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The cost of inbreeding in Arabidopsis

Abstract

Population geneticists have long sought to estimate the distribution of selection intensities among genes of diverse function across the genome. Only recently have DNA sequencing and analytical techniques converged to make this possible. Important advances have come from comparing genetic variation within species (polymorphism) with fixed differences between species (divergence)1,2. These approaches have been used to examine individual genes for evidence of selection. Here we use the fact that the time since species divergence allows combination of data across genes. In a comparison of amino-acid replacements among species of the mustard weed Arabidopsis with those among species of the fruitfly Drosophila, we find evidence for predominantly beneficial gene substitutions in Drosophila but predominantly detrimental substitutions in Arabidopsis. We attribute this difference to the Arabidopsis mating system of partial self-fertilization, which corroborates a prediction of population genetics theory3,4,5,6 that species with a high frequency of inbreeding are less efficient in eliminating deleterious mutations owing to their reduced effective population size.

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Figure 1: Means of the posterior distributions of the selection parameters γ (dots) and the 95% credible intervals (vertical lines), in rank order according to the mean, for the genes in Arabidopsis (open circles) and Drosophila (filled circles).
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References

  1. McDonald, J. H. & Kreitman, M. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351, 652–654 (1991).

    Article  ADS  CAS  Google Scholar 

  2. Sawyer, S. A. & Hartl, D. L. Population genetics of polymorphism and divergence. Genetics 132, 1161–1176 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Charlesworth, D., Morgan, M. T. & Charlesworth, B. The effect of deleterious mutations on neutral molecular variation. J. Hered. 84, 321–325 (1993).

    Article  Google Scholar 

  4. Kondrashov, A. S. Muller's ratchet under epistatic selection. Genetics 136, 1469–1473 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Caballero, A. & Santiago, E. Response to selection from new mutation and effective size of partially inbred populations. I. Theoretical results. Genet. Res. 66, 213–225 (1995).

    Article  Google Scholar 

  6. Wang, J. L., Hill, W. G., Charlesworth, D. & Charlesworth, B. Dynamics of inbreeding depression due to deleterious mutations in small populations: Mutation parameters and inbreeding rate. Genet. Res. 74, 165–178 (1999).

    Article  CAS  Google Scholar 

  7. Hartl, D. L., Moriyama, E. N. & Sawyer, S. A. Selection intensity for codon bias. Genetics 138, 227–234 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Akashi, H. Inferring weak selection from patterns of polymorphism and divergence at ‘silent’ sites in Drosophila DNA. Genetics 139, 1067–1076 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Gelman, A., Carlin, J. S., Stern, H. S. & Rubin, D. B. Bayesian Data Analysis (Chapman & Hall, London, 1997).

    MATH  Google Scholar 

  10. Carlin, B. P. & Louis, T. A. Bayes and Empirical Bayes Methods for Data Analysis (Chapman & Hall, London, 2000).

    Book  Google Scholar 

  11. Gilks, R., Richardson, S. & Spiegelhalter, D. J. Markov Chain Monte Carlo in Practice (Chapman & Hall, London, 1996).

    MATH  Google Scholar 

  12. Metropolis, N., Rosenbluth, A. W., Rosenbluth, M. N., Teller, A. H. & Teller, E. Equations of state calculations by fast computing machines. J. Chem. Phys. 21, 1087–1091 (1953).

    Article  ADS  CAS  Google Scholar 

  13. Geman, S. & Geman, D. Stochastic relaxation, Gibbs distributions and the Bayesian restoration of images. IEEE Trans. Pattern Anal. Machine Intell. 6, 721–741 (1984).

    Article  CAS  Google Scholar 

  14. Gelman, A. & Rubin, D. B. Inference from iterative simulation using multiple sequences. Statist. Sci. 7, 457–511 (1992).

    Article  ADS  Google Scholar 

  15. Abbott, R. J. & Gomes, M. F. Population genetic structure and the outcrossing rate of Arabidopsis thaliana. Heredity 62, 411–418 (1989).

    Article  Google Scholar 

  16. Savolainen, O., Langley, C. H., Lazzaro, B. P. & Freville, H. Contrasting patterns of nucleotide polymorphism at the Adh locus in the outcrossing Arabidopsis lyrata and the selfing Arabidopsis thaliana. Mol. Biol. Evol. 17, 645–655 (2000).

    Article  CAS  Google Scholar 

  17. Kusaba, M. et al. Self-incompatibility in the genus Arabidopsis: Characterization of the S locus in the outcrossing A. lyrata and its autogamous relative A. thaliana. Plant Cell 13, 627–643 (2001).

    Article  CAS  Google Scholar 

  18. Caccone, A., Amato, G. D. & Powell, J. R. Rates and patterns of scnDNA and mtDNA divergence within the Drosophila melanogaster subgroup. Genetics 118, 671–683 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank D. Weinreich and D. Rand for providing the Drosophila data, and A. Kondrashov for numerous suggestions for improving the presentation. This work was supported by grants from the US Public Health Service, the US National Science Foundation, Howard Hughes and Marshall Sherfield Fellowships to C.D.B., and an Alfred P. Sloan Foundation Young Investigator Award to M.D.P.

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Correspondence to Daniel L. Hartl.

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Additional supplementary information accompanies this paper on the authors' website http://www.oeb.harvard.edu/hartl/lab. (TXT 5 kb)

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Bustamante, C., Nielsen, R., Sawyer, S. et al. The cost of inbreeding in Arabidopsis. Nature 416, 531–534 (2002). https://doi.org/10.1038/416531a

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