• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. Jun 2003; 164(2): 613–620.
PMCID: PMC1462578

Change of the heterogametic sex from male to female in the frog.


Two different types of sex chromosomes, XX/XY and ZZ/ZW, exist in the Japanese frog Rana rugosa. They are separated in two local forms that share a common origin in hybridization between the other two forms (West Japan and Kanto) with male heterogametic sex determination and homomorphic sex chromosomes. In this study, to find out how the different types of sex chromosomes differentiated, particularly the evolutionary reason for the heterogametic sex change from male to female, we performed artificial crossings between the West Japan and Kanto forms and mitochondrial 12S rRNA gene sequence analysis. The crossing results showed male bias using mother frogs with West Japan cytoplasm and female bias using those with Kanto cytoplasm. The mitochondrial genes of ZZ/ZW and XX/XY forms, respectively, were similar in sequence to those of the West Japan and Kanto forms. These results suggest that in the primary ZZ/ZW form, the West Japan strain was maternal and thus male bias was caused by the introgression of the Kanto strain while in the primary XX/XY form and vice versa. We therefore hypothesize that sex ratio bias according to the maternal origin of the hybrid population was a trigger for the sex chromosome differentiation and the change of heterogametic sex.

Full Text

The Full Text of this article is available as a PDF (238K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Huang B, Wang S, Ning Y, Lamb AN, Bartley J. Autosomal XX sex reversal caused by duplication of SOX9. Am J Med Genet. 1999 Dec 3;87(4):349–353. [PubMed]
  • Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980 Dec;16(2):111–120. [PubMed]
  • Miura I, Ohtani H, Kashiwagi A, Hanada H, Nakamura M. Structural differences between XX and ZW sex lampbrush chromosomes in Rana rugosa females (Anura: Ranidae). Chromosoma. 1996 Oct;105(4):237–241. [PubMed]
  • Miura I, Ohtani H, Hanada H, Ichikawa Y, Kashiwagi A, Nakamura M. Evidence for two successive pericentric inversions in sex lampbrush chromosomes of Rana rugosa (Anura: Ranidae). Chromosoma. 1997 Aug;106(3):178–182. [PubMed]
  • Miura I, Ohtani H, Nakamura M, Ichikawa Y, Saitoh K. The origin and differentiation of the heteromorphic sex chromosomes Z, W, X, and Y in the frog Rana rugosa, inferred from the sequences of a sex-linked gene, ADP/ATP translocase. Mol Biol Evol. 1998 Dec;15(12):1612–1619. [PubMed]
  • Nakajima T, Takase M, Miura I, Nakamura M. Two isoforms of FTZ-F1 messenger RNA: molecular cloning and their expression in the frog testis. Gene. 2000 May 2;248(1-2):203–212. [PubMed]
  • Ohtani H, Miura I, Kondo Y, Uchibori M. Amphidiploidy recovers the viability of hybrids of European and east Asian water frogs. J Exp Zool. 1997 Oct 1;279(2):113–117. [PubMed]
  • Ohtani H, Miura I, Hanada H, Ichikawa Y. Alteration of the sex determining system resulting from structural change of the sex chromosomes in the frog Rana rugosa. J Exp Zool. 2000 Feb 15;286(3):313–319. [PubMed]
  • Bishop CE, Whitworth DJ, Qin Y, Agoulnik AI, Agoulnik IU, Harrison WR, Behringer RR, Overbeek PA. A transgenic insertion upstream of sox9 is associated with dominant XX sex reversal in the mouse. Nat Genet. 2000 Dec;26(4):490–494. [PubMed]
  • O'Neill M, Binder M, Smith C, Andrews J, Reed K, Smith M, Millar C, Lambert D, Sinclair A. ASW: a gene with conserved avian W-linkage and female specific expression in chick embryonic gonad. Dev Genes Evol. 2000 May;210(5):243–249. [PubMed]
  • Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. [PubMed]
  • Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol. 1981;17(6):368–376. [PubMed]
  • Sakisaka Y, Yahara T, Miura I, Kasuya E. Maternal control of sex ratio in Rana rugosa: evidence from DNA sexing. Mol Ecol. 2000 Nov;9(11):1711–1715. [PubMed]
  • Sumida M, Ogata M, Kaneda H, Yonekawa H. Evolutionary relationships among Japanese pond frogs inferred from mitochondrial DNA sequences of cytochrome b and 12S ribosomal RNA genes. Genes Genet Syst. 1998 Apr;73(2):121–133. [PubMed]
  • Graves JA. Interactions between SRY and SOX genes in mammalian sex determination. Bioessays. 1998 Mar;20(3):264–269. [PubMed]
  • Yoneyama Y. [The nucleotide sequences of the heavy and light strand replication origins of the Rana catesbeiana mitochondrial genome]. Nihon Ika Daigaku Zasshi. 1987 Aug;54(4):429–440. [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America


Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...


Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...