Recombination drives the evolution of mutational robustness

Wagner, 2005 Gibson, 2000, Canalization in evolutionary genetics: a stabilizing theory?, Bioessays, 22, 372, 10.1002/(SICI)1521-1878(200004)22:4<372::AID-BIES7>3.0.CO;2-J Wagner, 1997, A population genetic theory of canalization, Evolution, 51, 329, 10.1111/j.1558-5646.1997.tb02420.x Mayer, 2017, Evolvability and robustness: a paradox restored, J Theor Biol, 430, 78, 10.1016/j.jtbi.2017.07.004 Wagner, 2008, Robustness and evolvability: a paradox resolved, Proc Biol Sci, 275, 91 Wilke, 2001, Evolution of digital organisms at high mutation rates leads to survival of the flattest, Nature, 412, 331, 10.1038/35085569 Codoñer, 2006, The fittest versus the flattest: experimental confirmation of the quasispecies effect with subviral pathogens, PLoS Pathog, 2, e136, 10.1371/journal.ppat.0020136 Sanjuán, 2007, Selection for robustness in mutagenized RNA viruses, PLoS Genet, 3, e93, 10.1371/journal.pgen.0030093 Meiklejohn, 2002, A single mode of canalization, Trends Ecol Evol, 17, 468, 10.1016/S0169-5347(02)02596-X Endler, 1977, Geographic variation, speciation, and clines, Monogr Popul Biol, 10, 1 Burton, 1990, Hybrid breakdown in developmental time in the copepod tigriopus californicus, Evolution, 44, 1814, 10.1111/j.1558-5646.1990.tb05252.x Breeuwer, 1995, Hybrid breakdown between two haplodiploid species: the role of nuclear and cytoplasmic genes, Evolution, 49, 705, 10.1111/j.1558-5646.1995.tb02307.x Gibson, 2013, Genetic and developmental basis of F2 hybrid breakdown in Nasonia parasitoid wasps, Evolution, 67, 2124, 10.1111/evo.12080 Kvitek, 2011, Reciprocal sign epistasis between frequently experimentally evolved adaptive mutations causes a rugged fitness landscape, PLoS Genet, 7, e1002056, 10.1371/journal.pgen.1002056 de Visser, 2014, Empirical fitness landscapes and the predictability of evolution, Nat Rev Genet, 15, 480, 10.1038/nrg3744 Corbett-Detig, 2013, Genetic incompatibilities are widespread within species, Nature, 504, 135, 10.1038/nature12678 Collaborative Cross Consortium, 2012, The genome architecture of the Collaborative Cross mouse genetic reference population, Genetics, 190, 389, 10.1534/genetics.111.132639 Srivastava, 2017, Genomes of the mouse collaborative cross, Genetics, 206, 537, 10.1534/genetics.116.198838 Azevedo, 2006, Sexual reproduction selects for robustness and negative epistasis in artificial gene networks, Nature, 440, 87, 10.1038/nature04488 Misevic, 2006, Sexual reproduction reshapes the genetic architecture of digital organisms, Proc Biol Sci, 273, 457 Martin, 2009, Effects of recombination on complex regulatory circuits, Genetics, 183, 673, 10.1534/genetics.109.104174 Whitlock, 2016, An evolving genetic architecture interacts with hill-robertson interference to determine the benefit of sex, Genetics, 203, 923, 10.1534/genetics.116.186916 Fisher, 1930 Yang, 2017, Genetic interaction network as an important determinant of gene order in genome evolution, Mol Biol Evol, 34, 3254, 10.1093/molbev/msx264 Osbourn, 2009, Operons. Cell Mol Life Sci, 66, 3755, 10.1007/s00018-009-0114-3 Wong, 2005, Birth of a metabolic gene cluster in yeast by adaptive gene relocation, Nat Genet, 37, 777, 10.1038/ng1584 Field, 2008, Metabolic diversification—independent assembly of operon-like gene clusters in different plants, Science, 320, 543, 10.1126/science.1154990 Cascales, 2007, Colicin biology, Microbiol Mol Biol Rev, 71, 158, 10.1128/MMBR.00036-06 Nuckolls, 2017, Wtf genes are prolific dual poison-antidote meiotic drivers, Elife, 6, 10.7554/eLife.26033 Pál, 2003, Evidence for co-evolution of gene order and recombination rate, Nat Genet, 33, 392, 10.1038/ng1111 McGaugh, 2012, Genomic impacts of chromosomal inversions in parapatric Drosophila species, Philos Trans R Soc Lond B Biol Sci, 367, 422, 10.1098/rstb.2011.0250 Hooper, 2017, Chromosomal inversion differences correlate with range overlap in passerine birds, Nat Ecol Evol, 1, 1526, 10.1038/s41559-017-0284-6 Kirubakaran, 2016, Two adjacent inversions maintain genomic differentiation between migratory and stationary ecotypes of Atlantic cod, Mol Ecol, 25, 2130, 10.1111/mec.13592 Joron, 2011, Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry, Nature, 477, 203, 10.1038/nature10341 Jay, 2018, Supergene evolution triggered by the introgression of a chromosomal inversion, Curr Biol, 28, 1839, 10.1016/j.cub.2018.04.072 Wang, 2013, A Y-like social chromosome causes alternative colony organization in fire ants, Nature, 493, 664, 10.1038/nature11832 Weinreich, 2006, Darwinian evolution can follow only very few mutational paths to fitter proteins, Science, 312, 111, 10.1126/science.1123539 Bank, 2016, On the (un) predictability of a large intragenic fitness landscape, Proc Natl Acad Sci Unit States Am, 113, 14085, 10.1073/pnas.1612676113 Li, 2016, The fitness landscape of a tRNA gene, Science, 352, 837, 10.1126/science.aae0568 Domingo, 2018, Pairwise and higher-order genetic interactions during the evolution of a tRNA, Nature, 558, 117, 10.1038/s41586-018-0170-7 Poon, 2005, The coupon collector and the suppressor mutation: estimating the number of compensatory mutations by maximum likelihood, Genetics, 170, 1323, 10.1534/genetics.104.037259 Sackman, 2018, Additive phenotypes underlie epistasis of fitness effects, Genetics, 208, 339, 10.1534/genetics.117.300451 Vale, 2012, The distribution of mutational fitness effects of phage φX174 on different hosts, Evolution, 66, 3495, 10.1111/j.1558-5646.2012.01691.x Lindsey, 2013, Evolutionary rescue from extinction is contingent on a lower rate of environmental change, Nature, 494, 463, 10.1038/nature11879 Gorter, 2018, Local fitness landscapes predict yeast evolutionary dynamics in directionally changing environments, Genetics, 208, 307, 10.1534/genetics.117.300519 Chou, 2011, Diminishing returns epistasis among beneficial mutations decelerates adaptation, Science, 332, 1190, 10.1126/science.1203799 Kalirad, 2017, Spiraling complexity: a test of the snowball effect in a computational model of RNA folding, Genetics, 206, 377, 10.1534/genetics.116.196030 Nghe, 2018, Sign epistasis caused by hierarchy within signalling cascades, Nat Commun, 9, 1451, 10.1038/s41467-018-03644-8 Lohaus, 2010, Genetic architecture and the evolution of sex, J Hered, 101, S142, 10.1093/jhered/esq013 Lang, 2013, Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations, Nature, 500, 571, 10.1038/nature12344 Good, 2017, The dynamics of molecular evolution over 60,000 generations, Nature, 551, 45, 10.1038/nature24287 Watson, 2011, Genome structure and the benefit of sex, Evolution, 65, 523, 10.1111/j.1558-5646.2010.01144.x Lynch, 1998 Morley, 2017, Dynamics of molecular evolution in RNA virus populations depend on sudden versus gradual environmental change, Evolution, 71, 872, 10.1111/evo.13193 Buskirk, 2017, Hitchhiking and epistasis give rise to cohort dynamics in adapting populations, Proc Natl Acad Sci USA, 10.1073/pnas.1702314114 Malmberg, 1977, The evolution of epistasis and the advantage of recombination in populations of bacteriophage T4, Genetics, 86, 607, 10.1093/genetics/86.3.607 de Visser, 2009, Exploring the effect of sex on empirical fitness landscapes, Am Nat, 174, S15, 10.1086/599081 Crow, 1956, Genetics of DDT resistance in Drosophila, 408 Moradigaravand, 2014, Recombination accelerates adaptation on a large-scale empirical fitness landscape in HIV-1, PLoS Genet, 10, e1004439, 10.1371/journal.pgen.1004439 Qi, 2004, A gene cluster for secondary metabolism in oat: implications for the evolution of metabolic diversity in plants, Proc Natl Acad Sci U S A, 101, 8233, 10.1073/pnas.0401301101 Costanzo, 2016, A global genetic interaction network maps a wiring diagram of cellular function, Science, 353