The nucleotypic effects of cellular DNA content in cartilaginous and ray-finned fishes.

Cytological and organismal characteristics associated with cellular DNA content underpin most adaptionist interpretations of genome size variation. Since fishes are the only group of vertebrate for which relationships between genome size and key cellular parameters are uncertain, the cytological correlates of genome size were examined in this group. The cell and nuclear areas of erythrocytes showed a highly significant positive correlation with each other and with genome size across 22 cartilaginous and 201 ray-finned fishes. Regressions remained significant at all taxonomic levels, as well as among different fish lineages. However, the results revealed that cartilaginous fishes possess higher cytogenomic ratios than ray-finned fishes, as do cold-water fishes relative to their warm-water counterparts. Increases in genome size owing to ploidy shifts were found to influence cell and nucleus size in an immediate and causative manner, an effect that persists in ancient polyploid lineages. These correlations with cytological parameters known to have important influences on organismal phenotypes support an adaptive interpretation for genome size variation in fishes.

[1]  S. Raychaudhuri,et al.  Chromosome numbers, genome sizes, cell volumes and evolution of snake-head fish (family Channidae) , 1988 .

[2]  T. Gregory,et al.  A BIRD'S‐EYE VIEW OF THE C‐VALUE ENIGMA: GENOME SIZE, CELL SIZE, AND METABOLIC RATE IN THE CLASS AVES , 2002, Evolution; international journal of organic evolution.

[3]  P. Hebert,et al.  Genome-size evolution in fishes , 2004 .

[4]  A. Vinogradov.  NUCLEOTYPIC EFFECT IN HOMEOTHERMS: BODY‐MASS INDEPENDENT RESTING METABOLIC RATE OF PASSERINE BIRDS IS RELATED TO GENOME SIZE , 1997, Evolution; international journal of organic evolution.

[5]  M. White,et al.  The blood cells of the Antarctic icefish Chaenocephalus aceratus Lönnberg: light and electron microscopic observations , 1981 .

[6]  A. Mirsky,et al.  THE DESOXYRIBONUCLEIC ACID CONTENT OF ANIMAL CELLS AND ITS EVOLUTIONARY SIGNIFICANCE , 1951, The Journal of general physiology.

[7]  K. Berven.  The genetic basis of altitudinal variation in the wood frog Rana sylvatica II. An experimental analysis of larval development , 2004, Oecologia.

[8]  G. Eble,et al.  Comparative hematology in marine fish. , 1992, Comparative biochemistry and physiology. Comparative physiology.

[9]  Dmitri A Petrov,et al.  Mutational equilibrium model of genome size evolution. , 2002, Theoretical population biology.

[10]  William D. Taylor,et al.  Phenotypic Correlates of Genomic DNA Content in Unicellular Eukaryotes and Other Cells , 1983, The American Naturalist.

[11]  J. Coyne,et al.  Heritability of two morphological characters within and among natural populations of Drosophila melanogaster. , 1987, Genetics.

[12]  R. Pedersen.  DNA content, ribosomal gene multiplicity, and cell size in fish. , 1971, The Journal of experimental zoology.

[13]  T. Benfey.  The Physiology and Behavior of Triploid Fishes , 1999 .

[14]  A. Larson,et al.  DEVELOPMENTAL CORRELATES OF GENOME SIZE IN PLETHODONTID SALAMANDERS AND THEIR IMPLICATIONS FOR GENOME EVOLUTION , 1987, Evolution; international journal of organic evolution.

[15]  Á. Spotorno,et al.  Genome size variation and its phenotypic consequences in Phyllotis rodents. , 1991, Hereditas.

[16]  P. Hebert,et al.  From Pixels to Picograms , 2002, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[17]  T. Gregory,et al.  Nucleotypic effects without nuclei: genome size and erythrocyte size in mammals. , 2000, Genome.

[18]  J. Vaughn,et al.  CHANGING NUCLEAR HISTONE PATTERNS DURING DEVELOPMENT III. THE DEOXYRIBONUCLEIC ACID CONTENT OF SPERMATOGENIC CELLS IN THE CRAB EMERITA ANALOGA , 1969, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[19]  P. F. Scholander,et al.  Climatic Adaptation in Arctic and Tropical Poikilotherms , 1953, Physiological Zoology.

[20]  I. Leslie,et al.  Chemical changes in the developing chick embryo related to the deoxyribonucleic acid content of the nucleus. , 1950, The Biochemical journal.

[21]  E. Olmo.  Quantitative Variations in the Nuclear DNA and Phylogenesis of the Amphibia , 1973 .

[22]  W. Doolittle,et al.  Selfish genes, the phenotype paradigm and genome evolution , 1980, Nature.

[23]  B. Sidell,et al.  Metabolic responses of striped bass (Morone saxatilis) to temperature acclimation. I. Alterations in carbon sources for hepatic energy metabolism. , 1981, The Journal of experimental zoology.

[24]  M. Bennett,et al.  The duration of meiosis , 1971, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[25]  E. Olmo.  Nucleotype and cell size in vertebrates: a review. , 1983, Basic and applied histochemistry.

[26]  R. Gregory,et al.  The modulation of DNA content: proximate causes and ultimate consequences. , 1999, Genome research.

[27]  L. Compagno,et al.  Sharks of the world :an annotated and illustrated catalogue of shark species known to date , 1984 .

[28]  T. Cavalier-smith.  r- and K-tactics in the evolution of protist developmental systems: cell and genome size, phenotype diversifying selection, and cell cycle patterns. , 1980, Bio Systems.

[29]  G. F. Holeton.  Metabolic Cold Adaptation of Polar Fish: Fact or Artefact? , 1974, Physiological Zoology.

[30]  G. A. Horridge,et al.  Animal species and evolution. , 1964 .

[31]  T. Gregory.  The bigger the C-value, the larger the cell: genome size and red blood cell size in vertebrates. , 2001, Blood cells, molecules & diseases.

[32]  J. David,et al.  Similarities and differences in latitudinal adaptation of two Drosophila sibling species , 1975, Nature.

[33]  E. Martins.  The Comparative Method in Evolutionary Biology, Paul H. Harvey, Mark D. Pagel. Oxford University Press, Oxford (1991), vii, + 239 Price $24.95 paperback , 1992 .

[34]  S. Perdrix-Gillot.  DNA synthesis and endomitoses in the giant nuclei of the silkgland of Bombyx mori. , 1979, Biochimie.

[35]  R. Ricklefs,et al.  Applications of phylogenetically independent contrasts : a mixed progress report , 1996 .

[36]  M. Pagel,et al.  Variation across species in the size of the nuclear genome supports the junk-DNA explanation for the C-value paradox , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[37]  B. Sheafor,et al.  Red Blood Cells: Centerpiece in the Evolution of the Vertebrate Circulatory System , 1999 .

[38]  P. Hebert,et al.  The cellular basis of divergent head morphologies in Daphnia , 1997 .

[39]  T. Gregory,et al.  Coincidence, coevolution, or causation? DNA content, cellsize, and the C‐value enigma , 2001, Biological reviews of the Cambridge Philosophical Society.

[40]  R. Ojeda,et al.  Discovery of tetraploidy in a mammal , 1999, Nature.

[41]  B. Sidell,et al.  Structural and biochemical analyses of cardiac ventricular enlargement in cold-acclimated striped bass. , 1997, The American journal of physiology.

[42]  P. A. Lay,et al.  What determines the size of teleost erythrocytes? Correlations with oxygen transport and nuclear volume , 2004, Fish Physiology and Biochemistry.

[43]  J. Van't Hof,et al.  A relationship between DNA content, nuclear volume, and minimum mitotic cycle time. , 1963, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Cellular DNA Contents and Cell Volumes of Batoids , 1995 .

[45]  F. Crick,et al.  Selfish DNA: the ultimate parasite , 1980, Nature.

[46]  V. French,et al.  EVOLUTION AND DEVELOPMENT OF BODY SIZE AND CELL SIZE IN DROSOPHILA MELANOGASTER IN RESPONSE TO TEMPERATURE , 1994, Evolution; international journal of organic evolution.

[47]  T. Cavalier-smith,et al.  Nuclear volume control by nucleoskeletal DNA, selection for cell volume and cell growth rate, and the solution of the DNA C-value paradox. , 1978, Journal of cell science.

[48]  A. Vinogradov.  NUCLEOTYPIC EFFECT IN HOMEOTHERMS: BODY‐MASS‐CORRECTED BASAL METABOLIC RATE OF MAMMALS IS RELATED TO GENOME SIZE , 1995, Evolution; international journal of organic evolution.

[49]  L. Lowcock,et al.  Genome size and metabolic rate in salamanders , 1991 .

[50]  D. Wake,et al.  Genome size, secondary simplification, and the evolution of the brain in salamanders. , 1997, Brain, behavior and evolution.

[51]  A. Morescalchi,et al.  Evolution of the genome and cell sizes in salamanders , 1975, Experientia.

[52]  R. Gregory.  The evolution of the genome , 2005 .

[53]  R. Forster,et al.  The Effect of Size of Red Cells on the Kinetics of Their Oxygen Uptake , 1966, The Journal of general physiology.

[54]  P. G. Martin.  Variation in the amounts of nucleic acids in the cells of different species of higher plants. , 1966, Experimental cell research.

[55]  I. Johnston.  Cold adaptation in marine organisms. , 1990, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[56]  K. Berven,et al.  THE GENETIC BASIS OF ALTITUDINAL VARIATION IN THE WOOD FROG RANA SYLVATICA. I. AN EXPERIMENTAL ANALYSIS OF LIFE HISTORY TRAITS , 1982, Evolution; international journal of organic evolution.

[57]  E. Tchernov,et al.  The evolution of genome size: what can be learned from anuran development? , 2001, The Journal of experimental zoology.

[58]  B. Sidell,et al.  Metabolic responses of striped bass (Morone saxatilis) to temperature acclimation. II. Alterations in metabolic carbon sources and distributions of fiber types in locomotory muscle , 1982 .

[59]  B. Commoner,et al.  Roles Of Deoxyribonucleic Acid in Inheritance , 1964, Nature.

[60]  R. Macarthur,et al.  The Theory of Island Biogeography , 1969 .

[61]  H. Szarski,et al.  Cell size and the concept of wasteful and frugal evolutionary strategies. , 1983, Journal of theoretical biology.

[62]  E. H. Bryant.  MORPHOMETRIC ADAPTATION OF THE HOUSEFLY, MUSCA DOMESTICA L., IN THE UNITED STATES , 1977, Evolution; international journal of organic evolution.

[63]  P. Hebert,et al.  Evolutionary implications of the relationship between genome size and body size in flatworms and copepods , 2000, Heredity.

[64]  S. Ohno,et al.  So much "junk" DNA in our genome. , 1972, Brookhaven symposia in biology.