Comparative studies of the presence and expression of Hox genes have been made in the invertebrates. It was found that the branchiopod crustacean Artemia franciscana has at least four different Hox genes, which are equivalent to those of the insects (Averof and Akam, 1995). It was also found that certain genetic defects due to the Deformed gene, Dfd, of Drosophila melanogaster are remediated by the transfection of the human HOX 4.2 gene (McGinnis et al., 1990).
Lynch and Conery (2000) proposed that the process of genomic duplication contributed more to the diversification of the species through the loss or silencing of extra-copies, than through the creation of new functions. This model is called speciation through duplication of the genome, and divergent resolution. The evolution of the duplicated genes can occur through three different routes: 1) a copy can be silenced by degenerative mutations (nonfunctionalization); 2) a copy can acquire a new function and be preserved through natural selection, while the other continues with the original function (“neo-functionalization”); 3) both copies could have mutations that reduce expression to that of the single-copy ancestor gene (“subfunctionalization”). Previously studies had been made of the electrophoretic patterns of an albumin type plasmatic protein, comparing the diploid anuran O. cultripes and the tetraploid O. americanus. While electrophoresis of the 2n, with two co-dominant alleles, showed three phenotypes in the population, following a (p + q)2 distribution, the 4n had five phenotypes, giving a (p + q)4 distribution (Beçak et al., 1968b; Beçak, 1969). Similar observations were found in the electrophoresis of the G6PD, 6-PGD and LDH enzyme patterns (Schwantes et al., 1969). The results demonstrated that the four genes of 4n were expressed in each individual, but quantitatively the final product was similar to that of the 2n. Two hypotheses were formulated (Beçak, 1969): 1) there was asynchrony in the genomes of the 4n, resulting in a situation in which one diploid lot was active at a time; 2) at the level of regulatory genes, there was a greater repression of the 4n genome, in comparison with the 2n genome that actually could be translated as a higher methylation level in the 4n as compared to the 2n. These two hypotheses could be correlated. These hypotheses approximate those of the mechanism proposed by Lynch and Conery (2000), called “subfunctionalization”.
The suggestion that the tandem duplications also had an important role in the increase in anatomical complexity was reinforced by the comparative data of the Hox genes in Coelenterata and Bilateria (Rosa et al., 1999). An increase was found in the median Hox genes in the divergence of the Coelenterata and Bilateria, before the radiation of the latter group. Increases in the posterior Hox genes also would have occurred in the Enterocoela, including the vertebrates, after divergence from the other Bilateria.
The theory of evolution through genomic duplication establishes that polyploidy ceases to occur from the reptiles on, due to the development of differentiated sexual chromosomes. The total duplication of the chromosomes would affect the equilibrium of the mechanism of sex determination (Figure 4). In the case of bisexual homeothermic animals, there are rare reports of autopolyploidy, as has been described in a 3n chicken (Ohno et al., 1963). Among the rodents, it was suggested that Mesocricetus auratus (2n = 44) is an allopolyploid species originated from the hybridization of Cricetus cricetus with Cricetus griseus (2n = 22). However, the DNA values (Moses and Yerganian, 1952) do not support this idea. The recent description of tetraploid rodents Tympanoctomys barrerae (Octodontidae, 4n = 102) is supported by DNA content data (Gallardo et al., 1999). Detailed cytological analyses remain to be made for a characterization of the type of ploidy. In humans, there are known cases of ploidies in fetuses, in inviable newborns, and in a few isolated cases of tetraploid or mosaic children, which have survived a few years (Edwards et al., 1967; Gardner, 1982).
PANANIMALIA GENOME - CAMBRIAN
Anaximander, a Greek philosopher (6th century B.C.) suggested that life began from a primordial mud, going through a sequence from inferior to superior life forms, giving rise to man from a type of fish.
The notable paleontological discovery of the Cephalochordata Yunnanozoon lividum in Cambrian rocks in China (Chen et al, 1995) indicates that the Chordata emerged during the Cambrian explosion. This event apparently occurred during a short period of 10 million years. Equally interesting was the finding of the Agnatha Promissum pulchrum in the upper Ordovician in South Africa (Gabbot et al, 1995). According to Gould (1995), the Cambrian explosion indicates the abrupt formation of the Animal kingdom, in which all of the structural archetypes arose during the same period. The paleontological data, together with the molecular information of the Hox genes in animals that descended from the Cambrian, convinced Ohno (1996, 1999) that the second polyploidy coincided with the development of the Gnathostomata in the Ordovician period.
The theory of the pananimalia genome proposed that various phyla of the animal kingdom emerged simultaneously during this short period of Cambrian explosion, without the individual genes presenting functional diversification. Otherwise, all of the animals of the various phyla would have the same genome, differing in the differential use of groups of individual genes (Ohno, 1996, 1997). A prototype would be Hallucigenia sparsa, probably having only one Hox gene, or a group of eight Hox genes, as in the arthropods.
PHYLOGENY OF THE ANURANS BASED ON HYPOTHESIS 2R
The phylogeny of the amphibia is not well resolved due to the rarity of fossils between the Paleozoic and the present. Based on the genetic theory of evolutive polyploidy, the origin of the modern amphibians (Anura, Urodela and Apoda) is polyphyletic (Ohno, 1970). The most primitive amphibian, Ichthyostega, of the extinct subclass Stegocephalia, would have appeared in the Devonian, through the evolution of Osteolepis fish (Crossopterygii, Rhipidistia) (Figure 4). In the following period, Carboniferous and Permian, these first amphibians, Ichthyostega, originated two phylogenetic lines, producing the Lepospondyli and the Rhachitomes. The former would have given origin to the modern Urodela and Gymnophiona, and the latter to the modern Anura. There would also have been branching in the Ichthyostega line, which gave rise to the first reptiles (Cotylosaurus). These reptiles would have given rise, through branching, to the Diapsida, Anapsida and Synapsida. The Diapsida branched out, giving rise to the dinosaurs, pterosaurs, other reptiles, birds, crocodiles, and Rhynchocephalia. The Anapsida apparently evolved to turtles, and the Synapsida became the Icthiosaurs and mammals.
The molecular estimates, based on differences in gene sequences, were found to be coherent with calculations made based on fossil evidence. A difference between the two calculations was found in the diversification of certain orders of placental mammals, at the beginning of the Cretaceous, and before the extinction of the dinosaurs, in the Cretaceous-Jurassic period. A four times greater divergence in the molecular clock, than that previously established from fossil evidence, was also found for the rodents (Kumar and Hedges, 1998).
Morescalchi, 1973, established a phylogenic model in Amphibia, comparing their data on DNA quantity and cytogenetic characters with those of various other authors. In Anura, they took into account the presence of microchromosomes in ancient families, such as the Ascaphidae and the Discoglossidae (Bogart, 1970), the polyploidy in the Leptodactylidae (Beçak et al., 1966, 1967; Bogart, 1967), centric fusions (Wickbom, 1945, 1949; Beçak, 1968; Rabello, 1970), the types of meiotic chiasmata in various families and the supernumerary chromosomes (Ullerich, 1967; Rabello, 1970). Single or multiple post-polyploidy translocations (Beçak and Beçak, 1974b, 1998) and translocations in diploids (Lourenço et al., 2000) were found after this analysis, as were differentiated sexual chromosomes (Schmid, 1980; Schempp and Schmid, 1981; Schmid et al., 1983). The model of Morescalchi indicates that in Anura the oldest families, Ascaphidae and Discoglossidae, evolved to Pipidae, Rhinophrynidae, Pelobatidae, and Leptodactylidae, in the upper Jurassic. Hylidae, Ranidae and Bufonidae originated from the Leptodactylidae. Fossils of the Microhylidae have only been found in the Cenozoic (Miocene); it is not known if these anurans arose recently, or if they are more primitive. We conclude that the genomic duplication in tetraploid and octoploid anurans in the Leptodactylidae, Hylidae and other families, indicates that this mechanism can occur as an independent event, and more than once in the same evolutionary lineage.
We thank Helir Serralvo for help with editing and with photomicroscopy.
Acedo, M.D.P., Paranhos-Baccalà, G., Denoya, C.D. and Ruiz, I.R.G. (1997). Molecular cloning of exons II and III of the a-globin major gene from Odontophrynus americanus 2n and 4n (Amphibia, Anura). Braz. J. Genet. 20: 613-617.
Adams, K.L., Cronn, R., Percifield, R. and Wendel, J.F. (2003). Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc. Natl. Acad. Sci. USA 100: 4649-4654.
Almeida, T.M.B., Ruiz, I.R.G. and Beçak, W. (1986). Ribosomal gene activity detected by silver staining in two diploid populations of Odontophrynus americanus (Amphibia, Anura) from Southern Brazil. Rev. Bras. Genet. IX: 433-437.
Alvares, L.E., Brison, O. and Ruiz, I.R.G. (1998). Identification of enhancer-like elements in the ribosomal intergenic spacer of Odontophrynus americanus 2n and 4n (Amphibia, Anura). Genetica 104: 41-44.
Amores, A., Force A., Yan, Y.-L., Joly, L., Amemiya, C., Fritz, A., Ho, R.K., Langeland, J., Prince, V., Wang, Y.-L., Westerfield, M., Ekker, M. and Postlethwait, J.H. (1998). Zebrafish hox clusters and vertebrate genome evolution. Science 282: 1711-1714.
Aparicio, S., Hawker, K., Cottage, A., Mikawa, Y., Zuo, L., Venkatesh, B., Chen, E., Krumlauf, R. and Brenner, S. (1997). Organization of the Fugu rubripes Hox clusters: evidence for continuing evolution of vertebrate Hox complexes. Nat. Genet. 16: 79-83.
Atkin, N.B. and Ohno, S. (1967). DNA values of four primitive chordates. Chromosoma 23: 10-13.
Averof, M. and Akam, M. (1995). Hox genes and the diversification of insect and crustacean body plans. Nature 376: 420-423.
Bachmann, K. and Bogart, J.P. (1975). Comparative cytochemical measurements in the diploid-tetraploid species pair of hylid frogs Hyla chrysoscelis and H. versicolor. Cytogenet. Cell Genet. 15: 186-194.
Bailey, J.A., Carrel, L., Chakravarti, A. and Eichler, E.E. (2000). Molecular evidence for a relationship between LINE-1 elements and X chromosome inactivation: The Lyon repeat hypothesis. Proc. Natl. Acad. Sci. USA 97: 6634-6639.
Batistic, R.F., Beçak, W. and Beçak, M.L. (1973). DNA autoradiographic patterns in diploid, triploid and tetraploid amphibians (Ceratophrydidae). Cytologia 36: 687-697.
Batistic, R.F., Soma, M., Beçak, M.L. and Beçak, W. (1975). Further studies on polyploid amphibians - A diploid population of Phillomedusa burmeisteri. J. Hered. 66: 160-162.
Baylin, S.B. and Herman, J.G. (2000). DNA hypermethylation in tumorigenesis. Trends Genet. 16: 168-173.
Beçak, M.L. (1968). Chromosomal analysis of eighteen species of Anura. Caryologia 21: 191-208.
Beçak, M.L. and Beçak, W. (1970). Further studies on polyploid amphibians (Ceratophrydidae). III. Meiotic aspects of the interspecific triploid hybrid: Odontophrynus cultripes (2n = 22) x O. americanus (4n = 44). Chromosoma 31: 377-385.
Beçak, M.L. and Beçak, W. (1974a). Studies on polyploid amphibians. Karyotype evolution and phylogeny of the genus Odontophrynus. J. Herpetol. 8: 337-341.
Beçak, M.L. and Beçak, W. (1974b). Diploidization in Eleutherodactylus (Leptodactylidae-Amphibia). Experientia 30: 624-625.
Beçak, M.L. and Beçak, W. (1998). Evolution by polyploidy in Amphibia: new insights. Cytogenet. Cell Genet. 80: 28-33.
Beçak, M.L. and Fukuda, K. (1979). Arrangement of nucleosomes in condensed chromatin fibres. Experientia 35: 24-26.
Beçak, M.L. and Fukuda-Pizzocaro, K. (1980). Chromatin circles in amphibian previtelogenic oocytes. Experientia 36: 164-166.
Beçak, M.L., Beçak, W. and Rabello, M.N. (1966). Cytological evidence of constant tetraploidy in the bisexual South American frog Odontophrynus americanus. Chromosoma 19: 188-193.
Beçak, M.L., Beçak, W. and Rabello, M.N. (1967). Further studies on polyploid amphibians (Ceratophrydidae). I. Mitotic and meiotic aspects. Chromosoma 22: 192-201.
Beçak, M.L., Denaro, L. and Beçak, W. (1970a). Polyploidy and mechanisms of karyotypic diversification in Amphibia. Cytogenetics 9: 225-238.
Beçak, M.L., Beçak, W. and Vizotto, L.D. (1970b). A diploid population of the polyploid amphibian Odontophrynus americanus and an artificial intraspecific triploid hybrid. Experientia 26: 545-546.
Beçak, M.L., Fukuda, K. and Mendes Carneiro, S. (1977). Chromatin ultrastructure of lower vertebrates. Experientia 33: 1314-1316.
Beçak, M.L., Mendes Carneiro, S. and Fukuda, K. (1978). Circles in spermatocyte chromatin loops. Electron microscopy and AgAs-NORs studies. Experientia 34: 171-172.
Beçak, M.L., Stocco dos Santos, R.C., Soares-Scott, M.D., Batistic, R.F. and Costa, H. (1988). Chromosome structure in man and Amphibia-Anura, restriction enzymes. Rev. Bras. Genet. 11: 939-948.
Beçak, W. (1969). Genic action and polymorphism in polyploid species of amphibians. Genetics 61 (Suppl): 183-190.
Beçak, W. and Goissis, G. (1971). DNA and RNA content in diploid and tetraploid amphibians. Experientia 27: 345-346.
Beçak, W. and Pueyo, M.T. (1970). Gene regulation in the polyploid amphibian Odontophrynus americanus. Exp. Cell Res. 63: 448-451.
Beçak, W., Beçak, M.L., Lavalle, D. and Schreiber, G. (1967). Further studies on polyploid amphibians (Ceratophrydidae) II. Content and nuclear volume. Chromosoma 23: 14-23.
Beçak, W., Beçak, M.L. and Langlada, F.G. (1968a). Artificial triploid hybrids by interspecific mating of Odontophrynus (Amphibia-Anura). Experientia 24: 1162-1163.
Beçak, W., Schwantes, A.R. and Schwantes, M.L. (1968b). Polymorphism of albumin-like proteins in the South American tetraploid frog Odontophrynus americanus (Salientia: Ceratophrydidae). J. Exp. Zool. 168: 473-476.
Beçak, W., Beçak, M.L., Schreiber, G., Lavalle, D. and Amorim, F.O. (1970). Interspecific variability of DNA content in Amphibia. Experientia 22: 204-206.
Bernardi, G., Olofsson, B., Filipski, J., Zerial, M., Salinas, J., Cuny, G., Meunier-Rotival, M. and Rodier, F. (1985). The mosaic genome of warm-blooded vertebrates. Science 228: 953-958.
Bestor, T.H. (1990). DNA methylation: evolution of a bacterial immune function into a regulator of gene expression and genome structure in higher eukaryotes. Philos. Trans. R. Soc. Lond.B. Biol. Sci. 326: 179-187.
Bird, A.P. (1995). Gene number, noise reduction and biological complexity. Trends Genet. 11: 94-100.
Bird, A. (2002). DNA methylation patterns and epigenetic memory. Genes Dev. 16: 6-21.
Birnstein, V.J. (1982). Structural characteristics of genome organization in Amphibia: Differential staining of chromosomes and DNA structure. J. Mol. Evol. 18: 73-91.
Bogart, J.P. (1967). Chromosomes of the South American amphibian family Ceratophridae with a reconsideration of the taxonomic status of Odontophrynus americanus. Can. J. Genet. Cytol. 9: 531-542.
Bogart, J.P. (1970). Systematic problems in the amphibian family Leptodactylidae (Anura) as indicated by karyotypic analysis. Cytogenetics 9: 369-383.
Bogart, J.P. and Wasserman, A.O. (1972). Diploid-polyploid cryptic species pairs: a possible clue to evolution by polyploidization in anuran amphibians. Cytogenetics 11: 7-24.
Borel, F., Lohez, O.D., Lacroix, F.B. and Margolis, R.L. (2002). Multiple centrosomes arise from tetraploidy checkpoint failure and mitotic centrosome clusters in p53 and RB pocket protein-compromised cells. Proc. Natl. Acad. Sci. USA 99: 9818-9824.
Chen, J.-Y., Dzik, J., Edgecombe, G.-D., Ramsköld, L. and Zhou, G.-Q. (1995). A possible Early Cambrian chordate. Nature 377: 720-722.
Cianciarullo, A.M., Naoum, P.C., Bertho, A.L., Kobashi, L.S., Beçak, W. and Soares, M.J. (2000). Aspects of gene regulation in the diploid and tetraploid Odontophrynus americanus (Amphibia, Anura, Leptodactilydae). Gen. Mol. Biol. 23: 357-364.
Comings, D.E., Avelino, E. and Beçak, W. (1973). Heavy shoulder DNA in snakes. Cytogenet. Cell Genet. 12: 2-7.
Cortadas, J. and Ruiz, I.R.G. (1988). The organization of ribosomal genes in diploid and tetraploid species of the genus Odontophrynus (Amphibia, Anura). Chromosoma 96: 437-442.
Dillon, N. and Festenstein, R. (2002). Unravelling heterochromatin: competition between positive and negative factors regulates accessibility. Trends Genet. 18: 252-258.
Edwards, J.H., Yuncken, C., Rushton, D.I., Richards, S. and Mittwoch, U. (1967). Three cases of triploidy in man. Cytogenetics 6: 81-104.
Felsenfeld, G. (1992). Chromatin as an essential part of the transcriptional mechanism. Nature 355: 219-224.
Gabbot, S.E., Aldridge, R.J. and Theron, J.N. (1995). A giant conodont with preserved muscle tissue from the upper Ordovician of South Africa. Nature 374: 800-803.
Gallardo, M.H., Bickham, J.W., Honeycutt, R.L., Ojeda, R.A. and Köhler, N. (1999). Discovery of tetraploidy in a mammal. Nature 401: 341.
Garcia-Fernandez, J. and Holland, P.W. (1994). Archetypal organization of the amphioxus Hox genes cluster. Nature 370: 563-566.
Gardner, L.I. (1982). The lessons of polyploid. Relation to congenital asymmetry and the Russell-Silver syndrome. Am. J. Dis. Child. 36: 292-293.
Gould, S.J. (1995). Of it, not above it. Nature 377: 681-682.
Hashimshony, T., Zhang, J., Keshet, I., Bustin, M. and Cedar, H. (2003). The role of DNA methylation in setting up chromatin structure during development. Nat. Genet. 34: 187-192.
Hendrich, B. and Tweedie, S. (2003). The methyl-CpG binding domain and the evolving role of DNA methylation in animals. Trends Genet. 19: 269-277.
Jackson-Grusby, L., Beard, C., Possemato, R., Tudor, M., Fambrough, D., Csankovszki, G., Dausman, J., Lee, P., Wilson, C., Lander, E. and Jaenisch, R. (2001). Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nat. Genet. 27: 31-39.
Jenkins Jr., F.A. and Walsh, D.M. (1993). An Early Jurassic caecilian with limbs. Nature 365: 246-250.
Jost, J.P. and Hofsteenge, J. (1992). The repressor MDBP-2 is a member of the histone H1 family that binds preferentially in vitro and in vivo to methylated nonspecific DNA sequences. Proc. Natl. Acad. Sci. USA 89: 9499-9503.
Kawamura, T. (1984). Polyploidy in amphibians. Zool. Sci. 1: 1-5.
Koh, E.G.L., Lam, K., Christoffels, A., Erdmann, M.V., Brenner, S. and Venkatesh, B. (2003). Hox gene clusters in the Indonesian Coelacanth, Latimeria menadoensis. Proc. Natl. Acad. Sci. USA 100: 1084-1088.
Kumar, S. and Hedges, S.B. (1998). A molecular time scale for vertebrate evolution. Nature 392: 917-919.
Larhammar, D. and Risinger, C. (1994). Why so few pseudogenes in the tetraploid species? Trends Genet. 10: 418-419.
Lourenço, L.B., Recco-Pimentel, S.M. and Cardoso, A.J. (2000). A second case of multivalent meiotic configurations in diploid species of Anura. Genet. Mol. Biol. 23: 131-133.
Lynch, M. and Conery, J.S. (2000). The evolution fate and consequences of duplicate gene. Science 290: 1151-1155.
Lyon, M.F. (1998). X-chromosome inactivation: a repeat hypothesis. Cytogenet. Cell Genet. 80: 133-137.
Lyon, M.F. (2000). LINE-1 elements and X chromosome inactivation: A function for “junk” DNA? Proc. Natl. Acad. Sci. USA 97: 6248-6249.
Martin, A.P. (1999). Increasing genomic complexity by gene duplication and the origin of vertebrates. Am. Nat. 154: 111-128.
Mendes-Carneiro, S. (1975). Observações sobre a ultra-estrutura das células germinativas masculinas da espécie diplo-tetraplóide de Odontophrynus americanus (Amphibia-Anura). Mem. Inst. Butantan 39: 135-148.
McGinnis, N., Kuziora M.A. and McGinnis, W. (1990). Human Hox-4.2 and Drosophila Deformed encode similar regulatory specificities in Drosophila embryos and larvae. Cell 63: 969-976.
Mezquita, J., Connor, W., Einkfein, R.J. and Dixon, G.H. (1985). An H-1 histone gene from rainbow-trout (Salmo gairdnerii). J. Mol. Evol. 21: 209-219.
Moore, G. (2002). Meiosis in allopolyploids - the importance of “Tefloon” chromosomes. Trends Genet. 18: 456-463.
Morescalchi, A. (1973). Amphibia. In: Cytotaxonomy and Vertebrate Evolution (Chiarelli, A.B. and Capanna, E., eds.). Academic Press, London, New York, pp. 223-348.
Moses, M.J. and Yerganian, G. (1952). Desoxypentose nucleic acid (DNA) content and cytotaxonomy of several Cricetinae (hamster). Genetics 37: 607-608.
Muller, H.J. (1925). Why polyploidy is rare in animals than in plants. Ann. Nat. 59: 346-353.
Mutter, G.L., Stewart, C.L., Chaponot, M.L. and Pomponio, R.J. (1993). Oppositely imprinted genes H19 and insulin-like growth factor 2 are coexpressed in human androgenetic trophoblast. Am. J. Hum. Genet. 53: 1096-1102.
Naruya, S. (2002). Evolutionary genomics: molecular evolution at the genomic scale. Trends Genet. 18: 239-240.
Ohno, S. (1970). Evolution by Gene Duplication. Spring-Verlag, Berlin, Heidelberg, New York.
Ohno, S. (1996). The notion of the Cambrian pananimalia genome. Proc. Natl. Acad. Sci. USA 93: 8475-8478.
Ohno, S. (1997). The reason for as well as the consequence of the Cambrian explosion in animal evolution. J. Mol. Evol. 44 (Suppl): S23-S27.
Ohno, S. (1999). Gene duplication and the uniqueness of vertebrate genome circa 1970-1999. Sem. Cell Dev. Biol. 10: 517-522.
Ohno, S. and Atkin, N.B. (1966). Comparative DNA values and chromosome complements of eight species of fishes. Chromosoma 18: 455-466.
Ohno, S. and Beçak, M.L. (1993). Can a protein influence the fate of its own coding sequence? The amino- and carboxyl-terminal regions of H1 histone. Proc. Natl. Acad. Sci. USA 90: 7341-7345.
Ohno, S., Kittrell, W.A., Christian, L.C., Stenius, C. and Witt, G.A. (1963). An adult triploid chicken (Gallus domesticus) with a left ovotestis. Cytogenetics 2: 42-49.
Ohno, S., Wolf, U. and Atkin, N.B. (1968). Evolution from fish to mammals by gene duplication. Hereditas 59: 169-187.
Osborn, T.C., Pires, J.C., Birchler, J.A., Auger, D.L., Chen, Z.J., Lee, H.S., Comai, L., Madlung, A., Doerge, R.W., Colot, V. and Martienssen, R.A. (2003). Understanding mechanisms of novel gene expression in polyploids. Trends Genet. 19: 141-147.
Park, K.-Y. and Pfeifer, K. (2003). Epigenetic interplay. Nat. Genet. 34: 126-128.
Postlethwait, J.H., Yan, Y.L., Gates, M.A., Horne, S., Amores, A., Brownlie, A., Donovan, A., Egan, E.S., Force, A., Gong, Z., Goutel, C., Fritz, A., Kelsh, R., Knapik, E., Liao, E., Paw, B., Ransom, D., Singer, A., Thomson, M., Abduljabbar, T.S., Yelick, P., Beier, D., Joly, J.S., Larhammar, D., Rosa, F., Westerfield, M., Zon, L.I., Johnson, S.L., Talbot, W.S. and Ekker, M. (1998). Vertebrate genome evolution and the zebrafish gene map. Nat. Genet. 18: 345-349.
Rabello, M.N. (1970). Chromosomal studies in Brazilian anurans. Caryologia 23: 45-59.
Rosa, R. de, Grenier, J.K., Andreeva, T., Cook, C.E., Adoutte, A., Akam, M., Carroll, S.B. and Balavoine, G. (1999). Hox genes in brachiopods and priapulids and protostome evolution. Nature 339: 772-776.
Ruiz, I.R.G. and Beçak, W. (1976). Further studies on polyploid amphibians V. C-banding in diploid and tetraploid species of Odontophrynus. Chromosoma 54: 69-74.
Ruiz, I.R.G. and Brison, O. (1989). Methylation of ribosomal cistrons in diploid and tetraploid Odontophrynus americanus (Amphibia, Anura). Chromosoma 98: 86-92.
Ruiz, I.R.G., Bonaldo, M.F. and Beçak, W. (1980). In situ localization of ribosomal genes in a natural triploid of Odontophrynus. J. Hered. 71: 55-57.
Ruiz, I.R.G., Soma, M. and Beçak, W. (1981). Nucleolar organizer regions and constitutive heterochromatin in polyploid species of the genus Odontophrynus (Amphibia, Anura). Cytogenet. Cell Genet. 29: 84-98.
Saez, F.A. and Brum-Zorilla, N. (1966). Karyotype variation in some species of the genus Odontophrynus (Amphibia, Anura). Caryologia 19: 55-63.
Schempp, W. and Schmid, M. (1981). Chromosome banding in Amphibia. VI. BrdU-replication patterns in anura and demonstration of XX/XY sex chromosomes in Rana esculenta. Chromosoma 83: 697-710.
Schmid, M. (1978). Chromosome banding in Amphibia I. Constitutive heterochromatin and nucleolar regions in Bufo adn Hyla. Chromosoma 66: 361-388.
Schmid, M. (1980). Chromosome banding in Amphibia. V. Highly differentiated ZZ/ZW sex chromosomes and exceptional genomes size in Pyxicephalus adspersus (Anura, Ranidae). Chromosoma 80: 69-96.
Schmid, M. and Almeida, C.G. (1988). Chromosome banding in Amphibia XII. Restriction endonuclease banding. Chromosoma 96: 283-290.
Schmid, M., Haaf, T., Geile, B. and Sims, S. (1983). Unusual heteromorphic sex chromosomes in a marsupial frog. Experientia 39: 1153-1155.
Schmid, M., Haaf, T. and Schempp, W. (1985). Chromosome banding in Amphibia IX. The polyploid karyotypes of Odontophrynus americanus and Ceratophrys ornata (Anura, Leptodactylidae). Chromosoma 91: 172-184.
Schmidtke, J., Beçak, W. and Engel, W. (1976). The reduction of genic activity in the tetraploid Odontophrynus americanus is not due to loss of ribosomal DNA. Experientia 32: 27-28.
Schwantes, A.R., Schwantes, M.L.B. and Beçak, W. (1969). Electrophoretic patterns of G-6-PD, 6-PGD and LDH in polyploid amphibians (Ceratophrydidae). Rev. Bras. Pesqui. Med. Biol. 2: 41-44.
Schwantes, M.L.B., Schwantes, A.R. and Beçak, W. (1976). Estudo comparativo de dez enzimas num sistema diploide do gênero Odontophrynus americanus (Ceratophrynidae-Anura). Cienc. Cult. 28 (Suppl): 280-281.
Schwantes, M.L.B., Schwantes, A.R. and Beçak, W. (1977). Electrophoretic studies on polyploid amphibians. I. 6-phosphogluconatedehydrogenase (6-PGD). Comp. Biochem. Physiol. 56B: 393-396.
Simmen, N.W., Leitgeb, S., Clarck, V.H., Jones, S.J.M. and Bird, A. (1998). Gene number in an invertebrate chordata, Ciona intestinalis. Proc. Natl. Acad. Sci. USA 95: 4437-4460.
Soares-Scott, M.D., Trajtengertz, I., Soma, M. and Beçak, M.L. (1988). C and AgAs bands of the octaploid untanha frog Ceratophrys dorsata (C. aurita) (8n = 104, Amphibia, Anura). Rev. Bras. Genet. 11: 625-631.
Spring, J. (1997).Vertebrate evolution by interspecific hybridisation - are we polyploid? FEBS Lett. 400: 2-8.
Strahl, B. and Allis, C.D. (2000). The language of covalent histone modifications. Nature 403: 41-45.
Ullerich, F. (1967). Weitere untersuchungen über chromosomen verhältnisse und DNS-gehalt bei Anuran (Amphibia). Chromosoma 21: 345-368.
Wickbom, T. (1945). Cytological studies on Dipnoi, Urodela, Anura and Emys. Hereditas 31: 241-346.
Wickbom, T. (1949). Further cytological studies on Anura and Urodela. Hereditas 35: 33-48.
Wolf, V., Ritter, H., Atkin, N.B. and Ohno, S. (1969). Polyploidization in the fish family Cyprinidae, order Cypriniformes. I. DNA-content and chromosome sets in various species of Cyprinidae. Humangenetik 7: 240-244.