A power law for cells

Darwin observed that multiple, lowly organized, rudimentary, or exaggerated structures show increased relative variability. However, the cellular basis for these laws has never been investigated. Some animals, such as the nematode Caenorhabditis elegans, are famous for having organs that possess the same number of cells in all individuals, a property known as eutely. But for most multicellular creatures, the extent of cell number variability is unknown. Here we estimate variability in organ cell number for a variety of animals, plants, slime moulds, and volvocine algae. We find that the mean and variance in cell number obey a power law with an exponent of 2, comparable to Taylor's law in ecological processes. Relative cell number variability, as measured by the coefficient of variation, differs widely across taxa and tissues, but is generally independent of mean cell number among homologous tissues of closely related species. We show that the power law for cell number variability can be explained by stochastic branching process models based on the properties of cell lineages. We also identify taxa in which the precision of developmental control appears to have evolved. We propose that the scale independence of relative cell number variability is maintained by natural selection.

[1]  M. Busslinger,et al.  Independent regulation of the two Pax5 alleles during B-cell development , 1999, Nature Genetics.

[2]  J. Truman,et al.  Distribution of GABA‐like immunoreactive neurons in insects suggests lineage homology , 1998, The Journal of comparative neurology.

[3]  M. Raff,et al.  Social controls on cell survival and cell death , 1992, Nature.

[4]  D. Emlen,et al.  The developmental basis for allometry in insects. , 1999, Development.

[5]  Sewall Wright,et al.  Evolution and the Genetics of Populations. I, Genetic and Biometric Foundations. , 1969 .

[6]  T. E. Harris,et al.  The Theory of Branching Processes. , 1963 .

[7]  T. Sachs,et al.  Epigenetic selection: an alternative mechanism of pattern formation. , 1988, Journal of theoretical biology.

[8]  G. Williams,et al.  Natural selection : domains, levels, and challenges. , 1994 .

[9]  C. Darwin The Origin of Species by Means of Natural Selection, Or, The Preservation of Favoured Races in the Struggle for Life , 1859 .

[10]  T. Dobzhansky,et al.  Evolution and the Genetics of Populations, Vol. 1, Genetic and Biometric Foundations , 1969 .

[11]  V. Koufopanou,et al.  The Evolution of Soma in the Volvocales , 1994, The American Naturalist.

[12]  F. Galis,et al.  Why do almost all mammals have seven cervical vertebrae? Developmental constraints, Hox genes, and cancer. , 1999, The Journal of experimental zoology.

[13]  L. Taylor,et al.  Variance and the large scale spatial stability of aphids, moths and birds. , 1980 .

[14]  E. Macagno Number and distribution of neurons in leech segmental ganglia , 1980, The Journal of comparative neurology.

[15]  Isidore Geoffroy Saint-Hilaire Histoire générale et particulière des anomalies de l'organisation chez l'homme et les animaux. , 1832 .

[16]  B. Bainbridge,et al.  Genetics , 1981, Experientia.

[17]  S. W. Emmons,et al.  Developmental biology: Variable cell number in nematodes , 1999, Nature.

[18]  O. Pourquié,et al.  A clock-work somite. , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[19]  B. Scheres,et al.  Cellular organisation of the Arabidopsis thaliana root. , 1993, Development.

[20]  I. Schmalhausen Factors of evolution : the theory of stabilizing selection , 1946 .

[21]  A. Møller,et al.  A resolution of the lek paradox , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[22]  L. Rowe,et al.  The lek paradox and the capture of genetic variance by condition dependent traits , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[23]  P. Bryant,et al.  Organ and cell allometry in Hawaiian Drosophila: how to make a big fly , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[24]  R. Pearl Biometrics , 1914, The American Naturalist.

[25]  A. C. James,et al.  Cellular basis of wing size variation in Drosophila melanogaster: a comparison of latitudinal clines on two continents , 2000, Heredity.

[26]  E. Conklin Body size and cell size , 1912 .

[27]  Scott F. Gilbert,et al.  Embryology : constructing the organism , 1997 .

[28]  S. Pitnick Investment in Testes and the Cost of Making Long Sperm in Drosophila , 1996, The American Naturalist.

[29]  C. Benoist,et al.  Another view of the selective model of thymocyte selection , 1993, Cell.

[30]  F. W. Robertson Studies in Quantitative Inheritance. Xii. Cell Size and Number in Relation to Genetic and Environmental Variation of Body Size in Drosophila. , 1959, Genetics.

[31]  S. W. Emmons,et al.  Somatic polyploidization and cellular proliferation drive body size evolution in nematodes. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[32]  G. Edelman Topobiology: An Introduction To Molecular Embryology , 1988 .

[33]  R. Britten Underlying assumptions of developmental models. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[34]  A. C. James,et al.  Genetic and environmental responses to temperature of Drosophila melanogaster from a latitudinal cline. , 1997, Genetics.

[35]  T M Mayhew,et al.  Purkinje cell complements in mammalian cerebella and the biases incurred by counting nucleoli. , 1993, Journal of anatomy.

[36]  A. C. James,et al.  Cellular basis and developmental timing in a size cline of Drosophila melanogaster. , 1995, Genetics.

[37]  A. Mccarthy Development , 1996, Current Opinion in Neurobiology.

[38]  K. Okazaki,et al.  TOTAL CELL NUMBER AND NUMBER OF THE PRIMARY MESENCHYME CELLS IN WHOLE, 1/2 AND 1/4 LARVAE OF CLYPEASTER JAPONICUS * , 1979, Development, growth & differentiation.

[39]  J. Sulston,et al.  The embryonic cell lineage of the nematode Caenorhabditis elegans. , 1983, Developmental biology.

[40]  R. Strom,et al.  Genetic and Environmental Control of Variation in Retinal Ganglion Cell Number in Mice , 1996, The Journal of Neuroscience.

[41]  I. Conlon,et al.  Size Control in Animal Development , 1999, Cell.

[42]  William Bateson,et al.  Materials for the Study of Variation: Treated with Especial Regard to Discontinuity in the Origin of Species , 1894 .

[43]  D. Wake,et al.  Miniaturization of Body Size: Organismal Consequences and Evolutionary Significance , 1993 .

[44]  Eutely or Cell Constancy in Its Relation to Body Size , 1932 .

[45]  S P Allen,et al.  Somite number and vertebrate evolution. , 1998, Development.

[46]  M. Hassell,et al.  Variability in the abundance of animal and plant species , 1982, Nature.

[47]  W. Arthur Varable segment number in centipedes: population genetics meets evolutionary developmental biology , 1999, Evolution & development.

[48]  S. Leal Genetics and Analysis of Quantitative Traits , 2001 .

[49]  S. Wright Evolution and the Genetics of Populations, Volume 3: Experimental Results and Evolutionary Deductions , 1977 .

[50]  Arne Ø. Mooers,et al.  Size and complexity among multicellular organisms , 1997 .

[51]  Robert W. Williams,et al.  Natural Variation in Neuron Number in Mice Is Linked to a Major Quantitative Trait Locus on Chr 11 , 1998, The Journal of Neuroscience.

[52]  H. Schnabel,et al.  Assessing normal embryogenesis in Caenorhabditis elegans using a 4D microscope: variability of development and regional specification. , 1997, Developmental biology.

[53]  S. W. Emmons,et al.  The demise of the Platonic worm , 2000 .

[54]  J. Slack Topobiology: An introduction to molecular embryology G. M. Edelman. Basic Books, New York (1988), 240 pp. price $69.50 , 1991, Neuroscience.

[55]  B. Barres,et al.  Programmed cell death and the control of cell survival: lessons from the nervous system. , 1993, Science.

[56]  J. Sulston,et al.  Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. , 1977, Developmental biology.

[57]  A. Arkin,et al.  Stochastic mechanisms in gene expression. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[58]  M. Lynch,et al.  Genetics and Analysis of Quantitative Traits , 1996 .

[59]  R. Strom,et al.  Cell Production and Cell Death in the Generation of Variation in Neuron Number , 1998, The Journal of Neuroscience.

[60]  R Cowan Branching process results in terms of moments of the generation-time distribution. , 1985, Biometrics.

[61]  V. G. Springer,et al.  A Survey of Vertebral Numbers in Sharks , 1964 .

[62]  G. Bell,et al.  DEVELOPMENTAL MUTANTS OF VOLVOX: DOES MUTATION RECREATE THE PATTERNS OF PHYLOGENETIC DIVERSITY? , 1991, Evolution; international journal of organic evolution.

[63]  A. Gray,et al.  I. THE ORIGIN OF SPECIES BY MEANS OF NATURAL SELECTION , 1963 .

[64]  Ian P. Woiwod,et al.  THE DENSITY-DEPENDENCE OF SPATIAL BEHAVIOUR AND THE RARITY OF RANDOMNESS , 1978 .

[65]  M. Keeling Simple stochastic models and their power-law type behaviour. , 2000, Theoretical population biology.

[66]  Sally A. Moody,et al.  Cell lineage and fate determination , 1999 .

[67]  H. Nijhout,et al.  The development and evolution of exaggerated morphologies in insects. , 2000, Annual review of entomology.

[68]  S. Frank The design of adaptive systems: optimal parameters for variation and selection in learning and development. , 1997, Journal of theoretical biology.

[69]  R Cowan,et al.  Cell population dynamics during the differentiative phase of tissue development. , 1986, Journal of theoretical biology.

[70]  A. Arkin,et al.  It's a noisy business! Genetic regulation at the nanomolar scale. , 1999, Trends in genetics : TIG.

[71]  A. Kluge,et al.  Impact of the Lognormal Distribution on Studies of Phenotypic Variation and Evolutionary Rates , 1971 .

[72]  W. Kerfoot Selection of an Appropriate Index for the Study of the Variability of Lizard and Snake Body Scale Counts , 1969 .

[73]  K. Madhavan,et al.  Morphogenesis of the epidermis of adult abdomen of Drosophila. , 2017, Journal of embryology and experimental morphology.

[74]  L. R. Taylor,et al.  Aggregation, Variance and the Mean , 1961, Nature.

[75]  P. Schaap,et al.  The possible involvement of oscillatory cAMP signaling in multicellular morphogenesis of the cellular slime molds. , 1984, Developmental biology.

[76]  E. Davidson,et al.  Origin of Bilaterian Body Plans: Evolution of Developmental Regulatory Mechanisms , 1995, Science.