Abstract
Evolvability, the ability of a biological system to respond to selection, has recently become a key concept in evolutionary developmental biology and an integral part of the vocabulary of a budding extended evolutionary synthesis. While some of the theoretical principles behind the evolvability of complex organisms have been established, there are also several aspects of it that remain controversial. How does evolvability itself evolve? Is evolvability constrained by mutation? Can current definitions account for evolutionary innovations?
Here, I will describe some of the research programs dedicated to the study of evolvability of complex organisms. I will then establish its relationship with modularity and robustness and conclude with questions about the nature of evolvability that remain unresolved. My aim is to show that research in evolvability has become integrative in nature and that this change has been aided by an increasing incorporation of the genotype-to-phenotype map into the variation-based evolutionary theory.
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References
Alberch P (1991) From genes to phenotype: dynamical systems and evolvability. Genetica 84(1):5–11
Arendt D, Musser JM, Baker CV, Bergman A, Cepko C, Erwin DH, Pavlicev M, Schlosser G, Widder S, Laubichler MD, Wagner GP (2016) The origin and evolution of cell types. Nat Rev Genet 17(12):744–757
Blows MW, McGuigan K (2015) The distribution of genetic variance across phenotypic space and the response to selection. Mol Ecol 24(9):2056–2072
Cheverud JM (1988) A comparison of genetic and phenotypic correlations. Evolution 42(5):958–968
Dawkins R (1988) The evolution of evolvability. In: Langton C (ed) Artificial life: the proceedings of an interdiciplinary workshop on the synthesis and simulation of living systems. Addison Wesley, Santa Fe, pp 202–220
Draghi JA, Parsons TL, Wagner GP, Plotkin JB (2010) Mutational robustness can facilitate adaptation. Nature 463(7279):353–355
Garcia-Gonzalez F, Simmons LW, Tomkins JL, Kotiaho JS, Evans JP (2012) Comparing evolvabilities: common errors surrounding the calculation and use of coefficients of additive genetic variation. Evolution 66(8):2341–2349
Gerhart J, Kirschner M (1997) Cells, embryos, and evolution: toward a cellular and developmental understanding of phenotypic variation and evolutionary adaptability, vol 575.21 GER. Blackwell Science, Malden
Gould SJ (1966) Allometry and size in ontogeny and phylogeny. Biol Rev 41(4):587–638
Hansen TF (2006) The evolution of genetic architecture. Annu Rev Ecol Evol S 37:123–157. https://doi.org/10.1146/annurev.ecolsys.37.091305.110224
Hansen TF, Houle D (2008) Measuring and comparing evolvability and constraint in multivariate characters. J Evol Biol 21(5):1201–1219
Hill WG (1982) Rates of change in quantitative traits from fixation of new mutations. Proc Natl Acad Sci 79(1):142–145
Houle D (1992) Comparing evolvability and variability of quantitative traits. Genetics 130(1):195–204
Houle D, Bolstad GH, van der Linde K, Hansen TF (2017) Mutation predicts 40 million years of fly wing evolution. Nature 548(7668):447–450
Lande R (1979) Quantitative genetic-analysis of multivariate evolution, applied to brain – body size allometry. Evolution 33(1):402–416
Leamy LJ, Routman EJ, Cheverud JM (1999) Quantitative trait loci for early-and late-developing skull characters in mice: a test of the genetic independence model of morphological integration. Am Nat 153(2):201–214
Lynch VJ, Leclerc RD, May G, Wagner GP (2011) Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat Genet 43(11):1154–1159
Marroig G, Cheverud JM (2005) Size as a line of least evolutionary resistance: diet and adaptive morphological radiation in new world monkeys. Evolution 59(5):1128–1142
Müller GB, Streicher J (1989) Ontogeny of the syndesmosis tibiofibularis and the evolution of the bird hindlimb: a caenogenetic feature triggers phenotypic novelty. Anat Embryol 179(4):327–339
Nuño de la Rosa L (2017) Computing the extended synthesis: mapping the dynamics and conceptual structure of the evolvability research front. J Exp Zool Part B Mol Dev Evol 328:395–411
Pavličev M, Cheverud JM (2015) Constraints evolve: context dependency of gene effects allows evolution of pleiotropy. Annu Rev Ecol Evol Syst 46(1):413–434. https://doi.org/10.1146/annurev-ecolsys-120213-091721
Pavlicev M, Wagner GP (2012) Coming to grips with evolvability. Evol Educ Outreach 5(2):231–244
Pavlicev M, Kenney-Hunt JP, Norgard EA, Roseman CC, Wolf JB, Cheverud JM (2008) Genetic variation in pleiotropy: differential epistasis as a source of variation in the allometric relationship between long bone lengths and body weight. Evolution 62(1):199–213
Pavlicev M, Cheverud JM, Wagner GP (2010) Evolution of adaptive phenotypic variation patterns by direct selection for evolvability. Proc R Soc Lond B Biol Sci 278:1903–1912. https://doi.org/10.1098/rspb.2010.2113
Pigliucci M (2008) Is evolvability evolvable? Nat Rev Genet 9(1):75–82
Pigliucci M, Muller GB (2010) Evolution-the extended synthesis. MIT Press, Cambridge, Massachusetts, vol 576.82 E9.
Rasmussen S, Knudsen C, Feldberg R, Hindsholm M (1990) The coreworld: emergence and evolution of cooperative structures in a computational chemistry. Physica D 42(1–3):111–134
Schluter D (1996) Adaptive radiation along genetic lines of least resistance. Evolution 50(5):1766–1774
Schuster P, Fontana W, Stadler PF, Hofacker IL (1994) From sequences to shapes and back: a case study in RNA secondary structures. Proc R Soc Lond B Biol Sci 255(1344):279–284
True JR, Haag ES (2001) Developmental system drift and flexibility in evolutionary trajectories. Evol Dev 3(2):109–119
Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150(3811):563–565
Wagner GP, Altenberg L (1996) Perspective: complex adaptations and the evolution of evolvability. Evolution 50(3):967–976
Wagner GP, Lynch VJ (2010) Evolutionary novelties. Curr Biol 20(2):R48–R52
Wagner GP, Zhang J (2011) The pleiotropic structure of the genotype–phenotype map: the evolvability of complex organisms. Nat Rev Genet 12(3):204–213
Walsh B, Blows MW (2009) Abundant genetic variation+ strong selection= multivariate genetic constraints: a geometric view of adaptation. Annu Rev Ecol Evol Syst 40:41–59
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Porto, A. (2018). Variational Approaches to Evolvability: Short- and Long-Term Perspectives. In: Nuno de la Rosa, L., Müller, G. (eds) Evolutionary Developmental Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-33038-9_114-1
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DOI: https://doi.org/10.1007/978-3-319-33038-9_114-1
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