideas. Heredity, 83, 103–109.
Mitton, J. B. (1978). Relationship between heterozygosity for enzyme loci and variation of morphological characters in natural populations. Nature, 273, 661–662.
Mitton, J. B. (1993). Enzyme heterozygosity, metabolism, and developmental stability. Genetica, 89, 47–65.
Mitton, J. B., & Grant, M. C. (1984). Associations among protein heterozygosity, growth rate, and developmental homeostasis. Annual Review of Ecology and Systematics, 15, 479–499.
Mitton, J. B., & Pierce, B. A. (1980). The distribution of individual heterozygosity in natural populations. Genetics, 95, 1043–1054.
Møller, A. P., & Saino, N. (2004). Immune response and survival. Oikos, 104, 299–304.
Moses, L. E., Gale, L. C., & Altmann, J. (1992). Methods for analysis of unbalanced, longitudinal, growth data. American Journal of Primatology, 28, 49–59.
Mousseau, T. A., & Fox, C. W. (1998). The adaptive significance of maternal effects. Trends in Ecology & Evolution, 13, 403–407.
Oh, K. P., & Badyaev, A. V. (2006). Adaptive genetic complementarity in mate choice coexists with preference for elaborate sexual traits. Proceedings of the Royal Society of London, Series B: Biological Sciences, 273, 1913–1919.
Pemberton, J. (2004). Measuring inbreeding depression in the wild: The old ways are the best. Trends in Ecology & Evolution, 19, 613–615.
Potti, J. (1999). Maternal effects and the pervasive impact of nestling history on egg size in a passerine bird. Evolution, 53, 279–285.
Pusey, A., & Wolf, M. (1996). Inbreeding avoidance in animals. Trends in Ecology & Evolution, 11, 201–206.
Rasanen, K., & Kruuk, L. E. B. (2007). Maternal effects and evolution at ecological time-scales. Functional Ecology, 21, 408–421.
Réale, D., & Roff, D. A. (2003). Inbreeding, developmental stability, and canalization in the sand cricket Gryllus firmus. Evolution, 57, 597–605.
Reed, D. H., Lowe, E. H., Briscoe, D. A., & Frankham, R. (2003). Fitness and adaptation in a novel environment: Effect of inbreeding, prior environment, and lineage. Evolution, 57, 1822–1828.
Reed, W. L. (1999). Consequences of egg-size variation in the red-winged blackbird. Auk, 116, 549–552.
Ricklefs, R. E. (1973). Patterns of growth in birds. II. Growth rate and mode of development. Ibis, 115, 177–201.
Roff, D. A. (1997). Evolutionary quantitative genetics. New York: Chapman and Hall.
Roff, D. A. (1998). Effects of inbreeding on morphological and life history traits of the sand cricket, Gryllus firmus. Heredity, 81, 28–37.
Rousset, F. (2002). Inbreeding and relatedness coefficients: What do they measure? Heredity, 88, 371–380.
Saino, N., Calza, S., & Møller, A. P. (1997). Immunocompetence of nestling barn swallows in relation to brood size and parental effort. Journal of Animal Ecology, 66, 827–836.
Schmalhausen, I. I. (1949). Factors of evolution. Philadelphia, Pennsylvania: Blakiston.
Schulte-Hostedde, A. I., Zinner, B., Millar, J. S., & Hickling, G. J. (2005). Restitution of mass-size residuals: Validating body condition indices. Ecology, 86, 155–163.
Schultz, B. B. (1985). Levene’s test for relative variation. Systematic Zoology, 34, 449–456.
Setchell, J. M., Lee, P. C., Wickings, E. J., & Dixson, A. F. (2001). Growth and ontogeny of sexual size dimorphism in the mandrill (Mandrillus sphinx). American Journal of Physical Anthropology, 115, 349–360.
Shaw, R. G. (1991). The comparison of quantitative genetic parameters between populations. Evolution, 45, 143–151.
van de Casteele, T. V., Galbusera, P., & Matthysen, E. (2001). A comparison of microsatellite-based pairwise relatedness estimators. Molecular Ecology, 10, 1539–1549.
Wang, J. (2002). An estimator for pairwise relatedness using molecular markers. Genetics, 160, 1203–1215.
Wang, Z., Baker, A. J., Hill, G. E., & Edwards, S. V. (2003). Reconciling actual and inferred population histories in the house finch (Carpodacus mexicanus) by AFLP analysis. Evolution, 57, 2852–2864.
West-Eberhard, M. J. (2003). Developmental plasticity and evolution. Oxford University Press.
Whitlock, M. C., & Fowler, K. (1996). The distribution among populations in phenotypic variance with inbreeding. Evolution, 50, 1919–1926.
Whitlock, M. C., & Fowler, K. (1999). The changes in genetic and environmental variance with inbreeding in Drosophila melanogaster. Genetics, 152, 345–353.
Williams, T. D. (1994). Intraspecific variation in egg size and egg composition in birds: Effects on offspring fitness. Biological Reviews, 69, 35–59.
Wilson, A. J., Kruuk, L. E. B., & Coltman, D. W. (2005). Ontogenetic patterns in heritable variation for body size: Using random regression models in a wild ungulate population. American Naturalist, 166, E177–E192.
Wilson, A. J., & Réale, D. (2006). Ontogeny of additive and maternal genetic effects: Lessons from domestic mammals. American Naturalist, 167, E23–E38.
Wright, S. (1921). Systems of mating II. The effects of inbreeding on the genetic composition of a population. Genetics, 6, 124–143.
Yezerinac, S. M., Lougheed, S. C., & Handford, P. (1992). Morphological variability and enzyme heterozygosity: Individual and population level correlations. Evolution, 46, 1959–1964.
Young, R. L., & Badyaev, A. V. (2007). Evolution of ontogeny: Linking epigenetic remodeling and genetic adaptation in skeletal structures. Integrative and Comparative Biology, 47, 234–244.
Acknowledgments
We thank R. Young, D. Acevedo Seaman, R. Duckworth, J. Good, L. Reed, E. Landeen, and two anonymous reviewers for helpful suggestions that greatly improved the manuscript. We thank J. Hubbard, T. Hamstra, E. Lindstedt, J. Merkle, L. Mizstal, R. Mui, E. Solares, and C. Secomb for help with the fieldwork and molecular analyses. This study was funded by grants from the NSF (DEB-0075388, DEB-0077804, IOB-0218313), the Packard Foundation, and the James Silliman Memorial Research Award.
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Oh, K.P., Badyaev, A.V. Evolution of Adaptation and Mate Choice: Parental Relatedness Affects Expression of Phenotypic Variance in a Natural Population. Evol Biol 35, 111–124 (2008). https://doi.org/10.1007/s11692-008-9017-8
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DOI: https://doi.org/10.1007/s11692-008-9017-8