The DOI matches its Crossref record; 14 of the 14 references it cites were found in a registry or an index.
CANALIZATION OF DEVELOPMENT AND THE INHERITANCE OF ACQUIRED CHARACTERS
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“This robustness (compatibility with a larger set of environmental conditions) can be a target of evolution, as argued by Waddington and others [36–38].”
From Fundamental constraints to the logic of living systems (2024) · cites this paper as [36]
In the citing paper
“We frame this issue using the concept of developmental canalization88, whereby natural selection on developmental programmes in humans has led to robustness in a range of genetic or environmental perturbations89,90: typical development occurs along a ‘track’ (FIG. 1c).”
From Systems biology and gene networks in neurodevelopmental and neurodegenerative disorders (2015) · cites this paper as [88]
In the citing paper
“In addition, most studies recruit survivors of the original birth cohorts. This means all participants must have survived in order to observe whether they get the outcome of interest. Selection of participants on surviving their genetic make-up and the outcome of interest or a competing risk of the outcome effectively applies covariable adjustment on survival into the estimates.173–175”
From Mendelian randomization (2022) · cites this paper as [175]
Citations
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Kayserili, M. A., Gerrard, D. T., Tomančák, P., & Kalinka, A. T. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1003200 · Cited by 41
“The canalisation of embryonic development, such that it is resistant to environmental or genetic perturbations, has long been recognized as a crucial element contributing to the evolution of robustness in developmental systems [70].”
BackgroundChao, L., Rang, C. U., Proenca, A. M., & Chao, J. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004700 · Cited by 36
Ryan, C. P., Brownlie, J. C., & Whyard, S. (2016) · Genome Biology and Evolution · doi:10.1093/gbe/evw284 · Cited by 35
“DNA was extracted from single worms using a previously described method (Williams et al. 1992).”
MethodGene expression regulation by heat-shock proteins: the cardinal roles of HSF1 and Hsp90
Mazaira, G. I., Daneri-Becerra, C., Zgajnar, N. R., Lotufo, C. M., & Galigniana, M. D. (2017) · Biochemical Society Transactions · doi:10.1042/bst20170335 · Cited by 36
Rapid adaptation to cold in the invasive cane toadRhinella marina
Mittan, C., & Zamudio, K. R. (2018) · Conservation Physiology · doi:10.1093/conphys/coy075 · Cited by 36
“This initial adaptive plastic response may then become canalized through genetic accommodation, providing constitutive expression of a trait that was once a plastic response (Waddington, 1942; Pfennig et al., 2010).”
BackgroundA comparative study of endoderm differentiation in humans and chimpanzees
Blake, L. E., Thomas, S. M., Blischak, J., Hsiao, C. J., Chavarria, C. I., Myrthil, M., Gilad, Y., & Pavlovic, B. J. (2018) · Genome biology · doi:10.1186/s13059-018-1490-5 · Cited by 34
“This observation is consistent with the notion [30] that developmental pathways need to be tightly regulated in general.”
BackgroundMartin, E., Theis, S., Gay, G., Monier, B., Rouvière, C., & Suzanne, M. (2021) · Developmental Cell · doi:10.1016/j.devcel.2021.01.005 · Cited by 35
“This trait, called robustness, is characterized by a low level of variation of a given phenotype when subjected to environmental or genetic variations (Waddington, 1942).”
BackgroundMedina, M., Sharp, V. J. A., Ohdera, A. H., Bellantuono, A. J., Dalrymple, J., Gamero‐Mora, E., Steinworth, B. M., Hofmann, D. K., Martindale, M. Q., Morandini, A. C., et al. (2021) · CRC Press eBooks · doi:10.1201/9781003217503-9 · Cited by 37
Epigenetic Transgenerational Inheritance of the Effects of Obesogen Exposure
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“The British embryologist, Conrad Hal Waddington has been credited with coining the term “epigenetics” after his discovery that genetic assimilation drives phenotypic evolution (1, 2).”
BackgroundThe Role of Mathematical Models in Understanding Pattern Formation in Developmental Biology
Umulis, D. M., & Othmer, H. G. (2014) · Bulletin of Mathematical Biology · doi:10.1007/s11538-014-0019-7 · Cited by 32
“That is to say, they are adjusted so as to bring about one definite end-result regardless of minor variations in conditions during the course of the reactions (Waddington 1942).”
Ontology of evolution and methodology of taxonomy
Rasnitsyn, A. P. (2006) · Paleontological Journal · doi:10.1134/s003103010612001x · Cited by 37
Pandey, N., Bhola, S., Goldstone, A. B., Chen, F., Chrzanowski, J., Terranova, C. J., Ghillani, R., & Jepsen, K. J. (2009) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.090525 · Cited by 36
“The mechanism that mediates the interplay between genetically varying traits and environmental stimuli may be a by-product of natural selection((44)) or an FIG.”
Background2,3,7,8-Tetrachlorodibenzo-p-Dioxin Affects Size and Shape, But Not Asymmetry, of Mandibles in Mice
Allen, D. E., & Leamy, L. J. (2001) · Ecotoxicology · doi:10.1023/a:1016693911300 · Cited by 36
MicroRNA, the putative molecular control for mid-life decline
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Epigenetics and Plant Breeding
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Morphological Genetic Markers in Plants
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Embracing plant plasticity or robustness as a means of ensuring food security
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“We will only discuss those based on the concept of canalization proposed by Waddington in1942 49 who suggested that there must be some capacity of the genotype to buffer the phenotype against minor variations in genotype and environment 93 .”
Gene regulation technologies for gene and cell therapy
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Genetic assimilation and accommodation: Models and mechanisms
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“A theoretical concept that connects genetic and nongenetic sources of tumor heterogeneity is the “epigenetic landscape,” proposed by Waddington over 50 years ago [37] but has received renewed attention recently [19,20,38,39] (see Table A in S1 Text for definitions of terms useful for the following discussion).”
BackgroundNested Canalyzing Depth and Network Stability
Layne, L., Dimitrova, E., & Macauley, M. (2011) · Bulletin of Mathematical Biology · doi:10.1007/s11538-011-9692-y · Cited by 33
Quantifying the Decanalizing Effects of Spontaneous Mutations in Rhabditid Nematodes
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“The importance of canalization has been recognized for a long time (Waddington 1942; Schmalhausen 1949; Lerner 1954) and has been the subject of renewed interest in recent years (for recent reviews, see de Visser et al. 2003; Dworkin * E-mail: cbaer@zoo.ufl.edu.”
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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 37
“In the original meaning, a trait becomes canalized because the insensitivity to perturbations was considered to increase fitness (Waddington 1942, 1953; Wagner et al. 1997; Debat & David 2001).”
BackgroundEvolutionary developmental psychology: Current status and future directions
Geary, D. C. (2006) · Developmental Review · doi:10.1016/j.dr.2006.02.005 · Cited by 36
Inbreeding Affects Female Preference for Symmetry in Computer-Animated Sticklebacks
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Ligament versus bone cell identity in the zebrafish hyoid skeleton is regulated by mef2ca
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“When development goes awry in genetic mutants, the resulting phenotypes often vary substantially compared with the wild type (Waddington, 1942).”
BackgroundGeneralized norms of reaction for ecological developmental biology
Sarkar, S., & Fuller, T. L. (2002) · Evolution & Development · doi:10.1046/j.1525-142x.2003.03016.x · Cited by 35
Evolutionary Developmental Biology
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Fundamental constraints to the logic of living systems
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Proper Function and Recent Selection
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The molecular basis of cell memory in mammals: The epigenetic cycle
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“The term “epigenetics” was coined by C. H. Waddington in 1942, and it provided an explanation as to how the phenotypes of evolving organisms can respond to the environment without changing the genotype ( 13 , 14 ).”
BackgroundParamutation phenomena in plants
Pilu, R. (2015) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2015.08.015 · Cited by 34
Novel variation associated with species range expansion
Buckley, J., Bridle, J. R., & Pomiankowski, A. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-382 · Cited by 34
“Selection for canalization of developmental traits also makes these interesting candidates for responding in a novel manner to extreme environmental cues [8].”
BackgroundConstraints, Trade-offs and the Currency of Fitness
Acerenza, L. (2016) · Journal of Molecular Evolution · doi:10.1007/s00239-016-9730-3 · Cited by 33
“More generally, development shows a remarkable robustness to mutations or environmental perturbations, property that has been called canalization (Waddington 1942, 1957).”
A molecular concept of caste in insect societies
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“The fact that major mutations or extreme environmental treatments are generally accompanied by a burst of phenotypic variation also indicates that this buffering can be overcome by sufficiently strong perturbations.(2,3) The origin of this phenotypic stability, or robustness, has attracted a great deal of interest ove…”
BackgroundKatsanos, D., Koneru, S. L., Mestek, L., Gritti, N., Ghose, R., Appleford, P. J., Doitsidou, M., Woollard, A. C. S., van Zon, J. S., Poole, R. J., et al. (2017) · PLoS Biology · doi:10.1371/journal.pbio.2002429 · Cited by 31
“Since Waddington, who first discussed developmental variability [4], there is a growing interest in understanding phenotypic buffering using both theoretical and experimental approaches [5].”
Evolution of new miRNAs and cerebro-cortical development
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Conrad H. Waddington's contributions to avian and mammalian development, 1930-1940
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Role of mef2ca in developmental buffering of the zebrafish larval hyoid dermal skeleton
DeLaurier, A., Huycke, T. R., Nichols, J. T., Swartz, M. E., Larsen, A., Walker, C., Dowd, J., Pan, L., Moens, C. B., & Kimmel, C. B. (2013) · Developmental Biology · doi:10.1016/j.ydbio.2013.11.016 · Cited by 33
“Buffering can break down, resulting in increased phenotypic variation; indeed, the initial motivation for the canalization concept was to explain the increased variation commonly observed in mutants (Waddington, 1942).”
InfluentialGene Regulation: Enhancers Stepping Out of the Shadow
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A naturally occurring variant of Hsp90 that is associated with decanalization
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An introduction to Mendelian randomization with applications in neurology
Allman, P., Aban, I., Tiwari, H. K., & Cutter, G. (2018) · Multiple Sclerosis and Related Disorders · doi:10.1016/j.msard.2018.06.017 · Cited by 33
Genetic accommodation and the role of ancestral plasticity in the evolution of insect eusociality
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“Most studies providing empirical support for genetic accommodation employ artificial selection on experimentally induced phenotypes, some of which may not occur in nature (Suzuki and Nijhout, 2006; Waddington, 1942, 1953).”
BackgroundEpigenetic Effects of Curcumin in Cancer Prevention
Shanmugam, M. K., Arfuso, F., Sng, J., Bishayee, A., Kumar, A. P., & Sethi, G. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-812494-9.00005-6 · Cited by 35
MicroRNA governs bistable cell differentiation and lineage segregation via a noncanonical feedback
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“Waddington termed this process “canalization”, with greater net canalization during development resulting in less phenotypic variation among individuals in a population (Waddington, 1942).”
BackgroundKoehler, A. V. A., Springer, Y. P., Keeney, D. B., & Poulin, R. (2011) · Biological Journal of the Linnean Society · doi:10.1111/j.1095-8312.2011.01640.x · Cited by 33
“This could be explained by developmental canalization, or the ability of an organism to produce a consistent phenotype regardless of differences in genotype or environment (Waddington, 1942).”
BackgroundMultidimensional analysis of Drosophila wing variation in Evolution Canyon
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“This hypothesis, which traces back to work on canalization by Waddington in the mid-twentieth century ( Waddington 1942, 1957 ), was readvocated in the past 10 years with the discovery in Drosophila and Arabidopsis of the role of Hsp90 in the hide and release of cryptic genetic variation of putative adaptive value (Ru…”
BackgroundPolyakov, A. V., Onischenko, S. S., Ilyashenko, V. B., Searle, J. B., & Бородин, П. М. (2002) · ACTA THERIOLOGICA · doi:10.1007/bf03192464 · Cited by 33
Molecular mechanisms of canalization: Hsp90 and beyond
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“, canalization [42]) rather than increase it.”
‘Big frog, small frog’– maintaining proportions in embryonic development
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Replication of asymmetry ofa?b ridge count and behavioral discordance in monozygotic twins
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Relationships between fluctuating asymmetry and fitness: how good is the evidence?
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Tissue plasminogen activator in the trabecular endothelium.
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The Design of Subprimate Animal Studies
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Negative Feedback in Genetic Circuits Confers Evolutionary Resilience and Capacitance
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“Canalization is a term coined by Waddington to describe the robustness of phenotype to perturbations in environment or genotype (Waddington, 1942).”
BackgroundThe Influence of Canalization on the Robustness of Boolean Networks
Kadelka, C., Kuipers, J., & Laubenbacher, R. (2016) · Physica D Nonlinear Phenomena · doi:10.1016/j.physd.2017.05.002 · Cited by 33
Legacy effects of herbivory enhance performance and resistance of progeny plants
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“In other words, the physiological regulatory processes that maintain energy homeostasis may provide stability in metabolic trajectories, in an analogous way to the canalized developmental trajectories envisioned by Waddington (Meiklejohn and Hartl, 2002; Waddington, 1942, 1957).”
BackgroundMuscle‐induced loading as an important source of variation in craniofacial skeletal shape
Conith, A. J., Lam, D. T., & Albertson, R. C. (2018) · genesis · doi:10.1002/dvg.23263 · Cited by 32
“2019;57:e23263. wileyonlinelibrary.com/journal/dvg © 2018 Wiley Periodicals, Inc. 1 of 13 https://doi.org/10.1002/dvg.23263 (sensu Waddington (Waddington, 1942)), such as environmental factors, which may account for much of the remaining variation that is “missing” from association studies (Bossdorf, Richards, & Pigli…”
BackgroundInfluentialConvergence of spectrums: neuronal gene network states in autism spectrum disorder
Sullivan, J. M., Rubeis, S. D., & Schaefer, A. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.04.011 · Cited by 32
“The robustness of cell differentiation reflects the so-called “canalization” process towards a specific outcome from uncertain starting conditions [53] (Figure 2).”
BackgroundMethodInfluentialHarris, L. A., Beik, S. P., Ozawa, P. M. M., Jimenez, L., & Weaver, A. M. (2019) · Current Opinion in Systems Biology · doi:10.1016/j.coisb.2019.09.005 · Cited by 34
“Huang S: The molecular and mathematical basis of Waddington’s epigenetic landscape: a framework for post-Darwinian biology?”
BackgroundInfluentialPlant gene expression control using genome- and epigenome-editing technologies
Miglani, G. S., Kaur, A., & Kaur, L. (2019) · Journal of Crop Improvement · doi:10.1080/15427528.2019.1678541 · Cited by 33
“The term epigenetics was coined by Waddington (1942) to define mitotically and/or meiotically heritable yet reversible changes in gene expression.”
BackgroundWong, M., Newton, L. R., Hartmann, J., Hennrich, M. L., Wachsmuth, M., Ronchi, P., Guzmán‐Herrera, A., Schwab, Y., Gavin, A., & Gilmour, D. T. (2020) · Developmental Cell · doi:10.1016/j.devcel.2020.01.013 · Cited by 32
Gene expression plasticity and desert adaptation in house mice*
Bittner, N. K. J., Mack, K. L., & Nachman, M. W. (2021) · Evolution · doi:10.1111/evo.14172 · Cited by 32
“Adaptive plasticity can be followed by genetic changes as populations become established, in a process called “genetic assimilation” or the “Baldwin Effect” (Waddington 1942, 1952, 1953; Simpson 1953; Robinson and Dukas 1999; Price et al. 2003).”
Can the battle against tuberculosis gain from epigenetic research?
Esterhuyse, M. M., Linhart, H., & Kaufmann, S. H. E. (2012) · Trends in Microbiology · doi:10.1016/j.tim.2012.03.002 · Cited by 32
Getting the Measure of Positional Information
Jaeger, J., & Martínez-Arias, A. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000081 · Cited by 32
“Waddington in 1942 that developmental trajectories are buffered against perturbations, a phenomenon he called canalization [31].”
BackgroundDevelopmental instability: measures of resistance and resilience using pumpkin (Cucurbita pepo L.)
Freeman, D. C., Brown, M. L., DOBSON, M., JORDAN, Y., Kizy, A. E., Micallef, C., Hancock, L. C., Graham, J. H., & Emlen, J. M. (2003) · Biological Journal of the Linnean Society · doi:10.1046/j.1095-8312.2003.00123.x · Cited by 32
Canalization Breakdown and Evolution in a Source-Sink System
Kimbrell, T., & Holt, R. D. (2007) · The American Naturalist · doi:10.1086/511314 · Cited by 32
The relationship between the error catastrophe, survival of the flattest, and natural selection
Tejero, H., Marín, A., & Montero, F. (2011) · BMC Evolutionary Biology · doi:10.1186/1471-2148-11-2 · Cited by 33
“For the sake of clarity, canalization is considered to be the existence of different genotypes that produce the same phenotype [56], and neutrality to be the existence of different phenotypes with the same fitness [57].”
BackgroundBurman, J. T. (2012) · New Ideas in Psychology · doi:10.1016/j.newideapsych.2012.07.003 · Cited by 32
Lee, S., Kohane, I. S., & Kasif, S. (2005) · BMC Genomics · doi:10.1186/1471-2164-6-168 · Cited by 32
The field of cancer research: an indicator of present transformations in biology
Morange, M. (2007) · Oncogene · doi:10.1038/sj.onc.1210583 · Cited by 30
Lack of tailless leads to an increase in expression variability in Drosophila embryos
Janssens, H., Crombach, A., Wotton, K. R., Cicin-Sain, D., Surkova, S. Y., Lim, C. L., Samsonova, M. G., Akam, M. E., & Jaeger, J. (2013) · Developmental Biology · doi:10.1016/j.ydbio.2013.01.010 · Cited by 32
Kaneko, K. (2009) · Journal of Biosciences · doi:10.1007/s12038-009-0072-9 · Cited by 32
Learning regulatory models for cell development from single cell transcriptomic data
Babtie, A. C., Chan, T. E., & Stumpf, M. P. H. (2017) · Current Opinion in Systems Biology · doi:10.1016/j.coisb.2017.07.013 · Cited by 32
A Nonquiescent “Idling” Population State in Drug-Treated, BRAF-Mutated Melanoma
Paudel, B. B., Harris, L. A., Hardeman, K. N., Abugable, A. A., Hayford, C. E., Tyson, D. R., & Quaranta, V. (2018) · Biophysical Journal · doi:10.1016/j.bpj.2018.01.016 · Cited by 31
“The idea dates back to Waddington (28), who posited that cellular differentiation can be conceptualized as a dynamical trajectory through an ‘‘epigenetic landscape.”
BackgroundTransgenerational Plasticity and Bet-Hedging: A Framework for Reaction Norm Evolution
Joschinski, J., & Bonte, D. (2020) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2020.517183 · Cited by 34
“Plasticity has a long history of being related to reaction norm shapes (Woltereck, 1913; Bradshaw, 1965), but diversified bet-hedging is not as easily visualized, nor is the relationship with plasticity entirely clear.”
BackgroundEpigenetic inheritance and evolution: a historian's perspective
Loison, L. (2021) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2020.0120 · Cited by 31
“304]), the tense context of Lysenkoism and Waddington’s new research program [54,55], Simpson thought it necessary to bring clarity in this debated and complex issue, where so many terms were used more or less as synonyms (‘organic selection’, ‘coincident selection’, ‘post-adaptation’, ‘stabilizing selection’, etc.”
BackgroundBreen, J., Mur, L. A. J., Sivakumaran, A., Akinyemi, A., Wilkinson, M. J., & Lopez, C. M. R. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23063034 · Cited by 31
“Waddington [13] first proposed the term epigenotype to describe the interface between genotype and phenotype.”
BackgroundMacroevolutionary patterns of body plan canalization in euarthropods
Aria, C. (2020) · Paleobiology · doi:10.1017/pab.2020.36 · Cited by 28
“Canalization (Waddington 1942) is a fundamental concept in this context.”
BackgroundDas, A. B., Smith-Díaz, C. C., & Vissers, M. C. M. (2020) · Haematologica · doi:10.3324/haematol.2020.259283 · Cited by 25
DNA Methylation Levels in Different Tissues in Tea Plant via an Optimized HPLC Method
Gao, Y., Hao, J.-L., Wang, Z., Song, K.-J., Ye, J.-H., Zheng, X.-Q., Liang, Y.-R., & Lu, J.-L. (2019) · Horticulture, Environment, and Biotechnology · doi:10.1007/s13580-019-00180-2 · Cited by 20
“Epigenetics was first proposed by the famous biologist Waddington in 1942, and defined as “hereditary and environmental interaction leads to the emergence of the phenotype” (Waddington 1942).”
Background
Metadata
- Authors
- WADDINGTON, C. H.
- Affiliations
- University of Cambridge (GB)
- Corresponding author
- WADDINGTON, C. H.
- Venue
- Nature
- Published
- 1942-11
- Volume
- 150
- Issue
- 3811
- Pages
- 563-565
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2094902224
- Cited by
- 3,255
- References
- 14
- Citations by year
- 2026: 111 · 2025: 127 · 2024: 122 · 2023: 109 · 2022: 162 · 2021: 140 · 2020: 168 · 2019: 162 · 2018: 168 · 2017: 145 · 2016: 149 · 2015: 192 · 2014: 150 · 2013: 172 · 2012: 127
- FWCI
- 1.73
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Social Sciences › Arts and Humanities › History and Philosophy of Science › Philosophy of Biology and Scientific Explanation
- Social Sciences › Cultural Studies › Language and cultural evolution
- Keywords
- inheritance of acquired characteristics, Lamarckism, use and disuse, natural selection, random mutation, gene-environment interaction, adaptive evolution, heritable variation
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