Recurrent self-fertilization is thought to lead to reduced adaptive potential by decreasing the genetic diversity of populations, thus leading selfing lineages down an evolutionary "blind alley." Although well supported theoretically, empirical support for reduced adaptability in selfing species is limited. One limitation of classical theoretical models is that they assume pure additivity of the fitness-related traits that are under stabilizing selection, despite ample evidence that quantitative traits are subject to dominance. Here, we relax this assumption and explore the effect of dominance on a fitness-related trait under stabilizing selection for populations that differ in selfing rates. By decomposing the genetic variance into additional components specific to inbred populations, we show that dominance components can explain a substantial part of the genetic variance of inbred populations. We also show that ignoring these components leads to an upward bias in the predicted response to selection. Finally, we show that when considering the effect of dominance, the short-term evolutionary potential of populations remains comparable across the entire gradient in outcrossing rates, and genetic associations can even make selfing populations more evolvable on the longer term, reconciling theoretical, and empirical results.

AGAP Univ Montpellier CIRAD INRAE Institut Agro Montpellier 34000 France

Department of Biology Lund University Lund SE 223 62 Sweden

Department of Botany Charles University Prague Czechia

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Abney, M., M. S. McPeek, and C. Ober. 2000. Estimation of variance components of quantitative traits in inbred populations. The American Journal of Human Genetics 66:629-650.

Abu Awad, D., and S. Billiard. 2017. The double edged sword: The demographic consequences of the evolution of self-fertilization. Evolution 71:1178-1190.

Abu Awad, D., and D. Roze. 2018. Effects of partial selfing on the equilibrium genetic variance, mutation load, and inbreeding depression under stabilizing selection. Evolution 72:751-769.

Ashman, T. L., and C. J. Majetic. 2006. Genetic constraints on floral evolution: a review and evaluation of patterns. Heredity 96:343-352.

Baker, H. G. 1955. Self-compatibility and establishment after ‘long-distance’ dispersal. Evolution 9:347-349.

Barrett, S. C. 2003. Mating strategies in flowering plants: the outcrossing-selfing paradigm and beyond. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 358:991-1004.

Bulmer, M. G. 1974. Linkage disequilibrium and genetic variability. Genetics Research 23:281-289.

Bürger, R., G. P. Wagner, and F. Stettinger. 1989. How much heritable variation can be maintained in finite populations by mutation-selection balance? Evolution 43:1748-1766.

Carter, A. J., J. Hermisson, and T. F. Hansen. 2005. The role of epistatic gene interactions in the response to selection and the evolution of evolvability. Theoretical population biology 68 :179-196.

Charlesworth, D., and B. Charlesworth. 1995. Quantitative genetics in plants: the effect of the breeding system on genetic variability. Evolution 49:911-920.

Cheptou, P. O. 2004. Allee effect and self-fertilization in hermaphrodites: reproductive assurance in demographically stable populations. Evolution 58:2613-2621.

Cheptou, P. O. 2019. Does the evolution of self-fertilization rescue populations or increase the risk of extinction?. Annals of botany 123:337-345.

Cheptou, P. O. 2021. Pollination strategies in the face of pollinator decline. Botany Letters 1-8.

Class, B., and J. E. Brommer. 2020. Can dominance genetic variance be ignored in evolutionary quantitative genetic analyses of wild populations? Evolution.

Clo, J., L. Gay, and J. Ronfort. 2019. How does selfing affect the genetic variance of quantitative traits? An updated meta-analysis on empirical results in angiosperm species. Evolution.

Clo, J., J. Ronfort, and D. Abu Awad. 2020. Hidden genetic variance contributes to increase the short-term adaptive potential of selfing populations. Journal of Evolutionary Biology 33:1203-1215.

Cockerham, C. C., and B. S. Weir. 1984. Covariances of relatives stemming from a population undergoing mixed self and random mating. Biometrics: 157-164.

Dolgin, E. S., B. Charlesworth, S. E. Baird, and A. D. Cutter. 2007. Inbreeding and outbreeding depression in caenorhabditis nematodes. Evolution 61:1339-1352.

Eckert, C. G., K. E. Samis, and S. Dart. 2006. Reproductive assurance and the evolution of uniparental reproduction in flowering plants. Ecology and evolution of flowers 183:203.

Edwards, J. W., and K. R. Lamkey. 2002. Quantitative genetics of inbreeding in a synthetic maize population. Crop Science 42:1094-1104.

Falconer, D. S., and T. F. C. Mackay. 1996. Introduction to quantitative genetics. Pearson Education Limited, Edimbourg, U.K.

Fisher, R. A. 1941. Average excess and average effect of a gene substitution. Annals of Eugenics 11:53-63.

Gay, L., M. Siol, and J. Ronfort. 2013. Pedigree-free estimates of heritability in the wild: promising prospects for selfing populations. PloS one 8:e66983.

Geber, M. A., and L. R. Griffen. 2003. Inheritance and natural selection on functional traits. International Journal of Plant Sciences 164:S21-S42.

Gimond, C., R. Jovelin, S. Han, C. Ferrari, A. D. Cutter, and C. Braendle. 2013. Outbreeding depression with low genetic variation in selfing caenorhabditis nematodes. Evolution 67:3087-3101.

Glémin, S. 2003. How are deleterious mutations purged? Drift versus nonrandom mating. Evolution 57:2678-2687.

Goldberg, E. E., J. R. Kohn, R. Lande, K. A. Robertson, S. A. Smith, and B. Igić. 2010. Species Selection Maintains Self-Incompatibility. Science 330:493.

Griffin, P. C., and Y. Willi. 2014. Evolutionary shifts to self-fertilisation restricted to geographic range margins in North American Arabidopsis lyrata. Ecology Letters 17:484-490.

Grossenbacher, D., R. Briscoe Runquist, E. E. Goldberg, and Y. Brandvain. 2015. Geographic range size is predicted by plant mating system. Ecology letters 18:706-713.

Haldane, J. B. S. 1924. A mathematical theory of natural and artificial selection. Part II the influence of partial self-fertilisation, inbreeding, assortative mating, and selective fertilisation on the composition of mendelian populations, and on natural selection. Biological Reviews 1:158-163.

Hansen, T. F., C. Pélabon, and D. Houle. 2011. Heritability is not evolvability. Evolutionary Biology 38:258.

Hill, W. G., M. E. Goddard, and P. M. Visscher. 2008. Data and theory point to mainly additive genetic variance for complex traits. PLoS Genet 4:e1000008.

Hoeschele, I., and A. R. Vollema. 1993. Estimation of variance components with dominance and inbreeding in dairy cattle. Journal of Animal Breeding and Genetics 110:93-104.

Holeski, L. M., and J. K. Kelly. 2006. Mating system and the evolution of quantitative traits: an experimental study of Mimulus guttatus. Evolution 60:711-723.

Igic, B., and J. R. Kohn. 2006. The distribution of plant mating systems: study bias against obligately outcrossing species. Evolution 60:1098-1103.

Igic, B., and J. W. Busch. 2013. Is self-fertilization an evolutionary dead end?. New Phytologist 198:386-397.

Jullien, M., M. Navascués, J. Ronfort, K. Loridon, and L. Gay. 2019. Structure of multilocus genetic diversity in predominantly selfing populations. Heredity 123:176-191.

Keightley, P. D., and T. M. Bataillon. 2000. Multigeneration Maximum-Likelihood Analysis Applied to Mutation-Accumulation Experiments in Caenorhabditis elegans. Genetics 154:1193.

Kelly, J. K. 1999a. Response to selection in partially self-fertilizing populations. I. Selection on a single trait. Evolution 53:336-349.

Kelly, J. K. 1999b. Response to selection in partially self-fertilizing populations. II. Selection on multiple traits. Evolution 53:350-357.

Kelly, J. K. 2003. Deleterious mutations and the genetic variance of male fitness components in Mimulus guttatus. Genetics 164:1071-1085.

Kelly, J. K., and H. S. Arathi. 2003. Inbreeding and the genetic variance in floral traits of Mimulus guttatus. Heredity 90:77.

Kelly, J. K., and S. Williamson. 2000. Predicting response to selection on a quantitative trait: a comparison between models for mixed-mating populations. Journal of theoretical biology 207:37-56.

Kingsolver, J. G., H. E. Hoekstra, J. M. Hoekstra, D. Berrigan, S. N. Vignieri, C. E. Hill, … & P. Beerli. 2001. The strength of phenotypic selection in natural populations. The American Naturalist 157:245-261.

Lande, R. 1977. The influence of the mating system on the maintenance of genetic variability in polygenic characters. Genetics 86:485-498.

Lande, R. 1979. Quantitative genetic analysis of multivariate evolution, applied to brain: body size allometry. Evolution: 402-416.

Lande, R., and E. Porcher. 2015. Maintenance of quantitative genetic variance under partial self-fertilization, with implications for evolution of selfing. Genetics 200:891-906.

Lynch, M. 1988. The rate of polygenic mutation. Genetics Research 51:137-148.

Lynch, M., and B. Walsh. 1998. Genetics and analysis of quantitative traits. Sinauer Sunderland, MA.

Marriage, T. N., and J. K. Kelly. 2009. Inbreeding depression in an asexual population of Mimulus guttatus. Journal of Evolutionary Biology 22:2320-2331.

Martínez-Padilla, J., A. Estrada, R. Early, and F. García-González. 2017. Evolvability meets biogeography: evolutionary potential decreases at high and low environmental favourability. Proceedings of the Royal Society B: Biological Sciences 284:20170516.

Mittelbach, G. G., D. W. Schemske, H. V. Cornell, A. P. Allen, J. M. Brown, M. B. Bush, et al. 2007. Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecology Letters 10:315-331.

Merilä, J., L. E. B. Kruuk, and B. C. Sheldon. 2001. Natural selection on the genetical component of variance in body condition in a wild bird population. Journal of Evolutionary Biology 14:918-929.

Moeller, D. A., R. D. Briscoe Runquist, A. M. Moe, M. A. Geber, C. Goodwillie, P. O. Cheptou, …, A. A. Winn. 2017. Global biogeography of mating system variation in seed plants. Ecology Letters 20:375-384.

Mullin, T. J., E. K. Morgenstern, Y. S. Park, and D. P. Fowler. 1992. Genetic parameters from a clonally replicated test of black spruce (Picea mariana). Canadian Journal of Forest Research 22:24-36.

Nietlisbach, P., L. F. Keller, and E. Postma. 2016. Genetic variance components and heritability of multiallelic heterozygosity under inbreeding. Heredity 116:1-11.

Noël, E., P. Jarne, S. Glémin, A. MacKenzie, A. Segard, V. Sarda, et al. 2017. Experimental evidence for the negative effects of self-fertilization on the adaptive potential of populations. Current Biology 27:237-242.

Opedal, Ø. H. 2019. Evolutionary Potential of Herkogamy. eLS: 1-8.

Opedal, Ø. H., G. H. Bolstad, T. F. Hansen, W. S. Armbruster, and C. Pélabon. 2017. The evolvability of herkogamy: Quantifying the evolutionary potential of a composite trait. Evolution 71:1572-1586.

Peterson, M. L., and K. M. Kay. 2015. Mating system plasticity promotes persistence and adaptation of colonizing populations of hermaphroditic angiosperms. The American Naturalist 185:28-43.

Rhode, J. M., and M. B. Cruzan. 2005. Contributions of Heterosis and Epistasis to Hybrid Fitness. The American Naturalist 166:E124-E139.

Rieseberg, L. H., M. A. Archer, and R. K. Wayne. 1999. Transgressive segregation, adaptation and speciation. Heredity 83:363-372.

Ronce, O., F. H. Shaw, F. Rousset, and R. G. Shaw. 2009. Is inbreeding depression lower in maladapted populations? a quantitative genetics model. Evolution 63:1807-1819.

Shaw, R. G., D. L. Byers, and F. H. Shaw. 1998. Genetic components of variation in Nemophila menziesii undergoing inbreeding: morphology and flowering time. Genetics 150:1649-1661.

Shaw, F. H., C. J. Geyer, and R. G. Shaw. 2002. A comprehensive model of mutations affecting fitness and inferences for arabidopsis thaliana. Evolution 56:453-463.

Siepielski, A. M., M. B. Morrissey, M. Buoro, S. M. Carlson, C. M. Caruso, S. M. Clegg, et al. 2017. Precipitation drives global variation in natural selection. Science 355:959-962.

Silva, J. C., C. Hardner, and B. M. Potts. 2010. Genetic variation and parental performance under inbreeding for growth in Eucalyptus globulus. Annals of Forest Science 67:606-606.

Siol, M., J. M. Prosperi, I. Bonnin, and J. Ronfort. 2008. How multilocus genotypic pattern helps to understand the history of selfing populations: a case study in Medicago truncatula. Heredity 100:517.

Stebbins, G. L. 1957. Self fertilization and population variability in the higher plants. The American Naturalist 91:337-354.

Takebayashi, N., and P. L. Morrell. 2001. Is self-fertilization an evolutionary dead end? revisiting an old hypothesis with genetic theories and a macroevolutionary approach. American Journal of Botany 88:1143-1150.

Waldmann, P., J. Hallander, F. Hoti, and M. J. Sillanpää. 2008. Efficient Markov chain Monte Carlo implementation of Bayesian analysis of additive and dominance genetic variances in noninbred pedigrees. Genetics 179:1101-1112.

Walsh, B., and M. Lynch. 2018. Evolution and selection of quantitative traits. Oxford University Press.

Whitehead, M. R., R. Lanfear, R. J. Mitchell, and J. D. Karron. 2018. Plant mating systems often vary widely among populations. Frontiers in Ecology and Evolution 6:38.

Wolak, M. E., and L. F. Keller. 2014. Dominance genetic variance and inbreeding in natural populations. Quantitative genetics in the wild: 104-127.

Wright, S. 1931. Evolution in Mendelian populations. Genetics 16:97.

Wright, A. J., and C. C. Cockerham. 1985. Selection with partial selfing. I. Mass selection. Genetics 109:585-597.

Wright, S. I., S. Kalisz, and T. Slotte. 2013. Evolutionary consequences of self-fertilization in plants. Proc R Soc B 280:20130133.

The evolution of the additive variance of a trait under stabilizing selection after autopolyploidization

Fitness consequences of hybridization in a predominantly selfing species: insights into the role of dominance and epistatic incompatibilities

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