Identification of ancestral sex chromosomes in the frog Glandirana rugosa bearing XX-XY and ZZ-ZW sex-determining systems.
heterogametic sex
homomorphy
turnover
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
07 2022
07 2022
Historique:
revised:
03
05
2022
received:
16
12
2021
accepted:
24
05
2022
pubmed:
13
6
2022
medline:
14
7
2022
entrez:
12
6
2022
Statut:
ppublish
Résumé
Sex chromosomes constantly exist in a dynamic state of evolution: rapid turnover and change of heterogametic sex during homomorphic state, and often stepping out to a heteromorphic state followed by chromosomal decaying. However, the forces driving these different trajectories of sex chromosome evolution are still unclear. The Japanese frog Glandirana rugosa is one taxon well suited to the study on these driving forces. The species has two different heteromorphic sex chromosome systems, XX-XY and ZZ-ZW, which are separated in different geographic populations. Both XX-XY and ZZ-ZW sex chromosomes are represented by chromosome 7 (2n = 26). Phylogenetically, these two systems arose via hybridization between two ancestral lineages of West Japan and East Japan populations, of which sex chromosomes are homomorphic in both sexes and to date have not yet been identified. Identification of the sex chromosomes will give us important insight into the mechanisms of sex chromosome evolution in this species. Here, we used a high-throughput genomic approach to identify the homomorphic XX-XY sex chromosomes in both ancestral populations. Sex-linked DNA markers of West Japan were aligned to chromosome 1, whereas those of East Japan were aligned to chromosome 3. These results reveal that at least two turnovers across three different sex chromosomes 1, 3 and 7 occurred during evolution of this species. This finding raises the possibility that cohabitation of the two different sex chromosomes from ancestral lineages induced turnover to another new one in their hybrids, involving transition of heterogametic sex and evolution from homomorphy to heteromorphy.
Substances chimiques
Genetic Markers
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3859-3870Informations de copyright
© 2022 John Wiley & Sons Ltd.
Références
Bachtrog, D., Mank, J. E., Peichel, C. L., Kirkpatrick, M., Otto, S. P., Ashman, T. L., Hahn, M. W., Kitano, J., Mayrose, I., Ming, R., Perrin, N., Ross, L., Valenzuela, N., & Vamosi, J. C. (2014). Sex determination: Why so many ways of doing it? PLOS Biology, 12(7), e1001899.
Berger, I., Ryback, M., & Hotz, H. (1994). Artificial fertilization of water frogs. Amphibia-Reptilia, 15, 408-413.
Brelsford, A., Dufresnes, C., & Perrin, N. (2016). Trans-species variation in Dmrt1 is associated with sex determination in four European tree-frog species. Evolution, 70(4), 840-847. https://doi.org/10.1111/evo.12891
Charlesworth, D., Charlesworth, B., & Marais, G. (2005). Steps in the evolution of heteromorphic sex chromosomes. Heredity, 95(2), 118-128. https://doi.org/10.1038/sj.hdy.6800697
Denton, R. D., Kudra, R. S., Malcom, J. W., Preez, L. D., & Malone, J. H. (2018). The African bullfrog (Pyxicephalus adspersus) genome unites the two ancestral ingredients for making vertebrate sex chromosomes. bioRxiv, 1-25. https://doi.org/10.1101/329847
Devlin, R. H., & Nagahama, Y. (2002). Sex determination and sex differentiation in fish: Overview of genetic, physiological, and environmental influences. Aquaculture, 208, 191-364. https://doi.org/10.1016/S0044-8486(02)00057-1
Dufresnes, C., Borzée, A., Horn, A., Stöck, M., Ostini, M., Sermier, R., Wassef, J., Litvinchuck, S. N., Kosch, T. A., Waldman, B., Jang, Y., Brelsford, A., & Perrin, N. (2015). Sex-chromosome homomorphy in palearctic tree frogs results from both turnovers and X-Y recombination. Molecular Biology and Evolution, 32, 2328-2337. https://doi.org/10.1093/molbev/msv113
Ezaz, T., Sarre, S., O'Meally, D., Graves, J. M., & Georges, A. (2009). Sex chromosome evolution in lizards: Independent origins and rapid transitions. Cytogenetic and Genome Research, 127, 249-260.
Furman, B. L. S., Metzger, D. C. H., Darolti, I., Wright, A. E., Sandkam, B. A., Almeida, P., Shu, J. J., & Mank, J. E. (2020). Sex chromosome evolution: So many exceptions to the rules. Genome Biology and Evolution, 12(6), 750-763. https://doi.org/10.1093/gbe/evaa081
Gamble, T., Coryell, J., Ezaz, T., Lynch, J., Scantlebury, D. P., & Zarkower, D. (2015). Restriction site-associated DNA sequencing (RAD-seq) reveals an extraordinary number of transitions among gecko sex-determining systems. Molecular Biology and Evolution, 32, 1296-1309.
Gamble, T., Castoe, T. A., Nielsen, S. V., Banks, J. L., Card, D. C., Schield, D. R., Schuett, G. W., & Booth, W. (2017). The discovery of XY sex chromosomes in a Boa and Python. Current Biology, 27(14), 2148-2153.e4. https://doi.org/10.1016/j.cub.2017.06.010
Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q., Chen, Z., Mauceli, E., Hacohen, N., Gnirke, A., Rhind, N., di Palma, F., Birren, B. W., Nusbaum, C., Lindblad-Toh, K., … Regev, A. (2011). Full-length transcriptome assembly from RNA-seq data without a reference genome. Nature Biotechnology, 29, 644-652.
Graves, J. A. M. (2008). Weird animal genomes and the evolution of vertebrate sex and sex chromosome. Annual Review of Genetics, 42, 565-586.
Gruber, B., Unmack, P. J., Berry, O. F., & Georges, A. (2018). Dartr: An r package to facilitate analysis of SNP data generated from reduced representation genome sequencing. Molecular Ecology Resources, 18, 691-699.
Heini, M., Merilä, J., & Shikano, T. (2019). The evolution of sex determination associated with a chromosomal inversion. Nature Communications, 10(1), 145. https://doi.org/10.1038/s41467-018-08014-y
Jeffries, D. L., Lavanchy, G., Sermier, R., Sredl, M. J., Miura, I., Borzée, A., Barrow, L. N., Canestrelli, D., Crochet, P. A., Dufresnes, C., Fu, J., Ma, W. J., Garcia, C. M., Ghali, K., Nicieza, A. G., O'Donnell, R. P., Rodrigues, N., Romano, A., Martínez-Solano, I., … Perrin, A. (2018). A rapid rate of sex-chromosome turnover and non-random transitions in true frogs. Nature communications, 9, 4088. https://doi.org/10.1038/s41467-018-06517-2
Kajitani, R., Yoshimura, D., Okuno, M., Minakuchi, Y., Kagoshima, H., Fujiyama, A., Kubokawa, K., Kohara, Y., Toyoda, A., & Itoh, T. (2019). Platanus-allee is a de novo haplotype assembler enabling a comprehensive access to divergent heterozygous regions. Nature Communications, 10(1), 1702. https://doi.org/10.1038/s41467-019-09575-2
Karimi, K., Fortriede, J. D., Lotay, V. S., Burns, K. A., Wang, D. Z., Fisher, M. E., Pells, T. J., James-Zorn, C., Wang, Y., Ponferrada, V. G., & Chu, S. (2017). Xenbase: A genomic, epigenomic and transcriptomic model organism database. Nucleic Acids Research (NAR), 46(D1), D861-D868. https://doi.org/10.1093/nar/gkx936
Kashiwagi, K. (1993). Gynogenetic diploids in Rana rugosa and their offspring. Scientific Report of the Laboratory for Amphibian Biology, 12, 1-22.
Katsura, Y., Ikemura, T., Kajitani, R., Toyoda, A., Itoh, T., Ogata, M., Miura, I., Wada, K., Wada, Y., & Satta, Y. (2021). Comparative genomics of Glandirana rugosa using unsupervised AI reveals a high CG frequency. Life Science Alliance, 4(5), e202000905. https://doi.org/10.26508/lsa.202000905
Kikuchi, K., & Hamaguchi, S. (2013). Novel sex-determining genes in fish and sex chromosome evolution. Developmental Dynamics, 242(4), 339-353. https://doi.org/10.1002/dvdy.23927
Kilian, A., Wenzl, P., Huttner, E., Carling, J., Xia, L., Blois, H., Caig, V., Heller-Uszynska, K., Jaccoud, D., & Hopper, C. (2012). Diversity arrays technology: A generic genome profiling technology on open platforms. Data production and analysis in population genomics: methods and protocols, 888, 67-89.
Kostmann, A., Kratochvil, L., & Rovatsos, M. (2021). Poorly differentiated XX/XY sex chromosomes are widely shared across skink radiation. Proceedings of the Royal Society B, 288(1943), 20202139. https://doi.org/10.1098/rspb.2020.2139
Koyama, T., Nakamoto, M., Morishima, K., Yamashita, R., Yamashita, T., Sasaki, K., Kuruma, Y., Mizuno, N., Suzuki, M., Okada, Y., & Ieda, R. (2019). A SNP in a steroidogenic enzyme is associated with phenotypic sex in Seriola fishes. Current Biology, 29(11), 1901-1909. https://doi.org/10.1016/j.cub.2019.04.069
Kozielska, M., Weissing, F. J., Beukeboom, L. W., & Pen, I. (2010). Segregation distortion and the evolution of sex-determining mechanisms. Heredity, 104, 100-112.
Kratochvíl, L., Stöck, M., Rovatsos, M., Bullejos, M., Herpin, A., Jeffries, D. L., Peichel, C. L., Perrin, N., Valenzuela, N., & Pokorná, M. J. (2021). Expanding the classical paradigm: What we have learnt from vertebrates about sex chromosome evolution. Philosophical Transactions of the Royal Society B: Biological Sciences, 376(1833), 20200097. https://doi.org/10.1098/rstb.2020.0097
Kuwana, C., Fujita, H., Tagami, M., Matsuo, T., & Miura, I. (2021). Evolution of sex-chromosome heteromorphy in geographic populations of the Japanese Tago's brown frog complex. Cytogenetic and Genome Research, 161(1-2), 23-31. https://doi.org/10.1159/000512964
Mank, J. E., Promislow, D. E. L., & Avise, J. C. (2006). Evolution of alternative sex-determining mechanisms in teleost fishes. Biological Journal of the Linnean Society, 87, 83-93. https://doi.org/10.1111/j.1095-8312.2006.00558.x
Mawaribuchi, S., Ito, M., Ogata, M., Oota, H., Katsumura, T., Takamatsu, N., & Miura, I. (2016). Meiotic recombination counteracts male-biased mutation (male-driven evolution). Proceedings of the Royal Society B: Biological Sciences, 283(1823), 20152691. https://doi.org/10.1098/rspb.2015.2691
Miura, I. (1994). Sex chromosome differentiation in the Japanese brown frog, Rana japonica I. sex-related heteromorphism of the distribution pattern of constitutive heterochromatin in chromosome no.4 of the Wakuya population. Zoological Science, 11, 797-806.
Miura, I. (1995). The late replication banding patterns of chromosomes are highly conserved in the genera Rana, Hyla, and Bufo. Chromosoma, 103, 567-574.
Miura, I. (2007). An evolutionary witness: The frog Rana rugosa underwent change of heterogametic sex from XY male to ZW female. Sexual Development, 1, 323-331.
Miura, I. (2017). Sex determination and sex chromosomes in amphibia. Sexual Development, 11, 298-306. https://doi.org/10.1159/000485270
Miura, I., Nishioka, M., Borkin, L. K., & Wu, Z. (1995). The origin of the brown frogs with 2n = 24 chromosomes. Experientia, 51, 179-188.
Miura, I., & Ogata, M. (2013). Change of heterogametic sex from male to female: Why so easy in the frog? Chromosome Science, 16, 3-9.
Miura, I., Ohtani, H., Hanada, H., Ichikawa, Y., Kashiwagi, A., & Nakamura, M. (1997). Evidence for two successive pericentric inversions in sex lampbrush chromosomes of Rana rugosa (Anura: Ranidae). Chromosoma, 106, 178-182.
Miura, I., Ohtani, H., Nakamura, M., Ichikawa, Y., & Saitoh, K. (1998). The origin and differentiation of the heteromorphic sex chromosomes Z, W, X and Y of the frog Rana rugosa, inferred from the sequences of a sex-linked gene, ADP/ATP translocase. Moleclular Biology and Evolution, 15, 1612-1619.
Miura, I., Shams, F., Lin, S.-M., Cioffi, M. B., Liehr, T., Al-Rikabi, A., Kuwana, C., Srikulnath, K., Higaki, Y., & Ezaz, T. (2021). Evolution of a multiple sex-chromosome system by three-sequential translocations among potential sex-chromosomes in the Taiwanese frog Odorrana swinhoana. Cells, 10(3), 661. https://doi.org/10.3390/cells10030661
Nagai, Y., Doi, T., Ito, K., Yuasa, Y., Fujitani, T., Naito, J., Ogata, M., & Miura, I. (2018). The distributions and boundary of two distinct, local forms of Japanese pond frog, Pelophylax porosus brevipodus, inferred from sequences of mitochondrial DNA. Frontier in Genetics, 9, 79. https://doi.org/10.3389/fgene.2018.00079
Nishioka, M., Hanada, H., Miura, I., & Ryuzaki, M. (1994). Four kinds of sex chromosomes in Rana rugosa. Scientific Report of the Laboratory for Amphibian Biology, Hiroshima University, 13, 1-34.
Nishioka, M., Miura, I., & Saitoh, K. (1993). Sex chromosomes of Rana rugosa with special reference to local differences in sex determining mechanism. Scientific Report of the Laboratory for Amphibian Biology, Hiroshima University, 12, 55-81.
Nishioka, M., & Sumida, M. (1994). The position of sex-determining genes in the chromosomes of Rana nigromaculata and Rana brevipoda. Scientific Report of the Laboratory for Amphibian Biology, Hiroshima University, 13, 51-97.
Ogata, M., Lambert, M., Ezaz, T., & Miura, I. (2018). Reconstruction of female heterogamety from admixture of XX-XY and ZZ-ZW sex-chromosome systems within a frog species. Molecluar Ecology, 20, 4078-4089.
Ogata, M., Lee, J. Y., Kim, S. K., Ohtani, H., Sekiya, K., Igarashi, T., Hasegawa, Y., Ichikawa, Y., & Miura, I. (2002). The prototype of sex chromosomes found in Korean populations of Rana rugosa. Cytogenetic and Genome Research, 99(1-4), 185-193.
Ogata, M., Ohtani, H., Igarashi, T., Hasegawa, Y., Ichikawa, Y., & Miura, I. (2003). Change of the heterogametic sex from male to female in the frog. Genetics, 164(2), 613-620.
Ogata, M., Suzuki, K., Yuasa, Y., & Miura, I. (2021). Sex-chromosome evolution from a heteromorphic to a homomorphic system by inter-population hybridization in a frog. Proceedings of the Royal Society B: Biological Sciences, 376(1833), 20200105. https://doi.org/10.1098/rstb.2020.0105
Ohno, S. (1967). Sex chromosomes and sex-linked genes. Springer-Verlag.
Ohtani, H., Miura, I., Kondo, Y., & Uchibori, M. (1997). Amphidiploidy recovers the viability of hybrids between the European and far eastern water frogs. Journal of Experimental Zoology, 279, 113-117.
O'Meally, D., Ezaz, T., Georges, A., Sarre, S. D., & Graves, J. A. M. (2012). Are some chromosomes particularly good at sex? Insights from amniotes. Chromosome Research, 20, 7-19.
R Core Team. (2017). R: A language and environment for statistical computing, v. 3.3. 1. R Foundation for Statistical Computing 2016.
Ren, R., Ray, R., Li, P., Xu, J., Zhang, M., Liu, G., Yao, X., Kilian, A., & Yang, X. (2015). Construction of a high-density DArTseq SNP-based genetic map and identification of genomic regions with segregation distortion in a genetic population derived from a cross between feral and cultivated-type watermelon. Molecular Genetics and Genomics, 290, 1457-1470.
Rodrigues, N., Studer, T., Dufresnes, C., Ma, W. J., Veltsos, P., & Perrin, N. (2017). Dmrt1 polymorphism and sex-chromosome differentiation in Rana temporaria. Molecular Ecology, 26(19), 4897-4905. https://doi.org/10.1111/mec.14222
Ryuzaki, M., Hanada, H., Okumoto, H., Takizawa, N., & Nishioka, M. (1999). Evidence for heteromorphic sex chromosomes in males of Rana tagoi and Rana sakuraii in Nishitama district of Tokyo (Anura: Ranidae). Chromosome Research, 7, 31-42.
Saunders, P. A., Neuenschwander, S., & Perrin, N. (2018). Sex chromosome turnovers and genetic drift: A simulation study. Journal of Evolutionary Biology, 31(9), 1413-1419. https://doi.org/10.1111/jeb.13336
Stöck, M., Horn, A., Grossen, C., Lindtke, D., Sermier, R., Betto-Colliard, C., Dufresnes, C., Bonjour, E., Dumas, Z., Luquet, E., Maddalena, T., Sousa, H. C., Martinez-Solano, I., & Perrin, N. (2011). Ever-young sex chromosomes in European tree frogs. PLoS Biology, 9(5), e1001062. https://doi.org/10.1371/journal.pbio.1001062
Sumida, M. (1981). Studies on Ichinoseki population of Rana japonica. Scientific Report of the Laboratory for Amphibian Biology, Hiroshima University, 5, 1-46.
Sumida, M., & Nishioka, M. (1994). Geographic variability of sex-linked loci in the Japanese brown frog, Rana japonica. Scientific Report of the Laboratory for Amphibian Biology, Hiroshima University, 13, 173-195.
Veller, C., Muralidhar, P., ConsTable, G. W. A., & Nowak, M. A. (2017). Drift-induced selection between male and female heterogamety. Genetics, 207(2), 711-727. https://doi.org/10.1534/genetics.117.300151