Robustness and evolution: concepts, insights and challenges from a developmental model system
Open accessAbstract
Robustness, the persistence of an organismal trait under perturbations, is a ubiquitous property of complex living systems. We here discuss key concepts related to robustness with examples from vulva development in the nematode Caenorhabditis elegans. We emphasize the need to be clear about the perturbations a trait is (or is not) robust to. We discuss two prominent mechanistic causes of robustness, namely redundancy and distributed robustness. We also discuss possible evolutionary causes of robustness, one of which does not involve natural selection. To better understand robustness is of paramount importance for understanding organismal evolution. Part of the reason is that highly robust systems can accumulate cryptic variation that can serve as a source of new adaptations and evolutionary innovations. We point to some key challenges in improving our understanding of robustness.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Many biochemical networks are robust-remarkably stable under changes in external conditions and internal reaction parameters.
“The functioning of many biochemical networks is often robust - remarkably stable under changes in external conditions and internal reaction parameters.”
From Sloppiness, robustness, and evolvability in systems biology (2008) · cites this paper as [5]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Principles of Population Genetics.
Cormack, R. M., Hartl, D. L., & Clark, A. G. (1990) · Biometrics · doi:10.2307/2531471 · Cited by 5,283 · see citing works
Systematic functional analysis of the Caenorhabditis elegans genome using RNAi
Kamath, R. S., Fraser, A. G., Yan, D., Poulin, G. B., Durbin, R. M., Gotta, M., Kanapin, A. A., Bot, N. L., Moreno, S., Sohrmann, M., et al. (2003) · Nature · doi:10.1038/nature01278 · Cited by 3,542 · see citing works
Post-embryonic cell lineages of the nematode, Caenorhabditis elegans
Sulston, J. E., & Horvitz, H. R. (1977) · Developmental Biology · doi:10.1016/0012-1606(77)90158-0 · Cited by 3,479 · see citing works
CANALIZATION OF DEVELOPMENT AND THE INHERITANCE OF ACQUIRED CHARACTERS
WADDINGTON, C. H. (1942) · Nature · doi:10.1038/150563a0 · Cited by 3,255 · cited 5× · see citing works
“…uncover it is to experimentally drive the system out of its buffered range, using either environmental challenges such as heat shock or ether exposure as in the classical experiments by Waddington (Waddington 1942; Gibson and Hogness 1996), or mutations (Rutherford 2000; Gibson and Dworkin 2004).”
BackgroundMethodInfluentialPurification and Characterization
Tsai, C. S. (2006) · Biomacromolecules · doi:10.1002/0470080124.ch3 · Cited by 2,368 · see citing works
Comparing evolvability and variability of quantitative traits.
Houle, D. (1992) · Genetics · doi:10.1093/genetics/130.1.195 · Cited by 1,984 · see citing works
Robustness in simple biochemical networks
Barkai, N., & Leibler, S. (1997) · Nature · doi:10.1038/43199 · Cited by 1,513 · see citing works
Evolution of phenotypic plasticity: where are we going now?
Pigliucci, M. (2005) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2005.06.001 · Cited by 1,269 · see citing works
The segment polarity network is a robust developmental module
von Dassow, G., Meir, E., Munro, E. M., & Odell, G. M. (2000) · Nature · doi:10.1038/35018085 · Cited by 1,144 · see citing works
Fitness Landscapes and the Origin of Species
Sergey Gavrilets, B. (2004) · Cited by 1,058 · see citing works
Fitness Landscapes and the Origin of Species (MPB-41)
Sergey Gavrilets, B. (2004) · Princeton University Press eBooks · doi:10.1515/9780691187051 · Cited by 1,056 · see citing works
THE MOLECULAR BASIS OF DOMINANCE
KACSER, H., & Burns, J. A. (1981) · Genetics · doi:10.1093/genetics/97.3-4.639 · Cited by 1,040 · see citing works
Robustness and Evolvability in Living Systems
Wagner, A. (2005) · Princeton University Press eBooks · doi:10.1515/9781400849383 · Cited by 975 · see citing works
Self-citationIt’s a noisy business! Genetic regulation at the nanomolar scale
McAdams, H. H., & Arkin, A. P. (1999) · Trends in Genetics · doi:10.1016/s0168-9525(98)01659-x · Cited by 848 · see citing works
Principles of Population Genetics
Cazes, M.-H., Hartl, D. L., & Clark, A. (1999) · Population · doi:10.2307/1534724 · Cited by 761 · see citing works
PERSPECTIVE: EVOLUTION AND DETECTION OF GENETIC ROBUSTNESS
de Visser, J. A. G. M., Hermisson, J., Wagner, G. P., Ancel, L. W., Bagheri, H. C., Blanchard, J. L., Chao, L., Cheverud, J. M., Elena, S. F., Fontana, W., et al. (2003) · Evolution · doi:10.1111/j.0014-3820.2003.tb00377.x · Cited by 695 · see citing works
Self-citationWaddington's canalization revisited: Developmental stability and evolution
Siegal, M. L., & Bergman, A. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.102303999 · Cited by 640 · see citing works
Mapping phenotypes: canalization, plasticity and developmental stability
Debat, V., & David, P. (2001) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(01)02266-2 · Cited by 614 · cited 1× · see citing works
“For further reading on different aspects of biological robustness and canalization, a non-exhaustive list of more extensive reviews includes: Gibson and Wagner 2000; Debat and David 2001; de Visser et al. 2003; Gibson and Dworkin 2004; Flatt 2005; Wagner 2005a; Dworkin 2005a.”
BackgroundRobustness and evolvability in living systems
(2006) · Choice Reviews Online · doi:10.5860/choice.43-4658 · Cited by 580 · see citing works
Neutral evolution of mutational robustness
van Nimwegen, E., Crutchfield, J. P., & Huynen, M. A. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.17.9716 · Cited by 568 · see citing works
A POPULATION GENETIC THEORY OF CANALIZATION
Wagner, G. P., Booth, G., & Bagheri, H. C. (1997) · Evolution · doi:10.1111/j.1558-5646.1997.tb02420.x · Cited by 561 · see citing works
Regulation and cell autonomy during postembryonic development of Caenorhabditis elegans
Sulston, J. E., & White, J. G. (1980) · Developmental Biology · doi:10.1016/0012-1606(80)90353-x · Cited by 560 · see citing works
Ferguson, E. L., & Horvitz, H. R. (1985) · Genetics · doi:10.1093/genetics/110.1.17 · Cited by 547 · see citing works
Uncovering cryptic genetic variation
Gibson, G., & Dworkin, I. (2004) · Nature Reviews Genetics · doi:10.1038/nrg1426 · Cited by 546 · cited 4× · see citing works
“Gibson and Hogness 1996), or mutations (Rutherford 2000; Gibson and Dworkin 2004).”
BackgroundInfluentialPERSPECTIVE: SPONTANEOUS DELETERIOUS MUTATION
Lynch, M., Blanchard, J. L., Houle, D., Kibota, T. T., Schultz, S. T., Vassilieva, L. L., & Willis, J. H. (1999) · Evolution · doi:10.1111/j.1558-5646.1999.tb05361.x · Cited by 467 · see citing works
Robustness of the BMP morphogen gradient in Drosophila embryonic patterning
Eldar, A., Dorfman, R., Weiss, D., Ashe, H. L., Shilo, B., & Barkai, N. (2002) · Nature · doi:10.1038/nature01061 · Cited by 465 · see citing works
The Evolutionary Genetics of Canalization
Flatt, T. (2005) · The Quarterly Review of Biology · doi:10.1086/432265 · Cited by 459 · see citing works
Genetic and Environmental Regulation of Dauer Larva DevelopmentPreprint
Riddle, D. L., & Albert, P. S. (1997) · Cold Spring Harbor Monograph Archive · doi:10.1101/087969532.33.739 · Cited by 453 · see citing works
Gerhart, J. C., & Kirschner, M. W. (1997) · Cited by 437 · see citing works
McVean, G. T. (1997) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(97)89823-4 · Cited by 394 · see citing works
PERSPECTIVE:EVOLUTION AND DETECTION OF GENETIC ROBUSTNESS
de Visser, J. A. G. M., Hermisson, J., Wagner, G. P., et al. (2003) · Evolution · doi:10.1554/02-750r · Cited by 364 · see citing works
Fighting change with change: adaptive variation in an uncertain world
Ancel, L. W., & Bull, J. J. (2002) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(02)02633-2 · Cited by 359 · see citing works
DOES EVOLUTIONARY PLASTICITY EVOLVE?
Wagner, A. (1996) · Evolution · doi:10.1111/j.1558-5646.1996.tb02342.x · Cited by 341 · see citing works
Self-citationHigh mutation rate and predominance of insertions in the Caenorhabditis elegans nuclear genome
Denver, D. R., Morris, K., Lynch, M., & Thomas, W. K. (2004) · Nature · doi:10.1038/nature02697 · Cited by 340 · see citing works
Robustness, evolvability, and neutrality
Wagner, A. (2005) · FEBS Letters · doi:10.1016/j.febslet.2005.01.063 · Cited by 317 · see citing works
Self-citationLIMITS OF ADAPTATION: THE EVOLUTION OF SELECTIVE NEUTRALITY
Hartl, D. L., Dykhuizen, D. E., & Dean, A. M. (1985) · Genetics · doi:10.1093/genetics/111.3.655 · Cited by 298 · see citing works
Yoon, C. H., Lee, J., Jongeward, G. D., & Sternberg, P. W. (1995) · Science · doi:10.1126/science.7652556 · Cited by 291 · see citing works
Distributed robustness versus redundancy as causes of mutational robustness
Wagner, A. (2005) · BioEssays · doi:10.1002/bies.20170 · Cited by 290 · see citing works
Self-citationSelf-Enhanced Ligand Degradation Underlies Robustness of Morphogen Gradients
Eldar, A., Rosin, D., Shilo, B.-Z., & Barkai, N. (2003) · Developmental Cell · doi:10.1016/s1534-5807(03)00292-2 · Cited by 289 · see citing works
Ferguson, E. L., & Horvitz, H. R. (1989) · Genetics · doi:10.1093/genetics/123.1.109 · Cited by 258 · see citing works
Berset, T., Fröhli, E., Battu, G., Canevascini, S., & Hajnal, A. (2001) · Science · doi:10.1126/science.1055642 · Cited by 257 · see citing works
Eisenmann, D. M., Maloof, J., Simske, J. S., Kenyon, C. J., & Kim, S. K. (1998) · Development · doi:10.1242/dev.125.18.3667 · Cited by 256 · see citing works
Crosstalk Between the EGFR and LIN-12/Notch Pathways in C. elegans Vulval Development
Yoo, A. S. J., Bais, C., & Greenwald, I. (2004) · Science · doi:10.1126/science.1091639 · Cited by 255 · see citing works
Redundancy, antiredundancy, and the robustness of genomes
Krakauer, D. C., & Plotkin, J. B. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.032668599 · Cited by 254 · see citing works
Sternberg, P. W. (2005) · WormBook · doi:10.1895/wormbook.1.6.1 · Cited by 252 · see citing works
Meiklejohn, C. D., & Hartl, D. L. (2002) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(02)02596-x · Cited by 251 · see citing works
Sexual reproduction selects for robustness and negative epistasis in artificial gene networks
Azevedo, R. B. R., Lohaus, R., Srinivasan, S., Dang, K. K., & Burch, C. L. (2006) · Nature · doi:10.1038/nature04488 · Cited by 226 · see citing works
How should we explain variation in the genetic variance of traits?
Houle, D. (1998) · Genetica · doi:10.1023/a:1017034925212 · Cited by 219 · see citing works
Chen, N., & Greenwald, I. (2004) · Developmental Cell · doi:10.1016/s1534-5807(04)00021-8 · Cited by 212 · see citing works
How should we explain variation in the genetic variance of traits?
Houle, D. (1998) · Contemporary issues in genetics and evolution · doi:10.1007/978-94-011-5210-5_20 · Cited by 204 · see citing works
Different Levels of the C. elegans growth factor LIN-3 promote distinct vulval precursor fates
Katz, W. S., Hill, R. J., Clandinin, T. R., & Sternberg, P. W. (1995) · Cell · doi:10.1016/0092-8674(95)90317-8 · Cited by 204 · see citing works
THE FITNESS EFFECTS OF SPONTANEOUS MUTATIONS IN CAENORHABDITIS ELEGANS
Vassilieva, L. L., Hook, A. M., & Lynch, M. F. (2000) · Evolution · doi:10.1111/j.0014-3820.2000.tb00557.x · Cited by 196 · see citing works
Robustness, Flexibility, and the Role of Lateral Inhibition in the Neurogenic Network
Meir, E., von Dassow, G., Munro, E., & Odell, G. M. (2002) · Current Biology · doi:10.1016/s0960-9822(02)00839-4 · Cited by 193 · see citing works
Effect of Polymorphism in the Drosophila Regulatory Gene Ultrabithorax on Homeotic Stability
Gibson, G. C., & Hogness, D. S. (1996) · Science · doi:10.1126/science.271.5246.200 · Cited by 176 · see citing works
Sundaram, M. V. (2006) · WormBook · doi:10.1895/wormbook.1.80.1 · Cited by 163 · see citing works
To be or not to be active: the stochastic nature of enhancer action
Fiering, S., Whitelaw, E., & Martin, D. I. K. (2000) · BioEssays · doi:10.1002/(sici)1521-1878(200004)22:4 · Cited by 159 · see citing works
Endocytosis-mediated downregulation of LIN-12/Notch upon Ras activation in Caenorhabditis elegans
Shaye, D. D., & Greenwald, I. (2002) · Nature · doi:10.1038/nature01234 · Cited by 154 · see citing works
Adaptive Evolution on Neutral Networks
Wilke, C. O. (2001) · Bulletin of Mathematical Biology · doi:10.1006/bulm.2001.0244 · Cited by 128 · see citing works
Sequential signalling during Caenorhabditis elegans vulval induction
Simske, J. S., & Kirn, S. K. (1995) · Nature · doi:10.1038/375142a0 · Cited by 127 · see citing works
The Opportunity for Canalization and the Evolution of Genetic Networks
Proulx, S. R., & Phillips, P. C. (2005) · The American Naturalist · doi:10.1086/426873 · Cited by 113 · see citing works
Milton, C. C., Huynh, B., Batterham, P., Rutherford, S. L., & Hoffmann, A. A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1835613100 · Cited by 112 · see citing works
Ohmachi, M., Rocheleau, C. E., Church, D. L., Lambie, E. J., Schedl, T., & Sundaram, M. V. (2002) · Current Biology · doi:10.1016/s0960-9822(02)00690-5 · Cited by 111 · see citing works
ARK-1 Inhibits EGFR Signaling in C. elegans
Hopper, N. A., Lee, J., & Sternberg, P. W. (2000) · Molecular Cell · doi:10.1016/s1097-2765(05)00001-8 · Cited by 107 · see citing works
Dworkin, I. M., Pálsson, A., Birdsall, K., & Gibson, G. C. (2003) · Current Biology · doi:10.1016/j.cub.2003.10.001 · Cited by 98 · see citing works
Inhibition ofCaenorhabditis elegansvulval induction bygap-1and bylet-23receptor tyrosine kinasePreprint
Hajnal, A., Whitfield, C. W., & Kim, S. K. (1997) · Genes & Development · doi:10.1101/gad.11.20.2715 · Cited by 96 · see citing works
Evolutionary preservation of redundant duplicated genes
Krakauer, D. C., & Nowak, M. A. (1999) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.1999.0337 · Cited by 92 · see citing works
Wagner, A. (2000) · Genetics · doi:10.1093/genetics/154.3.1389 · Cited by 91 · see citing works
Self-citationChanges of Induction and Competence During the Evolution of Vulva Development in Nematodes
Sommer, R. J., & Sternberg, P. W. (1994) · Science · doi:10.1126/science.8016644 · Cited by 89 · see citing works
Berset, T., Fröhli, E., & Hajnal, A. (2005) · Genes & Development · doi:10.1101/gad.333505 · Cited by 87 · see citing works
Mosaic analysis of the let-23 gene function in vulval induction of Caenorhabditis elegans
Koga, M., & Ohshima, Y. (1995) · Development · doi:10.1242/dev.121.8.2655 · Cited by 86 · see citing works
Delattre, M., & Félix, M. (2001) · Current Biology · doi:10.1016/s0960-9822(01)00202-0 · Cited by 86 · see citing works
Self-citationDworkin, I. (2005) · Evolution; international journal of organic evolution · doi:10.1111/j.0014-3820.2005.tb01799.x · Cited by 78 · see citing works
Genetic measurement theory of epistatic effects
Wagner, G. P., Laubichler, M. D., & Bagheri, H. C. (1998) · Contemporary issues in genetics and evolution · doi:10.1007/978-94-011-5210-5_43 · Cited by 75 · see citing works
Canalization, Cryptic Variation, and Developmental Buffering
Dworkin, I. M. (2005) · Elsevier eBooks · doi:10.1016/b978-012088777-4/50010-7 · Cited by 72 · see citing works
Naturally occurring genetic variation affects Drosophila photoreceptor determination
Polaczyk, P., Gasperini, R., & Gibson, G. C. (1998) · Development Genes and Evolution · doi:10.1007/s004270050137 · Cited by 67 · see citing works
Two nested gonadal inductions of the vulva in nematodes
Félix, M., & Sternberg, P. W. (1997) · Development · doi:10.1242/dev.124.1.253 · Cited by 63 · see citing works
Self-citationIntercellular coupling amplifies fate segregation during Caenorhabditis elegans vulval development
Giurumescu, C. A., Sternberg, P. W., & Asthagiri, A. R. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506476103 · Cited by 59 · see citing works
A perfect vulva every time: Gradients and signaling cascades in C. elegans
Kenyon, C. J. (1995) · Cell · doi:10.1016/0092-8674(95)90302-x · Cited by 58 · see citing works
Genetic and Environmental Regulation of Dauer Larva Development -- C. elegans II
Riddle, D. L., Blumenthal, T., Meyer, B. J., & Priess (1997) · Cited by 58 · see citing works
Kao, G., Tuck, S., Baillie, D. L., & Sundaram, M. V. (2004) · Development · doi:10.1242/dev.00987 · Cited by 48 · see citing works
Galton and identification by fingerprints.
Stigler, S. M. (1995) · Genetics · doi:10.1093/genetics/140.3.857 · Cited by 43 · see citing works
Ferguson, E. L., & Horvitz, H. R. (1989) · Trends in Genetics · doi:10.1016/0168-9525(89)90158-3 · Cited by 41 · see citing works
Moghal, N., Garcia, L. R., Khan, L. A., Iwasaki, K., & Sternberg, P. W. (2003) · Development · doi:10.1242/dev.00670 · Cited by 39 · see citing works
Evolution of nematode development
Sommer, R. J. (2000) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(00)00110-6 · Cited by 37 · see citing works
A mechanistic study of evolvability using the mitogen‐activated protein kinase cascade
Nijhout, H. F., Berg, A., & Gibson, W. T. (2003) · Evolution & Development · doi:10.1046/j.1525-142x.2003.03035.x · Cited by 31 · see citing works
Effects of epistasis on phenotypic robustness in metabolic pathways
Bagheri, H. C., Hermisson, J., Vaišnys, J. R., & Wagner, G. P. (2003) · Mathematical Biosciences · doi:10.1016/s0025-5564(03)00057-9 · Cited by 28 · see citing works
Snell, E. A., Scemama, J., & Stellwag, E. J. (1999) · Journal of Experimental Zoology · doi:10.1002/(sici)1097-010x(19990415)285:1 · Cited by 25 · see citing works
Self-citationMediterranean pollution: one man's optimism
Walgate, R. (1978) · Nature · doi:10.1038/271200a0 · Cited by 2 · see citing works
Evolution of developmental mechanisms.
Ferrier, D. E. K., & Shimeld, S. M. (2002) · Genome biology · doi:10.1186/gb-2002-3-7-reports4020 · Cited by 2 · see citing works
Flagged first, then by citations
3 of the 93 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Dynamic reconfiguration of human brain networks during learning
Bassett, D. S., Wymbs, N. F., Porter, M. A., Mucha, P. J., Carlson, J. M., & Grafton, S. T. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1018985108 · Cited by 1,705 · see citing works
Understanding complexity in the human brain
Bassett, D. S., & Gazzaniga, M. S. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.03.006 · Cited by 572 · see citing works
Cryptic genetic variation: evolution's hidden substrate
Paaby, A. B., & Rockman, M. V. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3688 · Cited by 500 · see citing works
Fluctuating Asymmetry: Methods, Theory, and Applications
Graham, J. H., Raz, S., Hel-Or, H. Z., & Nevo, E. (2010) · Symmetry · doi:10.3390/sym2020466 · Cited by 421 · see citing works
Late seed maturation: drying without dying
Leprince, O., Pellizzaro, A., Berriri, S., & Buitink, J. (2016) · Journal of Experimental Botany · doi:10.1093/jxb/erw363 · Cited by 334 · see citing works
PHENOTYPIC PLASTICITY AND EPIGENETIC MARKING: AN ASSESSMENT OF EVIDENCE FOR GENETIC ACCOMMODATION
Schlichting, C. D., & Wund, M. A. (2014) · Evolution · doi:10.1111/evo.12348 · Cited by 284 · see citing works
Hidden Reaction Norms, Cryptic Genetic Variation, and Evolvability
Schlichting, C. D. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1438.010 · Cited by 261 · see citing works
Kvitek, D. J., & Sherlock, G. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003972 · Cited by 228 · see citing works
Brunetti, C., Fini, A., Sebastiani, F., Gori, A., & Tattini, M. (2018) · Frontiers in Plant Science · doi:10.3389/fpls.2018.01042 · Cited by 229 · see citing works
Evolutionary plasticity of segmentation clock networks
Krol, A., Roellig, D., Dequéant, M., Tassy, O., Glynn, E. F., Hattem, G. L., Mushegian, A. R., Oates, A. C., & Pourquié, O. (2011) · Development · doi:10.1242/dev.063834 · Cited by 194 · see citing works
Sensitivity, robustness, and identifiability in stochastic chemical kinetics models
Komorowski, M., Costa, M. J., Rand, D. A. J., & Stumpf, M. P. H. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1015814108 · Cited by 196 · see citing works
Sloppiness, robustness, and evolvability in systems biology
Daniels, B. C., Chen, Y.-J., Sethna, J. P., Gutenkunst, R. N., & Myers, C. R. (2008) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2008.06.008 · Cited by 192 · see citing works
Biological Robustness: Paradigms, Mechanisms, and Systems Principles
Whitacre, J. M. (2012) · Frontiers in Genetics · doi:10.3389/fgene.2012.00067 · Cited by 182 · see citing works
Eco-Evo-Devo: The Time Has Come
Abouheif, E., Favé, M.-J., Ibarraran-Viniegra, A. S., Lesoway, M. P., Rafiqi, A. M., & Rajakumar, R. (2013) · Advances in experimental medicine and biology · doi:10.1007/978-94-007-7347-9_6 · Cited by 170 · see citing works
Partial penetrance facilitates developmental evolution in bacteria
Eldar, A., Chary, V. K., Xenopoulos, P., Fontes, M. E., Losón, O. C., Dworkin, J. E., Piggot, P. J., & Elowitz, M. B. (2009) · Nature · doi:10.1038/nature08150 · Cited by 154 · see citing works
Role of Pleiotropy in the Evolution of a Cryptic Developmental Variation in Caenorhabditis elegans
Duveau, F., & Félix, M. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001230 · Cited by 116 · see citing works
Self-citationPhosphorylation Networks Regulating JNK Activity in Diverse Genetic Backgrounds
Bakal, C., Linding, R., Llense, F., Heffern, E. F. W., Martı́n-Blanco, E., Pawson, T. J., & Perrimon, N. (2008) · Science · doi:10.1126/science.1158739 · Cited by 124 · see citing works
A general computational method for robustness analysis with applications to synthetic gene networks
Rizk, A., Batt, G., Fages, F., & Soliman, S. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp200 · Cited by 112 · see citing works
Cryptic Quantitative Evolution of the Vulva Intercellular Signaling Network in Caenorhabditis
Félix, M. (2007) · Current Biology · doi:10.1016/j.cub.2006.12.024 · Cited by 109 · see citing works
Self-citationIt’s not magic – Hsp90 and its effects on genetic and epigenetic variation
Zabinsky, R. A., Mason, G. A., Queitsch, C., & Jarosz, D. F. (2018) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2018.05.015 · Cited by 104 · see citing works
Evolution of brain network dynamics in neurodevelopment
Chai, L. R., Khambhati, A. N., Ciric, R., Moore, T. M., Gur, R. C., Gur, R. E., Satterthwaite, T. D., & Bassett, D. S. (2017) · Network Neuroscience · doi:10.1162/netn_a_00001 · Cited by 100 · see citing works
Bias and Evolution of the Mutationally Accessible Phenotypic Space in a Developmental System
Braendle, C., Baer, C. F., & Félix, M. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1000877 · Cited by 94 · see citing works
Self-citationReview: ABA, flavonols, and the evolvability of land plants
Brunetti, C., Sebastiani, F., & Tattini, M. (2018) · Plant Science · doi:10.1016/j.plantsci.2018.12.010 · Cited by 94 · see citing works
Milloz, J., Duveau, F., Nuez, I., & Félix, M. (2008) · Genes & Development · doi:10.1101/gad.495308 · Cited by 93 · see citing works
Self-citationSpoken language achieves robustness and evolvability by exploiting degeneracy and neutrality
Winter, B. (2014) · Bioessays · doi:10.1002/bies.201400028 · Cited by 102 · see citing works
Feedback Control of Gene Expression Variability in the Caenorhabditis elegans Wnt Pathway
Ji, N., Middelkoop, T. C., Mentink, R. A., Betist, M. C., Tonegawa, S., Mooijman, D., Korswagen, H. C., & van Oudenaarden, A. (2013) · Cell · doi:10.1016/j.cell.2013.09.060 · Cited by 89 · see citing works
Zhu, M., Chen, W., Mirabet, V., Hong, L., Bovio, S., Strauss, S., Schwarz, E. M., Tsugawa, S., Wang, Z., Smith, R. S., et al. (2020) · Nature Plants · doi:10.1038/s41477-020-0666-7 · Cited by 82 · see citing works
Survival of the Currently Fittest: Genetics of Rainbow Trout Survival Across Time and Space
Vehviläinen, H., Kause, A., Quinton, C. D., Koskinen, H., & Paananen, T. (2008) · Genetics · doi:10.1534/genetics.108.089896 · Cited by 80 · see citing works
Wild worm embryogenesis harbors ubiquitous polygenic modifier variation
Paaby, A. B., White, A. G., Riccardi, D., Gunsalus, K. C., Piano, F., & Rockman, M. V. (2015) · eLife · doi:10.7554/elife.09178 · Cited by 74 · see citing works
Loss of Genetic Redundancy in Reductive Genome Evolution
Mendonça, A. G., Alves, R., & Pereira‐Leal, J. B. (2011) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1001082 · Cited by 77 · see citing works
Efficient Modeling and Simulation of Bacteria-Based Nanonetworks with BNSim
Wei, G., Bogdan, P., & Mărculescu, R. (2013) · IEEE Journal on Selected Areas in Communications · doi:10.1109/jsac.2013.sup2.12130019 · Cited by 76 · see citing works
Activator‐inhibitor dynamics of vertebrate limb pattern formation
Newman, S. A., & Bhat, R. (2007) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.20112 · Cited by 74 · see citing works
Cryptic Genetic Variation in Natural Populations: A Predictive Framework
Ledón‐Rettig, C. C., Pfennig, D. W., Chunco, A. J., & Dworkin, I. M. (2014) · Integrative and Comparative Biology · doi:10.1093/icb/icu077 · Cited by 73 · see citing works
A New Development: Evolving Concepts in Leaf Ontogeny
Townsley, B. T., & Sinha, N. R. (2012) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042811-105524 · Cited by 72 · see citing works
Systems Biology of Phenotypic Robustness and Plasticity
Nijhout, H. F., Sadre‐Marandi, F., Best, J. A., & Reed, M. C. (2017) · Integrative and Comparative Biology · doi:10.1093/icb/icx076 · Cited by 71 · see citing works
Systems biology of robustness and homeostatic mechanisms
Nijhout, H. F., Best, J. A., & Reed, M. C. (2018) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.1440 · Cited by 69 · see citing works
Hoyos, E., Kim, K., Milloz, J., Barkoulas, M., Pénigault, J.-B., Munro, E., & Félix, M. (2011) · Current Biology · doi:10.1016/j.cub.2011.02.040 · Cited by 71 · see citing works
Self-citationGrowing Up in a Changing World: Environmental Regulation of Development in Insects
Mirth, C. K., Saunders, T. E., & Amourda, C. (2020) · Annual Review of Entomology · doi:10.1146/annurev-ento-041620-083838 · Cited by 68 · see citing works
MicroRNA-dependent regulation of biomechanical genes establishes tissue stiffness homeostasis
Moro, A., Driscoll, T. P., Boraas, L. C., Armero, W., Kasper, D. M., Baeyens, N., Jouy, C., Mallikarjun, V., Swift, J., Ahn, S. J., et al. (2019) · Nature Cell Biology · doi:10.1038/s41556-019-0272-y · Cited by 65 · see citing works
Robustness and flexibility in nematode vulva development
Félix, M., & Barkoulas, M. (2012) · Trends in Genetics · doi:10.1016/j.tig.2012.01.002 · Cited by 64 · see citing works
Self-citationPredicting future learning from baseline network architecture
Mattar, M. G., Wymbs, N. F., Bock, A. S., Aguirre, G. K., Grafton, S. T., & Bassett, D. S. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.01.037 · Cited by 64 · see citing works
The origins of mutational robustness
Fares, M. A. (2015) · Trends in Genetics · doi:10.1016/j.tig.2015.04.008 · Cited by 60 · see citing works
Alavash, M., Doebler, P., Holling, H., Thiel, C. M., & Gießing, C. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.12.046 · Cited by 60 · see citing works
The developmental genetics of biological robustness
Mestek, L., & Barkoulas, M. (2015) · Annals of Botany · doi:10.1093/aob/mcv128 · Cited by 58 · see citing works
Robustness Against the Decision-Maker's Attitude to Risk in Problems With Conflicting Objectives
Bui, L. T., Abbass, H. A., Barlow, M., & Bender, A. (2010) · IEEE Transactions on Evolutionary Computation · doi:10.1109/tevc.2010.2051443 · Cited by 54 · see citing works
Weaver, B. P., Zabinsky, R. A., Weaver, Y. M., Lee, E. S., Xue, D., & Han, M. (2014) · eLife · doi:10.7554/elife.04265 · Cited by 54 · see citing works
Cryptic Variation between Species and the Basis of Hybrid Performance
Rosas, U., Barton, N., Copsey, L., de Reuille, P. B., & Coen, E. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000429 · Cited by 52 · see citing works
How does evolution tune biological noise?
Richard, M., & Yvert, G. (2014) · Frontiers in Genetics · doi:10.3389/fgene.2014.00374 · Cited by 51 · see citing works
Mechanisms and Evolution of Environmental Responses in Caenorhabditis elegans
Braendle, C., Milloz, J., & Félix, M. (2007) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(07)80005-6 · Cited by 43 · see citing works
Self-citationNetworked buffering: a basic mechanism for distributed robustness in complex adaptive systems
Whitacre, J. M., & Bender, A. (2010) · University of Birmingham Institutional Research Archive (University of Birmingham) · Cited by 46 · see citing works
BIOSOARM: a bio-inspired self-organising architecture for manufacturing cyber-physical shopfloors
Dias-Ferreira, J., Ribeiro, L., Akillioglu, H., Neves, P., & Onori, M. A. (2016) · Journal of Intelligent Manufacturing · doi:10.1007/s10845-016-1258-2 · Cited by 44 · see citing works
Studying evolution of the primary body axis in vivo and in vitro
Anlaş, K., & Trivedi, V. (2021) · eLife · doi:10.7554/elife.69066 · Cited by 41 · see citing works
Networked buffering: a basic mechanism for distributed robustness in complex adaptive systems
Whitacre, J. M., & Bender, A. (2010) · Theoretical Biology and Medical Modelling · doi:10.1186/1742-4682-7-20 · Cited by 55 · see citing works
Zuroff, T. R., Bernstein, H. C., Lloyd-Randolfi, J., Jiménez-Taracido, L., Stewart, P. S., & Carlson, R. P. (2010) · BMC Microbiology · doi:10.1186/1471-2180-10-185 · Cited by 38 · see citing works
Evolution of Gene Regulatory Networks by Fluctuating Selection and Intrinsic Constraints
Tsuda, M. E., & Kawata, M. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000873 · Cited by 36 · see citing works
Gametic selection, developmental trajectories, and extrinsic heterogeneity in Haldane's rule
Bundus, J. D., Alaei, R., & Cutter, A. D. (2015) · Evolution · doi:10.1111/evo.12708 · Cited by 34 · see citing works
Overcoming Redundancy: An RNAi Enhancer Screen for Morphogenesis Genes in Caenorhabditis elegans
Sawyer, J. M., Glass, S., Li, T., Shemer, G., White, N. D., Starostina, N. G., Kipreos, E. T., Jones, C. D., & Goldstein, B. (2011) · Genetics · doi:10.1534/genetics.111.129486 · Cited by 33 · see citing works
QST < FST As a signature of canalization
Lamy, J., Plomion, C., Kremer, A., & Delzon, S. (2012) · Molecular Ecology · doi:10.1111/mec.12017 · Cited by 35 · see citing works
Network architectures supporting learnability
Zurn, P., & Bassett, D. S. (2020) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0323 · Cited by 30 · see citing works
Dissecting Genetic Networks Underlying Complex Phenotypes: The Theoretical Framework
Zhang, F., Zhai, H., Paterson, A. H., Xu, J.-L., Gao, Y.-M., Zheng, T., Wu, R., Fu, B.-Y., Ali, J., & Zhi-Kang, L. I. (2011) · PLoS ONE · doi:10.1371/journal.pone.0014541 · Cited by 34 · see citing works
Gidalevitz, T., Wang, N., Deravaj, T., Alexander-Floyd, J., & Morimoto, R. I. (2013) · BMC Biology · doi:10.1186/1741-7007-11-100 · Cited by 31 · see citing works
Dineen, A., Nishimura, E. O., Goszczynski, B., Rothman, J. H., & McGhee, J. D. (2018) · Developmental Biology · doi:10.1016/j.ydbio.2017.12.023 · Cited by 32 · see citing works
A PUF Hub Drives Self-Renewal in Caenorhabditis elegans Germline Stem Cells
Haupt, K. A., Law, K. T., Enright, A. L., Kanzler, C. R., Shin, H., Wickens, M., & Kimble, J. E. (2019) · Genetics · doi:10.1534/genetics.119.302772 · Cited by 31 · see citing works
Distinct Functional Constraints Partition Sequence Conservation in a cis-Regulatory Element
Barrière, A., Gordon, K. L., & Ruvinsky, I. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002095 · Cited by 30 · see citing works
Speciation and the developmental alarm clock
Cutter, A. D., & Bundus, J. D. (2020) · eLife · doi:10.7554/elife.56276 · Cited by 30 · see citing works
Evolvability and robustness in a complex signalling circuit
Raman, K., & Wagner, A. (2011) · Molecular BioSystems · doi:10.1039/c0mb00165a · Cited by 29 · see citing works
Self-citationPossible genetic and epigenetic links between human inner speech, schizophrenia and altruism
Agnati, L. F., Barlow, P., Ghidoni, R., Borroto-Escuela, D. O., Guidolin, D., & Fuxe, K. (2012) · Brain Research · doi:10.1016/j.brainres.2012.02.074 · Cited by 29 · see citing works
Evolution in developmental phenotype space
Félix, M. (2012) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2012.08.003 · Cited by 28 · see citing works
Self-citationEcdysone coordinates plastic growth with robust pattern in the developing wing
Alves, A. N., Oliveira, M. M., Koyama, T., Shingleton, A. W., & Mirth, C. K. (2022) · eLife · doi:10.7554/elife.72666 · Cited by 28 · see citing works
Duma, G. M., Danieli, A., Mattar, M. G., Baggio, M., Vettorel, A., Bonanni, P., & Mento, G. (2022) · Cortex · doi:10.1016/j.cortex.2022.08.010 · Cited by 27 · see citing works
Braendle, C., & Félix, M. (2009) · Journal of Biosciences · doi:10.1007/s12038-009-0073-8 · Cited by 25 · see citing works
Self-citationStructural Analysis to Determine the Core of Hypoxia Response Network
Monika Heiner, A., & Sriram, K. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008600 · Cited by 25 · see citing works
Noise propagation with interlinked feed-forward pathways
Chepyala, S. R., Chen, Y., Yan, C. S., Lu, C.-Y. D., Wu, Y., & Hsu, C. (2016) · Scientific Reports · doi:10.1038/srep23607 · Cited by 23 · see citing works
Predicting Phenotypic Diversity and the Underlying Quantitative Molecular Transitions
Giurumescu, C. A., Sternberg, P. W., & Asthagiri, A. R. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000354 · Cited by 24 · see citing works
Defect-buffering cellular plasticity increases robustness of metazoan embryogenesis
Xiao, L., Fan, D., Qi, H., Cong, Y., & Du, Z. (2022) · Cell Systems · doi:10.1016/j.cels.2022.07.001 · Cited by 24 · see citing works
Genetic architecture of rainbow trout survival from egg to adult
Vehviläinen, H., Kause, A., Koskinen, H., & Paananen, T. (2010) · Genetics Research · doi:10.1017/s0016672310000017 · Cited by 24 · see citing works
Stochastic variation in Cardamine hirsuta petal number
Monniaux, M., Pieper, B., & Hay, A. (2015) · Annals of Botany · doi:10.1093/aob/mcv131 · Cited by 24 · see citing works
Developmental instability of vascular plants in contrasting microclimates at ‘Evolution Canyon’
Raz, S., Graham, J. H., Hel-Or, H. Z., Pavlı́ček, T., & Nevo, E. (2011) · Biological Journal of the Linnean Society · doi:10.1111/j.1095-8312.2011.01615.x · Cited by 23 · see citing works
Natural Variation of Molecular and Morphological Gibberellin Responses
Nam, Y.-J., Herman, D., Blomme, J., Chae, E., Kojima, M., Coppens, F., Storme, V., Daele, T. V., Dhondt, S., Sakakibara, H., et al. (2016) · PLANT PHYSIOLOGY · doi:10.1104/pp.16.01626 · Cited by 23 · see citing works
A parsimonious model of lineage-specific expansion of MADS-box genes in Physcomitrella patens
Barker, E. I., & Ashton, N. W. (2013) · Plant Cell Reports · doi:10.1007/s00299-013-1411-8 · Cited by 23 · see citing works
Bunditvorapoom, D., Kochakarn, T., Kotanan, N., Modchang, C., Kümpornsin, K., Loesbanluechai, D., Krasae, T., Cui, L., Chotivanich, K., White, N. J., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-30593-5 · Cited by 23 · see citing works
Extensive intraspecies cryptic variation in an ancient embryonic gene regulatory network
Cleuren, Y. N. T., Ewe, C. K., Chipman, K. C., Mears, E., Wood, C. G., Al-Alami, C. E. A., Alcorn, M. R., Turner, T. L., Joshi, P. M., Snell, R. G., et al. (2019) · eLife · doi:10.7554/elife.48220 · Cited by 21 · see citing works
Ewe, C. K., Cleuren, Y. N. T., & Rothman, J. H. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00170 · Cited by 21 · see citing works
Cryptic variation in vulva development by cis-regulatory evolution of a HAIRY-binding site
Kienle, S., & Sommer, R. J. (2013) · Nature Communications · doi:10.1038/ncomms2711 · Cited by 22 · see citing works
Developmental robustness in the Caenorhabditis elegans embryo
Maduro, M. (2015) · Molecular Reproduction and Development · doi:10.1002/mrd.22582 · Cited by 22 · see citing works
The Maternal-to-Zygotic Transition Targets Actin to Promote Robustness during Morphogenesis
Zheng, L., Sepúlveda, L. A., Lua, R. C., Lichtarge, O., Golding, I., & Sokac, A. M. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003901 · Cited by 19 · see citing works
Morphogenic machines evolve more rapidly than the signals that pattern them: lessons from amphibians
Shook, D. R., & Keller, R. E. (2007) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21204 · Cited by 20 · see citing works
The significance of developmental robustness for species diversity
Melzer, R., & Theißen, G. (2016) · Annals of Botany · doi:10.1093/aob/mcw018 · Cited by 19 · see citing works
Chen, B., & Lin, Y. (2011) · Evolutionary Bioinformatics · doi:10.4137/ebo.s8123 · Cited by 19 · see citing works
Forbes, C. E., Amey, R. C., Magerman, A. B., Duran, K. A., & Liu, M. (2018) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsy043 · Cited by 21 · see citing works
The Stochastic Evolutionary Game for a Population of Biological Networks under Natural Selection
Chen, B., & Ho, S.-J. (2014) · Evolutionary Bioinformatics · doi:10.4137/ebo.s13227 · Cited by 18 · see citing works
Coordinating Development: How Do Animals Integrate Plastic and Robust Developmental Processes?
Mirth, C. K., & Shingleton, A. W. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00008 · Cited by 18 · see citing works
Kivisaar, M. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2011.07824.x · Cited by 18 · see citing works
Spike, C. A., Huelgas‐Morales, G., Tsukamoto, T., & Greenstein, D. (2018) · Genetics · doi:10.1534/genetics.118.301421 · Cited by 18 · see citing works
Luecke, D. M., & Kopp, A. (2019) · Evolution · doi:10.1111/evo.13847 · Cited by 18 · see citing works
Sallee, M. D., Aydin, T., & Greenwald, I. (2015) · G3 Genes Genomes Genetics · doi:10.1534/g3.115.022608 · Cited by 17 · see citing works
Non-Darwinian Molecular Biology
Palazzo, A. F., & Kejiou, N. S. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.831068 · Cited by 17 · see citing works
Forestiero, S. (2022) · Theory in Biosciences · doi:10.1007/s12064-022-00369-7 · Cited by 17 · see citing works
Beyond modular enhancers: new questions in cis-regulatory evolution
McDonald, J. M. C., & Reed, R. D. (2024) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2024.07.005 · Cited by 15 · see citing works
Kim, K. J., & Fernandes, V. M. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000296 · Cited by 17 · see citing works
- Authors
- Félix, M.-A., & Wagner, A.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- University of Zurich (CH)
- ORCID
- Venue
- Heredity
- Published
- 2006-12-13
- Volume
- 100
- Issue
- 2
- Pages
- 132-140
- ISSN
- 0018-067X (ISSN-L)
- 1365-2540
- OpenAlex
- W2147777139
- Cited by
- 210
- References
- 93
- Citations by year
- 2026: 7 · 2025: 4 · 2024: 8 · 2023: 6 · 2022: 15 · 2021: 7 · 2020: 17 · 2019: 8 · 2018: 17 · 2017: 5 · 2016: 10 · 2015: 14 · 2014: 13 · 2013: 12 · 2012: 12
- FWCI
- 0.70
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Heredity (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, other-oa)
- HAL (submittedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- Agence Nationale de la Recherche (ANR-05)
- Centre National de la Recherche Scientifique
- National Institutes of Health
- National Institute of General Medical Sciences (R01GM063882, GM63882)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Social Sciences › Arts and Humanities › History and Philosophy of Science › Philosophy and History of Science
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- robustness, vulval development, Caenorhabditis elegans, redundancy, cryptic variation, evolutionary innovation, developmental robustness, natural selection
- MeSH terms
- Animals, Biological Evolution, Female, Vulva, Caenorhabditis elegans
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review