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Genome size and developmental complexity

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Abstract

Haploid genome size (C-value) is correlated positively with cell size, and negatively with cell division rate, in a variety of taxa. Because these associations are causative, genome size has the potential to impact (and in turn, be influenced by) organism-level characters affected by variation in either of these cell-level parameters. One such organismal feature is development. Developmental rate, in particular, has been associated with genome size in numerous plant, vertebrate, and invertebrate groups. However, rate is only one side of the developmental coin; the other important component is complexity. When developmental complexity is held essentially constant, as among many plants, developmental rate is the visibly relevant parameter. In this case, genome size can impose thresholds on developmental lifestyle (and vice versa), as among annual versus perennial plants. When developmental rate is constrained (as during time-limited amphibian metamorphosis), complexity becomes the notable variable. An appreciation for this rate-complexity interaction has so far been lacking, but is essential for an understanding of the relationships between genome size and development. Moreover, such an expanded view may help to explain patterns of variation in taxa as diverse as insects and fish. In each case, a hierarchical approach is necessary which recognizes the complex interaction of evolutionary processes operating at several levels of biological organization.

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References

  • Bachmann, K., 1972. Nuclear DNA and developmental rate in frogs. Quart. J. Florida Acad. Sci. 35: 225-231.

    Google Scholar 

  • Bachmann, K., K.L. Chambers & H.J. Price, 1985. Genome size and natural selection: observations and experiments in plants, pp. 267-276 in The Evolution of Genome Size, edited by T. Cavalier-Smith. Wiley, Chichester.

    Google Scholar 

  • Bemis, W.E., 1984. Paedomorphosis and the evolution of the Dipnoi. Paleobiology 10: 293-307.

    Google Scholar 

  • Bennett, M.D., 1971. The duration of meiosis. Proc. R. Soc. Lond. B 178: 277-299.

    Google Scholar 

  • Bennett, M.D., 1972. Nuclear DNA content and minimum generation time in herbaceous plants. Proc. R. Soc. Lond. B 181: 109-135.

    Google Scholar 

  • Bennett, M.D., 1976. DNA amount, latitude, and crop plant distribution. Env. Exp. Bot. 16: 93-108.

    Google Scholar 

  • Bennett, M.D., 1987. Variation in genomic form in plants and its ecological implications. New Phytol. 106 (Suppl.): 177-200.

    Google Scholar 

  • Bennett, M.D., I.J. Leitch & L. Hanson, 1998. DNA amounts in two samples of angiosperm weeds. Annal. Bot. 82 (Suppl. A): 121-134.

    Google Scholar 

  • Bullock, D. & A.L. Rayburn, 1991. Genome size variation in Southwestern US Indian maize populations may be a function of effective growing season. Maydica 36: 247-250.

    Google Scholar 

  • Camper, J.D., L.A. Ruedas, J.W. Bickham & J.R. Dixon, 1993. The relationship of genome size with developmental rates and reproductive strategies in five families of neotropical bufonoid frogs. Genet. (Life Sci. Adv.) 12: 79-87.

    Google Scholar 

  • Cavalier-Smith, T., 1985. Introduction: the evolutionary significance of genome size, pp. 1-36 in The Evolution of Genome Size, edited by T. Cavalier-Smith. Wiley, Chichester, UK.

    Google Scholar 

  • Cavalier-Smith, T., 1991. Coevolution of vertebrate genome, cell, and nuclear sizes, pp. 51-86 in Symposium on the Evolution of Terrestrial Vertebrates, edited by G. Ghiara et al. Mucchi, Modena.

  • Chipman, A.D., O. Khaner, A. Hass & E. Tchernov, 2001. The evolution of genome size: what can be learned from anuran development? J. Exp. Zool. (Mol. Dev. Evol.) 291: 365-374.

    Google Scholar 

  • Commoner, B., 1964. Roles of deoxyribonucleic acid in inheritance. Nature 202: 960-968.

    Google Scholar 

  • Dimitri, P. & N. Junakovic, 1999. Revisiting the selfish DNA hypothesis: new evidence on accumulation of transposable elements in heterochromatin. Trends Genet. 15: 123-124.

    Google Scholar 

  • Duellman, W.E. & L. Trueb, 1994. Biology of Amphibians. Johns Hopkins University Press, Baltimore, MD.

    Google Scholar 

  • Eldredge, N., 1985. Unfinished Synthesis. Oxford University Press. Oxford, UK.

    Google Scholar 

  • Finston, T.L., P.D.N. Hebert & R.B. Foottit, 1995. Genome size variation in aphids. Insect Biochem. Mol. Biol. 25: 189-196.

    Google Scholar 

  • Garstang, W., 1951. Larval Forms with Other Zoological Verses. Basil Blackwell, Oxford.

    Google Scholar 

  • Goin, O.B., C.J. Goin & K. Bachmann, 1968. DNA and amphibian life history. Copeia 1968: 532-540.

    Google Scholar 

  • Gould, S.J., 1977. Ontogeny and Phylogeny. Harvard University Press, Cambridge, MA.

    Google Scholar 

  • Gould, S.J., 1998. Gulliver's further travels: the necessity and difficulty of a hierarchical theory of selection. Phil. Trans. R. Soc. Lond. B 353: 307-314.

    Google Scholar 

  • Gregory, T.R. & P.D.N. Hebert, 1999. The modulation of DNA content: proximate causes and ultimate consequences. Genome Res. 9: 317-324.

    Google Scholar 

  • Gregory, T.R., P.D.N. Hebert & J. Kolasa, 2000. Evolutionary implications of the relationship between genome size and body size in flatworms and copepods. Heredity 84: 201-208.

    Google Scholar 

  • Gregory, T.R., 2000. Nucleotypic effects without nuclei: genome size and erythrocyte size in mammals. Genome 43: 895-901.

    Google Scholar 

  • Gregory, T.R., 2001a. Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma. Biol. Rev. 76: 65-101.

    Google Scholar 

  • Gregory, T.R., 2001b. Animal Genome Size Database. http:// www.genomesize.com.

  • Gregory, T.R., 2001c. The bigger the C-value, the larger the cell: genome size and red blood cell size in vertebrates. Blood Cells Mol. Dis. 27: 830-843.

    Google Scholar 

  • Gregory, T.R., 2002. A bird's-eye view of the C-value enigma: genome size, cell size, and metabolic rate in the class Aves. Evolution 56: 121-130.

    Google Scholar 

  • Greilhuber, J., 1997. The problem of variable genome size in plants (with special reference to woody plants), pp. 13-34 in Cytogenetic Studies of Forest Trees and Shrub Species, edited by Z. Borzan & S.E. Schlarbaum. Croatian Forests, Faculty of Forestry, University of Zagreb, Croatia.

    Google Scholar 

  • Greilhuber, J., 1998. Intraspecific variation in genome size: a critical reassessment. Annal. Bot. 82 (Suppl. A): 27-35.

    Google Scholar 

  • Grime, J.P. & M.A. Mowforth, 1982. Variation in genome size-an ecological interpretation. Nature 299: 151-153.

    Google Scholar 

  • Grime, J.P., J.M.L. Shacklock & S.R. Band, 1985. Nuclear DNA contents, shoot phenology and species co-existence in a limestone grassland community. New Phytol. 100: 435-445.

    Google Scholar 

  • Harvey, P.H. & M.D. Pagel, 1991, The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford.

    Google Scholar 

  • Hinegardner, R., 1968. Evolution of cellular DNA content in teleost fishes. Am. Nat. 102: 517-523.

    Google Scholar 

  • Hinegardner, R., 1976. Evolution of genome size, pp. 179-199 in Molecular Evolution, edited by F.J. Ayala. Sinauer Associates, Sunderland.

    Google Scholar 

  • Horner, H.A. & H.C. Macgregor, 1983. C-value and cell volume: their significance in the evolution and development of amphibians. J. Cell Sci. 63: 135-146.

    Google Scholar 

  • Jockusch, E.L., 1997. An evolutionary correlate of genome size change in plethodontid salamanders. Proc. R. Soc. Lond. B: Biol. Sci. 264: 597-604.

    Google Scholar 

  • John, B. & G.L.G. Miklos, 1988. The Eukaryote Genome in Development and Evolution. Allen & Unwin, London.

    Google Scholar 

  • Joss, J.M.P., 1998. Are extant lungfish neotenic? Clin. Exp. Pharmacol. Physiol. 25: 733-735.

    Google Scholar 

  • Kalendar, R., J. Tanskanen, S. Immonen, E. Nevo & A.H. Schulman, 2000. Genome evolution of wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence. Proc. Natl. Acad. Sci. USA 97: 6603-6607.

    Google Scholar 

  • Laurie, D.A. & M.D. Bennett, 1985. Nuclear DNA content in the genera Zea and Sorghum. Intergeneric, interspecific and intraspecific variation. Heredity 55: 307-313.

    Google Scholar 

  • Lay, P.A. & J. Baldwin, 1999. What determines the size of teleost erythrocytes? Correlations with oxygen transport and nuclear volume. Fish Physiol. Biochem. 20: 31-35.

    Google Scholar 

  • Licht, L.E. & L.A. Lowcock, 1991. Genome size and metabolic rate in salamanders. Comp. Biochem. Physiol. 100B: 83-92.

    Google Scholar 

  • Lieberman, B.S. & Vrba, E.S., 1995. Hierarchy theory, selection, and sorting. BioScience 45: 394-399.

    Google Scholar 

  • Loman, J., 1999. Early metamorphosis in common frog Rana temporaria tadpoles at risk of drying: an experimental demonstration. Amphibia-Reptilia 20: 421-430.

    Google Scholar 

  • Marks, S.B. & A. Collazo, 1998. Direct development in Desmognathus aeneus (Caudata: Plethodontidae): a staging table. Copeia 1998: 637-648.

    Google Scholar 

  • Martin, C.C. & R. Gordon, 1995. Differentiation trees, a junk DNA molecular clock, and the evolution of neoteny in salamanders. J. Evol. Biol. 8: 339-354.

    Google Scholar 

  • McLaren, I.A., J.-M. Sévigny & C.J. Corkett, 1988. Body size, development rates, and genome sizes among Calanus species. Hydrobiologia 167/168: 275-284.

    Google Scholar 

  • Mirsky, A.E. & H. Ris, 1951. The desoxyribonucleic acid content of animal cells and its evolutionary significance. J. Gen. Physiol. 34: 451-462.

    Google Scholar 

  • Morescalchi, A., 1990. Cytogenetics and the problem of Lissamphibian relationships, pp. 1-19 in Cytogenetics of Amphibians and Reptiles, edited by E. Olmo. Birkhauser Verlag, Basel, Switzerland.

    Google Scholar 

  • Mowforth, M.A. & J.P. Grime, 1989. Intra-population variation in nuclear DNA amount, cell size and growth rate in Poa annua L. Funct. Ecol. 3: 289-295.

    Google Scholar 

  • Naranjo, C.A., M.R. Ferrari, A.M. Palermo & L. Poggio, 1998. Karyotype, DNA content and meiotic behaviour in five South American species of Vicia (Fabaceae). Annal. Bot. 82: 757-764.

    Google Scholar 

  • Nardi, I., R. Batistoni, S. Marracci & B. Lanza, 1999. Repetitive DNA components of the large Hydromantes genome: phylogenetic and molecular aspects. Herpetologica 55: 131-139.

    Google Scholar 

  • Oeldorf, E., M. Nishioka & K. Bachmann, 1978. Nuclear DNA amounts and developmental rate in holarctic anura. Z. Zool. Syst. Evolutionsforsch. 16: 216-224.

    Google Scholar 

  • Ohno, S., 1974. Animal Cytogenetics, Vol. 4: Chordata, No. 1: Protochordata, Cyclostomata, and Pisces. Gebrüder Borntraeger, Berlin.

    Google Scholar 

  • Olmo, E., 1983. Nucleotype and cell size in vertebrates: a review. Bas. Appl. Histochem. 27: 227-256.

    Google Scholar 

  • Pagel, M. & R.A. Johnstone, 1992. Variation across species in the size of the nuclear genome supports the junk-DNA explanantion for the C-value paradox. Proc. Royal Soc. Lond. B 249: 119-124.

    Google Scholar 

  • Petrov, D.A., T.A. Sangster, J.S. Johnston, D.L. Hartl & K.L. Shaw, 2000. Evidence for DNA loss as a determinant of genome size. Science 287: 1060-1062.

    Google Scholar 

  • Pinder, A.W., K.B. Storey & G.R. Ultsch, 1992. Estivation and hibernation, pp. 250-274 in Environmental Physiology of the Amphibians, edited by M.E. Feder & W.W. Burggren. University of Chicago Press, Chicago.

    Google Scholar 

  • Poggio, L., M. Rosato, A.M. Chiavarino & C.A. Naranjo, 1998. Genome size and environmental correlations in maize (Zea mays ssp. mays, Poaceae). Annal. Bot. 82 (Suppl. A): 107-115.

    Google Scholar 

  • Rayburn, A.L., H.J. Price, J.D. Smith & J.R. Gold, 1985. C-band heterochromatin and DNA content in Zea mays. Am. J. Bot. 72: 1610-1617.

    Google Scholar 

  • Rayburn, A.L., J.W. Dudley & D.P. Biradar, 1994. Selection for early flowering results in simultaneous selection for reduced nuclear DNA content in maize. Plant Breed. 112: 318-322.

    Google Scholar 

  • Resslar, P.M., J.M. Stucky & J.P. Miksche, 1981. Cytophotometric determination of the amount of DNA in Arachis L. sect. Arachis (Leguminosae). Am. J. Bot. 68: 149-153.

    Google Scholar 

  • Roth, G., B. Rottluff, W. Grunwald, J. Hanken & R. Linke, 1990. Miniaturization in plethodontid salamanders (Caudata: Plethodontidae) and its consequences for the brain and visual system. Biol. J. Linn. Soc. 40: 165-190.

    Google Scholar 

  • Roth, G., K.C. Nishikawa, C. Naujoks-Manteuffel, A. Schmidt & D.B. Wake, 1993. Paedomorphosis and simplification in the nervous system of salamanders. Brain Behav. Evol. 42: 137-170.

    Google Scholar 

  • Roth, G. & A. Schmidt, 1993. The nervous system of plethodontid salamanders: insight into the interplay between genome, organism, behavior, and ecology. Herpetologica 49: 185-194.

    Google Scholar 

  • Roth, G., J. Blanke & D.B. Wake, 1994. Cell size predicts morphological complexity in the brains of frogs and salamanders. Proc. Natl. Acad. Sci. USA 91: 4796-4800.

    Google Scholar 

  • Roth, G., K.C. Nishikawa & D.B. Wake, 1997. Genome size, secondary simplification, and the evolution of the brain in salamanders. Brain Behav. Evol. 50: 50-59.

    Google Scholar 

  • SanMiguel, P. & J.L. Bennetzen, 1998. Evidence that a recent increase in maize genome size was caused by the massive amplification of intergene retrotransposons. Annal. Bot. 82 (Suppl. A): 37-44.

    Google Scholar 

  • SanMiguel, P., B.S. Gaut, A. Tikhonov, Y. Nakajima & J.L. Bennetzen, 1998. The paleontology of intergene retrotransposons of maize. Nature Genet. 20: 43-45.

    Google Scholar 

  • Sessions, S.K. & A. Larson, 1987. Developmental correlates of genome size in plethodontid salamanders and their implications for genome evolution. Evolution 41: 1239-1251.

    Google Scholar 

  • Shaffer, H.B. & S.R. Voss, 1996. Phylogenetic and mechanistic analysis of a developmentally integrated character complex: alternate life history modes in ambystomatid salamanders. Am. Zool. 36: 24-35.

    Google Scholar 

  • Shahbasov, V.G. & A.V. Ganchenko, 1990. Nonspecific tolerance and DNA content in genome of amphibians. Dokl. Akad. Nauk SSSR 314: 971-975.

    Google Scholar 

  • Singh, K.P., S.N. Raina & A.K. Singh, 1996. Variation in chromosomal DNA associated with the evolution of Arachis species. Genome 39: 890-897.

    Google Scholar 

  • Srivastava, S. & U.C. Lavania, 1991. Evolutionary DNA variation in Papaver. Genome 34: 763-768.

    Google Scholar 

  • Swift, H., 1950. The constancy of desoxyribose nucleic acid in plant nuclei. Proc. Natl. Acad. Sci. USA 36: 643-654.

    Google Scholar 

  • Szarski, H., 1983. Cell size and the concept of wasteful and frugal evolutionary strategies. J. Theoret. Biol. 105: 201-209.

    Google Scholar 

  • Thomson, K.S., 1972. An attempt to reconstruct evolutionary changes in the cellular DNA content of lungfish. J. Exp. Zool. 180: 363-372.

    Google Scholar 

  • Thomson, K.S. & K. Muraszko, 1978. Estimation of cell size and DNA content in fossil fishes and amphibians. J. Exp. Zool. 205: 315-320.

    Google Scholar 

  • Vignali, R. & I. Nardi, 1996. Unusual features of the urodele genome: do they have a role in evolution and development? Intl. J. Dev. Biol. 40: 637-643.

    Google Scholar 

  • Vinogradov, A.E., 1995. Nucleotypic effect in homeotherms: body mass-corrected basal metabolic rate of mammals is related to genome size. Evolution 49: 1249-1259.

    Google Scholar 

  • Vinogradov, A.E., 1997. Nucleotypic effect in homeotherms: bodymass independent metabolic rate of passerine birds is related to genome size. Evolution 51: 220-225.

    Google Scholar 

  • Vinogradov, A.E., 1999. Genome in toto. Genome 42: 361-362.

    Google Scholar 

  • Wake, D.B. & G. Roth, 1989. Paedomorphosis: new evidence for its importance in salamander evolution. Am. Zool. 29: 134A.

    Google Scholar 

  • Wake, D.B. & S.B. Marks, 1993. Development and evolution of plethodontid salamanders: a review of prior studies and a prospectus for future research. Herpetologica 49: 194-203.

    Google Scholar 

  • Watanabe, K., T. Yahara, T. Denda & K. Kosuge, 1999. Chromosomal evolution in the genus Brachyscome (Asteraceae, Astereae): statistical tests regarding correlation between changes in karyotype and habit using phylogenetic information. J. Plant Res. 112: 145-161.

    Google Scholar 

  • White, M.M. & I.A. McLaren, 2000. Copepod development rates in relation to genome size and 18S rDNA copy number. Genome 43: 750-755.

    Google Scholar 

  • Whiteman, H.H., 1994. Evolution of facultative paedomorphosis in salamanders. Quart. Rev. Biol. 69: 205-221.

    Google Scholar 

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Ryan Gregory, T. Genome size and developmental complexity. Genetica 115, 131–146 (2002). https://doi.org/10.1023/A:1016032400147

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