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Review Change of Heterogametic Sex from Male to Female Chromosome Science 16: 3-9, 2013 Miura and Ogata 3 Review Change of heterogametic sex from male to female: Why so easy in the frog? Ikuo Miura and Mitsuaki Ogata Received: November 08, 2013 / Accepted: December 10, 2013 © 2013 by the Society of Chromosome Research Abstract Overview of sex determination in vertebrates Male and female heterogameties are two distinct Hills and Green (1998) conclude that the sex determination modes for genetic sex determination. In almost all mam- in urodelan and anuran amphibians is all genetic (GSD), mals including humans, male is the heterogametic sex, and the ancestral type of heterogametic sex is female while female is the heterogametic sex in all birds. The (ZW), which has been changed to male (XY) at least above fact has contributed to creating a long-stand- seven times during the phylogeny. They mapped the ing idea among the researchers that “Heterogametic type of heterogametic sex on the phylogenetic tree and sex once fixed is not changed so easily to the other”. deduced that female heterogamety occupies most of the A marginally evolved recent idea, however, proposes that ancestral lineages. Application of this approach to other heterogametic sex could be changed to each other far vertebrates leads to the inference of their ancestral types more frequently than we ever expected. In fact, we can of sex determination as follows; male heterogamety in fish well see many cases of transitions in lower vertebrates. (after cyclostomes) (cf. Devlin and Nagahama, 2002 and Among them, Japanese frog Rana rugosa is surprisingly Chapman et al., 2007) and temperature sex determination unique, because it has already experienced the change (TSD) in reptiles (cf. Gamble, 2010 and Crawford NG et al., of heterogametic sex from male to female three times, 2012). Within every large taxon moreover, other types of within its own lineage. The fourth change, moreover, sex determination co-exist, showing that transition between seems to be on the verge of appearance at the central XY and ZW or GSD and TSD occurred frequently during Japan stage. Why does heterogametic sex change so speciation in vertebrates (Fig. 1). In addition, when the frequently in the frog? We review the sex determining class diverged from the main lineage, a change of the sex systems and conduct a discussion on driving-force to determination system seems to have occurred as follows: change the heterogametic sex, particularly from a point from male to female hetereogamety in the lineage from fish of view of uniqueness of this situation in phylogeny of to amphibians, from female heterogamety to TSD in the the frog and topography of Japanese Islands involved in lineage from amphibians to reptiles, and from TSD to ZW the population dynamics. and XY, in the lineages from reptiles to birds and mammals (Fig. 1), respectively. Before completing the above theory, Key words: sex-determination, sex-chromosome, however, the sex determining mechanisms of Agnatha, XY, ZW, Rana rugosa Sarcopterigyii and Caecilia need to be identified. Anyway, the big questions are: why do they repeat the transition of sex determining mechanism, and what drives it? Sex determination and sex chromosomes of frog Rana rugosa Frog R. rugosa distributed in Japan has uniquely XX- XY and ZZ-ZW sex determining systems in the separated geographic populations. The Japanese populations are Ikuo Miura (*) classified into five major geographic groups based on the Institute for Amphibian Biology, Graduate School of Science, Hiro- shima University, Kagamiyama 1-3-1, Higashi-Hiroshima 739-8526, sex determination, sex chromosome differentiation, and Japan genetic information on allozyme and mitochondrial DNA Institute for Applied Ecology, University of Canberra, ACT 2601, (Fig. 2). The two groups of West-Japan and East-Japan are Australia of XX-XY type for sex determination with homomorphic e-mail: [email protected] sex chromosomes, while XY, ZW and Neo-ZW groups are of XX-XY, ZZ-ZW and ZZ-ZW types, respectively, with Mitsuaki Ogata heteromorphic sex chromosomes (Nishioka et al., 1993b, Laboratory of Zoo Biology, Preservation and Research Center, 1994; Miura 2007; Ogata et al., 2008). It is evident that the Kawaishukucho 155-1, Asahiku, Yokohama 241–0804, Japan heterogametic sex was changed from male to female in the 4 Multiple change of heterogametic sex in frog Figure 1. Overview of sex determination in vertebrates. Male and female heterogameties are indicated by blue and red lines, respectively. Temperature sex determination and unknown case are depicted by yellow and gray lines, respectively. The switching points of sex determin- ing mechanisms are indicated by black circles. Numbers indicate orders, of which names are listed beside. Figure 2. Five geographic groups of frog Rana rugosa in Japan. The four mountain ranges and one region to separate the five groups are delin- eated by black and gray thick lines: a, Kitakami-Oou-Echigo mountains; b, Ryouhaku-Hida-Kiso-Akashi-Hakone mountains; c, Ibuki-Suzuka moun- tains; d, Nosaka Mountain; e, T-OH line (a line running from Tottori to Hyogo through Okayama Prefecture). Figure 3. Karyotypes of Rana rugosa, a female from the ZW group and a male from the West-Japan group. Late replicated regions are stained deeply. The subtelocentric Z and metacentric W chromosomes are the 7th largest in the complement (boxed). Chromosome 7 of the West- Japan group is the same subtelocentric as Z chromosome and is probably autosome. Sex chromosomes of the West-Japan group are not yet cytogenetically identified. Miura and Ogata 5 Figure 4. Chromosomes 7 of the five groups in R. rugosa. The Y and Z chromosomes are both subtelocentric (ST) and homologous to the chro- mosome 7 of the West-Japan group, while both X and W chromosomes are metacentric (M) and share a common origin from the more subtelo- centric chromosome 7 (mST) of the East-Japan group through a pericen- tromeric inversion (round arrow). Figure 5. Maximum likelihood tree, based on the sequences of three genes, Sox3, SF-1 and ADP/ATP translocase, residing on chromosome 7. The subtelocentric chromosomes, Y, Z and chromosome 7 of West-Japan, belong to the same clade, while the metacentric chromosomes W and X belong to another clade, which is closer to the more subtelocentric chromosome 7 of the East-Japan group. Numbers at each node in- dicate ML/NJ/MP bootstrap supports (500 replicates, % in 500 and 500). Abbreviations are the same as in Fig. 4. two groups of ZW and Neo-ZW, because the heterogametic sex chromosomes, as follows: Z and Y chromosomes sex is male in the ancestral groups of this species, West- share the origin from chromosome 7 of the West-Japan Japan and East-Japan, as well as in most members of the population, while W and X chromosomes share the origin family Ranidae, which this species belongs to (Hillis and from chromosome 7 of the East-Japan population (Fig. 4) Green, 1998). So, this frog constitutes an ideal material for (Miura et al., 1998). Sequence data on another two sex- study on the mechanism of heterogametic sex change. linked genes of Sox3 and SF-1 again evidently support The unique features in the frog species are constitution the dual origin of the sex chromosomes (Fig. 5). In shape, and origins of the sex chromosomes. The diploid the Z, Y and chromosome 7 of the West-Japan are all chromosome number is 26, consisting of five large and same, subtelocentric, while the W and X are the same, eight small pairs (Fig. 3). Heteromorphic sex chromosomes metacentric, but differ from chromosome 7 of the East- of the three groups, XY, ZW and Neo-ZW, belong to the Japan, which is more subtelocentric (Fig. 4). Therefore, chromosome No. 7, the second largest in the small pairs in the process of W and X chromosome differentiation, (Figs. 3 and 4). Sequence of the sex linked gene ADP/ one pericentromeric inversion occurred on the original ATP translocase (AAT) presents a dual origin of the chromosome 7 (Figs. 4 and 5). The inversion is well proved 6 Multiple change of heterogametic sex in frog by analyses of banding and telomere FISH (Miura et al., cytoplasmic choice, drove the change of heterogametic sex 2009): one telomere signal is seen on the internal region of from male to female in the ZW group. the X/W chromosome long arms, which is a reminiscent of the terminal tip of the original chromosome 7 short arm. Genetic dual structure of the frog species and topography of Japanese Islands Hybridization and sex ratio skewing The existence of two separated, ancestral populations Dual origin of the X/Y and Z/W sex chromosomes of West-Japan and East-Japan must be an original cause necessarily requires occurrence of hybridization at to induce change of the heterogametic sex in the frog. population level in the past, that is, the XY and ZW Allozyme and mitochondrial DNA data demonstrate that groups are found to share the same origin at hybridization the two ancestral populations are genetically somewhat between the West-Japan and East-Japan populations (Fig. distant (Nishioka et al., 1993a; Ogata et al., 2002). 6) (Miura et al., 1998; Ogata et al., 2003). Different shaped Incompatibility of the nuclear genome with cytoplasmic chromosomes 7 were met and paired in the same single one, therefore, probably disturbed the pre-existing sex cell, and chromosome 7 from the East-Japan underwent determination mechanisms and induced sex ratio skewing inversion and evolved to X chromosome in one and to W in the hybrids and backcrossed offspring (Ogata et al., chromosome on the other. The counterpart chromosome 2003). The sequence data also reveals the phylogenetic 7 from the West-Japan kept the original shape and evolved history of the frog, as follows: the ancestral population of to Y and Z chromosomes.
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