Abstract
Theoretical and experimental studies have provided evidence for a positive role of phenotype resistance to genetic mutation in enhancing long-term adaptation to novel environments. With the aim of contributing to an understanding of the origin and evolution of phenotypic robustness to genetic mutations in organismal systems, we adopted a theoretical approach, elaborating on a classical mathematical formalizations of evolutionary dynamics, the quasispecies model. We show that a certain level of phenotypic robustness is not only a favourable condition for adaptation to occur, but also a required condition for short-term adaptation in most real organismal systems. This appears as a threshold effect, i.e. as a minimum level of phenotypic robustness (critical robustness) below which evolutionary adaptation cannot consistently occur or be maintained, even in the case of sizably selection coefficients and in the absence of any drift effect. These results, are in agreement with the observed pervasiveness of robustness at different levels of biological organization, from molecules to whole organisms.
Similar content being viewed by others
References
Ahnert, S. E. (2017). Structural properties of genotype–phenotype maps. Journal of the Royal Society Interface, 14(132), 20170275.
Barve, A., & Wagner, A. (2013). A latent capacity for evolutionary innovation through exaptation in metabolic systems. Nature, 500(7461), 203.
Boyle, E. A., Li, Y. I., & Pritchard, J. K. (2017). An expanded view of complex traits: From polygenic to omnigenic. Cell, 169(7), 1177–1186.
Bull, J. J., Meyers, L. A., & Lachmann, M. (2005). Quasispecies made simple. PLoS Computational Biology, 1(6), e61.
Cerf, R., & Dalmau, J. (2018). The quasispecies for the Wright–Fisher model. Evolutionary Biology, 45, 318–323.
Denver, D. R., Morris, K., Lynch, M., & Thomas, W. K. (2004). High mutation rate and predominance of insertions in the caenorhabditis elegans nuclear genome. Nature, 430(7000), 679.
Draghi, J. A., Parsons, T. L., Wagner, G. P., & Plotkin, J. B. (2010). Mutational robustness can facilitate adaptation. Nature, 463(7279), 353–355.
Draghi, J. A., Parsons, T. L., & Plotkin, J. B. (2011). Epistasis increases the rate of conditionally neutral substitution in an adapting population. Genetics, 187(4), 1139–1152.
Drake, J. W., Charlesworth, B., Charlesworth, D., & Crow, J. F. (1998). Rates of spontaneous mutation. Genetics, 148(4), 1667–1686.
Edwards, J. S., & Palsson, B. O. (2000). Robustness analysis of the Escherichia coli metabolic network. Biotechnology Progress, 16(6), 927–939.
Eigen, M., McCaskill, J., & Schuster, P. (1989). The molecular quasi-species. Advances in Chemichal Physics, 75, 149–263.
Fares, M. A. (2015). The origins of mutational robustness. Trends in Genetics, 31(7), 373–381.
Félix, M. A., & Barkoulas, M. (2015). Pervasive robustness in biological systems. Nature Reviews Genetics, 16(8), 483–496.
Foster, P. L. (2007). Stress-induced mutagenesis in bacteria. Critical Reviews in Biochemistry and Molecular Biology, 42(5), 373–397.
Fusco, G., & Minelli, A. (2010). Phenotypic plasticity in development and evolution: Facts and concepts. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 1540, 547–556.
Galhardo, R. S., Hastings, P. J., & Rosenberg, S. M. (2007). Mutation as a stress response and the regulation of evolvability. Critical Reviews in Biochemistry and Molecular Biology, 42(5), 399–435.
Giaever, G., Chu, A. M., Ni, L., Connelly, C., Riles, L., Veronneau, S., et al. (2002). Functional profiling of the Saccharomyces cerevisiae genome. Nature, 418(6896), 387.
Gibson, G., & Reed, L. K. (2008). Cryptic genetic variation. Current Biology, 18(21), R989–R990.
Gorodetsky, P., & Tannenbaum, E. (2008). Effect of mutators on adaptability in time-varying fitness landscapes. Physical Review E, 77(4), 042901.
Green, R. M., Fish, J. L., Young, N. M., Smith, F. J., Roberts, B., Dolan, K., et al. (2017). Developmental nonlinearity drives phenotypic robustness. Nature Communications, 8, 1970.
Hansen, T. F. (2006). The evolution of genetic architecture. Annual Review of Ecology, Evolution, and Systematics, 37, 123–157.
Hayden, E. J., Ferrada, E., & Wagner, A. (2011). Cryptic genetic variation promotes rapid evolutionary adaptation in an RNA enzyme. Nature, 474(7349), 92–95.
Hermisson, J., & Wagner, G. P. (2004). The population genetic theory of hidden variation and genetic robustness. Genetics, 168(4), 2271–2284.
Kingsolver, J. G., Hoekstra, H. E., Hoekstra, J. M., Berrigan, D., Vignieri, S. N., Hill, C., et al. (2001). The strength of phenotypic selection in natural populations. The American Naturalist, 157(3), 245–261.
Kitano, H. (2004). Biological robustness. Nature Reviews Genetics, 5(11), 826–837.
Klingenberg, C. P. (2019). Phenotypic plasticity, developmental instability, and robustness: The concepts and how they are connected. Frontiers in Ecology and Evolution, 7, 56.
Mathieson, I., & McVean, G. (2013). Estimating selection coefficients in spatially structured populations from time series data of allele frequencies. Genetics, 193(3), 973–984.
Mayer, C., & Hansen, T. F. (2017). Evolvability and robustness: A paradox restored. Journal of Theoretical Biology, 430, 78–85.
Nielsen, R., & Yang, Z. (2003). Estimating the distribution of selection coefficients from phylogenetic data with applications to mitochondrial and viral DNA. Molecular Biology and Evolution, 20(8), 1231–1239.
Nijhout, H. F., & Davidowitz, G. (2003). Developmental perspectives on phenotypic variation, canalization, and fluctuating asymmetry. In M. Polak (Ed.), Developmental instability: Causes and consequences (pp. 3–13). New York: Oxford University Press.
Nilsson, M., & Snoad, N. (2002). Quasispecies evolution on a fitness landscape with a fluctuating peak. Physical Review E, 65(3), 031901.
Nowak, M. A. (2006). Evolutionary dynamics. Cambridge, MA: Harvard University Press.
Orr, H. A. (2000). Adaptation and the cost of complexity. Evolution, 54(1), 13–20.
Orr, H. A. (2005). The genetic theory of adaptation: A brief history. Nature Reviews Genetics, 6(2), 119–127.
Pavlicev, M., & Wagner, G. P. (2012). A model of developmental evolution: Selection, pleiotropy and compensation. Trends in Ecology & Evolution, 27(6), 316–322.
Pavlicev, M., Kenney-Hunt, J. P., Norgard, E. A., Roseman, C. C., Wolf, J. B., & Cheverud, J. M. (2008). Genetic variation in pleiotropy: Differential epistasis as a source of variation in the allometric relationship between long bone lengths and body weight. Evolution: International Journal of Organic Evolution, 62(1), 199–213.
Payne, J. L., & Wagner, A. (2019). The causes of evolvability and their evolution. Nature Reviews Genetics, 20, 24–38.
Raj, A., Peskin, C. S., Tranchina, D., Vargas, D. Y., & Tyagi, S. (2006). Stochastic mRNA synthesis in mammalian cells. PLoS Biology, 4(10), e309.
Raser, J. M., & O’Shea, E. K. (2005). Noise in gene expression: Origins, consequences, and control. Science, 309(5743), 2010–2013.
Reidys, C., Forst, C. V., & Schuster, P. (2001). Replication and mutation on neutral networks. Bulletin of Mathematical Biology, 63(1), 57–94.
Rennell, D., Bouvier, S. E., Hardy, L. W., & Poteete, A. R. (1991). Systematic mutation of bacteriophage t4 lysozyme. Journal of Molecular Biology, 222(1), 67–88.
Rigato, E., & Fusco, G. (2016). Enhancing effect of phenotype mutational robustness on adaptation in Escherichia coli. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 326(1), 31–37.
Rodrigues, J. F. M., & Wagner, A. (2009). Evolutionary plasticity and innovations in complex metabolic reaction networks. PLoS Computational Biology, 5(12), e1000613.
Sasaki, A., & Nowak, M. A. (2003). Mutation landscapes. Journal of Theoretical Biology, 224(2), 241–247.
Shikov, A. E., Skitchenko, R. K., Predeus, A. V., & Barbitoff, Y. A. (2020). Phenome-wide functional dissection of pleiotropic effects highlights key molecular pathways for human complex traits. Scientific Reports, 10(1), 1–10.
Sinha, N., & Nussinov, R. (2001). Point mutations and sequence variability in proteins: Redistributions of preexisting populations. Proceedings of the National Academy of Sciences USA, 98(6), 3139–3144.
Stelling, J., Sauer, U., Szallasi, Z., Doyle, F. J., & Doyle, J. (2004). Robustness of cellular functions. Cell, 118(6), 675–685.
Szamecz, B., Boross, G., Kalapis, D., Kovács, K., Fekete, G., Farkas, Z., et al. (2014). The genomic landscape of compensatory evolution. PLoS Biology, 12(8), e1001935.
Tachida, H. (2000). Dna evolution under weak selection. Gene, 261(1), 3–9.
Takeuchi, N., Poorthuis, P. H., & Hogeweg, P. (2005). Phenotypic error threshold; additivity and epistasis in RNA evolution. BMC Evolutionary Biology, 5(1), 9.
Tamuri, A. U., dos Reis, M., & Goldstein, R. A. (2012). Estimating the distribution of selection coefficients from phylogenetic data using sitewise mutation-selection models. Genetics, 190(3), 1101–1115.
Tanaka, K. M., Hopfen, C., Herbert, M. R., Schlötterer, C., Stern, D. L., Masly, J. P., et al. (2015). Genetic architecture and functional characterization of genes underlying the rapid diversification of male external genitalia between Drosophila simulans and Drosophila mauritiana. Genetics, 200(1), 357–369.
Turelli, M. (2017). Fisher’s infinitesimal model: A story for the ages. Theoretical Population Biology, 118, 46–49.
Vachias, C., Fritsch, C., Pouchin, P., Bardot, O., & Mirouse, V. (2014). Tight coordination of growth and differentiation between germline and soma provides robustness for drosophila egg development. Cell Reports, 9(2), 531–541.
Visscher, P. M., & Yang, J. (2016). A plethora of pleiotropy across complex traits. Nature Genetics, 48(7), 707.
Wagner, A. (2005). Distributed robustness versus redundancy as causes of mutational robustness. Bioessays, 27(2), 176–188.
Wagner, A. (2008). Robustness and evolvability: A paradox resolved. Proceedings of the Royal Society of London B: Biological Sciences, 275(1630), 91–100.
Wagner, A. (2011). The origins of evolutionary innovations: A theory of transformative change in living systems. Oxford: OUP.
Wagner, A. (2012). The role of robustness in phenotypic adaptation and innovation. Proceedings of the Royal Society of London B Biological Sciences, 279(1732), 1249–1258.
Wagner, A. (2013). Robustness and evolvability in living systems. Princeton: Princeton University Press.
Wagner, G. P., & Zhang, J. (2011). The pleiotropic structure of the genotype-phenotype map: The evolvability of complex organisms. Nature Reviews Genetics, 12(3), 204–213.
Wagner, G. P., Kenney-Hunt, J. P., Pavlicev, M., Peck, J. R., Waxman, D., & Cheverud, J. M. (2008). Pleiotropic scaling of gene effects and the ‘cost of complexity’. Nature, 452(7186), 470–472.
Walsh, B., & Lynch, M. (2018). Evolution and selection of quantitative traits. Oxford: Oxford University Press.
Wang, Z., Liao, B. Y., & Zhang, J. (2010). Genomic patterns of pleiotropy and the evolution of complexity. Proceedings of the National Academy of Sciences, 107(42), 18034–18039.
White, J. K., Gerdin, A. K., Karp, N. A., Ryder, E., Buljan, M., Bussell, J. N., et al. (2013). Genome-wide generation and systematic phenotyping of knockout mice reveals new roles for many genes. Cell, 154(2), 452–464.
Wild, G., & Traulsen, A. (2007). The different limits of weak selection and the evolutionary dynamics of finite populations. Journal of Theoretical Biology, 247(2), 382–390.
Wilke, C. O. (2005). Quasispecies theory in the context of population genetics. BMC Evolutionary biology, 5(1), 44.
Wu, B., Altrock, P. M., Wang, L., & Traulsen, A. (2010). Universality of weak selection. Physical Review E, 82(4), 046106.
Zheng, J., Payne, J. L., & Wagner, A. (2019). Cryptic genetic variation accelerates evolution by opening access to diverse adaptive peaks. Science, 365(6451), 347–353.
Acknowledgements
This work has been supported by a Grant from the Italian Ministry of Education, University and Research (MIUR) to GF. Mihaela Pavlicev provided insightful comments on a previous version of the article.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Rigato, E., Fusco, G. Effects of Phenotypic Robustness on Adaptive Evolutionary Dynamics. Evol Biol 47, 233–239 (2020). https://doi.org/10.1007/s11692-020-09506-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11692-020-09506-w