Organisms have evolved various mechanisms to cope with the differences in the gene copy numbers between sexes caused by degeneration of Y and W sex chromosomes. Complete dosage compensation or at least expression balance between sexes has been reported predominantly in XX/XY systems, but rarely in ZZ/ZW systems. However, this often-reported pattern is based on comparisons of lineages where sex chromosomes evolved from nonhomologous genomic regions, potentially differing in sensitivity to differences in gene copy numbers. Here we document that two reptilian lineages (XX/XY iguanas and ZZ/ZW softshell turtles), which independently co-opted the same ancestral genomic region for the function of sex chromosomes, evolved different gene dose regulatory mechanisms. The independent co-option of the same genomic region for the role of sex chromosomes as in the iguanas and the softshell turtles offers great opportunity for testing evolutionary scenarios on sex chromosome evolution under the explicit control of the genomic background and gene identity. We show that the parallel loss of functional genes from the Y chromosome of the green anole and the W chromosome of the Florida softshell turtle led to different dosage compensation mechanisms. Our approach controlling for genetic background thus does not support that the variability in the regulation of gene dose differences is a consequence of ancestral autosomal gene content.

Department of Ecology Faculty of Science Charles University Prague Czech Republic

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Acosta, A., Suárez-Varón, G., Rodríguez-Miranda, L. A., Lira-Noriega, A., Aguilar-Gómez, D., Gutiérrez-Mariscal, M., Hernández-Gallegos, O., Méndez-de-la-Cruz, F., & Cortez, D. (2019). Corytophanids replaced the pleurodont XY system with a new pair of XY chromosomes. Genome Biology and Evolution, 11, 2666-2677.

Alföldi, J., Di Palma, F., Grabherr, M., Williams, C., Kong, L., Mauceli, E., Russell, P., Lowe, C. B., Glor, R. E., Jaffe, J. D., Ray, D. A., Boissinot, S., Shedlock, A. M., Botka, C., Castoe, T. A., Colbourne, J. K., Fujita, M. K., Moreno, R. G., ten Hallers, B. F., … Lindblad-Toh, K. (2011). The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature, 477, 587-591.

Altmanová, M., Rovatsos, M., Johnson Pokorná, M., Veselý, M., Wagner, F., & Kratochvíl, L. (2018). All iguana families with the exception of basilisks share sex chromosomes. Zoology, 126, 98-102.

Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403-410.

Andrews, S. (2010). FastQC: A quality control tool for high throughput sequence data. Retrieved from http://www.bioinformatics.babraham.ac.uk.

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., … The Tree of Sex Consortium (2014). Sex determination: Why so many ways of doing it? PLoS Biology, 12, e1001899.

Baker, B. S., & Belote, J. M. (1983). Sex determination and dosage compensation in Drosophila melanogaster. Annual Review of Genetics, 17, 345-393.

Birchler, J. A. (2014). Facts and artifacts in studies of gene expression in aneuploids and sex chromosomes. Chromosoma, 123, 459-469.

Birchler, J. A., Riddle, N. C., Auger, D. L., & Veitia, R. A. (2005). Dosage balance in gene regulation: biological implications. Trends in Genetics, 21, 219-226.

Bista, B., & Valenzuela, N. (2020). Turtle insights into the evolution of the reptilian karyotype and the genomic architecture of sex determination. Genes, 11, 416.

Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114-2120.

Brockdorff, T., & Turner, B. M. (2015). Dosage compensation in mammals. Cold Spring Harbour Perspectives in Biology, 7, a019406.

Chan, E. T., Quon, G. T., Chua, G., Babak, T., Trochesset, M., Zirngibl, R. A., Aubin, J., Ratcliffe, M. J., Wilde, A., Brudno, M., Morris, Q. D., & Hughes, T. R. (2009). Conservation of core gene expression in vertebrate tissues. Journal of Biology, 16, 33.

Charlesworth, D., Charlesworth, B., & Marais, G. (2005). Steps in the evolution of heteromorphic sex chromosomes. Heredity, 95, 118-128.

Clinton, M. (1998). Sex determination and gonadal development: A bird's eye view. Journal of Experimental Zoology, 281, 457-465.

Crowson, D., Barrett, S. C. H., & Wright, S. I. (2017). Purifying and positive selection influence patterns of gene loss and gene expression in the evolution of a plant sex chromosome system. Molecular Biology and Evolution, 34, 1140-1154.

Deng, X., Hiatt, J. B., Nguyen, D. K., Ercan, S., Sturgill, D., Hillier, L. D. W., Schlesinger, F., Davis, C. A., Reinke, V. J., Gingeras, T. R., Shendure, J., Waterston, R. H., Oliver, B., Lieb, J. D., & Disteche, C. M. (2011). Evidence for compensatory upregulation of expressed X-linked genes in mammals, Caenorhabditis elegans and Drosophila melanogaster. Nature Genetics, 43, 1179-1185.

Deutschbauer, A. M., Jaramillo, D. F., Proctor, M., Kumm, J., Hillenmeyer, M. E., Davis, R. W., Nislow, C., & Giaever, G. (2005). Mechanisms of haploinsufficiency revealed by genome-wide profiling in yeast. Genetics, 169, 1915-1925.

Dürrbaum, M., & Storchová, Z. (2016). Effects of aneuploidy on gene expression: implications for cancer. FEBS Journal, 283, 791-802.

Ellegren, H. (2002). Dosage compensation: Do birds do it as well? Trends in Genetics, 18, 25-28.

Ewels, P., Magnusson, M., Lundin, S., & Käller, M. (2016). MultiQC: Summarize analysis results for multiple tools and samples in a single report. Bioinformatics, 32, 3047-3048.

Fruchard, C., Badouin, H., Latrasse, D., Devani, R. S., Muyle, A., Rhoné, B., Renner, S. S., Banerjee, A. K., Bendahmane, A., & Marais, G. A. B. (2020). Evidence for dosage compensation in Coccinia grandis, a plant with a highly heteromorphic XY System. Genes, 11, 787.

Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., & Regev, A. (2011). Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology, 29, 644-652.

Gu, L., & Walters, J. R. (2017). Evolution of sex chromosome dosage compensation in animals: A beautiful theory, undermined by facts and bedeviled by details. Genome Biology and Evolution, 9, 2461-2476.

Hutchins, E. D., Markov, G. J., Eckalbar, W. L., George, R. M., King, J. M., Tokuyama, M. A., Geiger, L. A., Emmert, N., Ammar, M. J., Allen, A. N., Siniard, A. L., Corneveaux, J. J., Fisher, R. E., Wade, J., DeNardo, D. F., Rawls, J. A., Huentelman, M. J., Wilson-Rawls, J., & Kusumi, K. (2014). Transcriptomic analysis of tail regeneration in the lizard Anolis carolinensis reveals activation of conserved vertebrate developmental and repair mechanisms. PLoS One, 9, e105004.

Huylmans, A. K., Macon, A., & Vicoso, B. (2017). Global dosage compensation is ubiquitous in Lepidoptera, but counteracted by the masculinization of the Z chromosome. Molecular Biology and Evolution, 34, 2637-2649.

Huylmans, A. K., Toups, M. A., Macon, A., Gammerdinger, W. J., & Vicoso, B. (2019). Sex-biased gene expression and dosage compensation on the Artemia franciscana Z-Chromosome. Genome Biology and Evolution, 11, 1033-1044.

Johnson Pokorná, M., & Kratochvíl, L. (2016). What was the ancestral sex-determining mechanism in amniote vertebrates? Biological Reviews, 91, 1-12.

Kawagoshi, T., Uno, Y., Matsubara, K., Matsuda, Y., & Nishida, C. (2009). The ZW micro-sex chromosomes of the Chinese soft-shelled turtle (Pelodiscus sinensis, Trionychidae, Testudines) have the same origin as chicken chromosome 15. Cytogenetic and Genome Research, 125, 125-131.

Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., & Drummond, A. (2012). Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647-1649.

Kratochvíl, L., Gamble, T., & Rovatsos, M. (2021). Sex chromosome evolution among amniotes: Is the origin of sex chromosomes non-random?. Philosophical Transactions of the Royal Society B: Biological Sciences, in press.

Mank, J. E. (2009). The W, X, Y and Z of sex-chromosome dosage compensation. Trends in Genetics, 25, 226-233.

Mank, J. E. (2013). Sex chromosome dosage compensation: definitely not for everyone. Trends in Genetics, 29, 677-683.

Mank, J. E., Vicoso, B., Berlin, S., & Charlesworth, B. (2010). Effective population size and the faster-X effect: empirical results and their interpretation. Evolution, 64, 663-674.

Marin, R., Cortez, D., Lamanna, F., Pradeepa, M. M., Leushkin, E., Julien, P., & Kaessmann, H. (2017). Convergent origination of a Drosophila-like dosage compensation mechanism in a reptile lineage. Genome Research, 27, 1974-1987.

Martin, H., Carpentier, F., Gallina, S., Godé, C., Schmitt, E., Muyle, A., Marais, G. A. B., & Touzet, P. (2019). Evolution of young sex chromosomes in two dioecious sister plant species with distinct sex determination systems. Genome Biology and Evolution, 11, 350-361.

Morrill, S. A., & Amon, A. (2019). Why haploinsufficiency persists. Proceedings of the National Academy of Sciences, 116, 11866-11871.

Muller, H. J. (1918). Genetic variability, twin hybrids and constant hybrids, in a case of balanced lethal factors. Genetics, 3, 422-499.

Mullon, C., Wright, A. E., Reuter, M., Pomiankowski, A., & Mank, J. E. (2015). Evolution of dosage compensation under sexual selection differs between X and Z chromosomes. Nature Communications, 6, 7720.

Muyle, A., Zemp, N., Deschamps, C., Mousset, S., Widmer, A., & Marais, G. A. B. (2012). Rapid de novo evolution of X chromosome dosage compensation in Silene latifolia, a plant with young sex chromosomes. PLoS Biology, 10, e1001308.

Naqvi, S., Bellott, D. W., Lin, K. S., & Page, D. C. (2018). Conserved microRNA targeting reveals preexisting gene dosage sensitivities that shaped amniote sex chromosome evolution. Genome Research, 28, 474-483.

Naurin, S., Hasselquist, D., Bensch, S., & Hansson, B. (2012). Sex-biased gene expression on the avian Z chromosome: highly expressed genes show higher male-biased expression. PLoS One, 7, e46854.

Nielsen, S. V., Guzmán-Méndez, I. A., Gamble, T., Blumer, M., Pinto, B. J., Kratochvíl, L., & Rovatsos, M. (2019). Escaping the evolutionary trap? Sex chromosome turnover in basilisks and related lizards (Corytophanidae: Squamata). Biology Letters, 15, 20190498.

O'Connor, R. E., Romanov, M. N., Kiazim, L. G., Barrett, P. M., Farré, M., Damas, J., Ferguson-Smith, M., Valenzuela, N., Larkin, D. M., & Griffin, D. K. (2018). Reconstruction of the diapsid ancestral genome permits chromosome evolution tracing in avian and non-avian dinosaurs. Nature Communications, 9, 1883.

Ohno, S. (1967). Sex chromosomes and sex-linked genes. Springer-Verlag.

Pan, Q., Anderson, J., Bertho, S., Herpin, A., Wilson, C., Postlethwait, J. H., & Guiguen, Y. (2016). Vertebrate sex-determining genes play musical chairs. Comptes Rendus Biologies, 339, 258-262.

Papadopulos, A. S., Chester, M., Ridout, K., & Filatov, D. A. (2015). Rapid Y degeneration and dosage compensation in plant sex chromosomes. Proceedings of the National Academy of Sciences, 112, 13021-13026.

Pessia, E., Engelstädter, J., & Marais, G. A. (2014). The evolution of X chromosome inactivation in mammals: the demise of Ohno's hypothesis? Cellular and Molecular Life Sciences, 71, 1383-1394.

Pessia, E., Makino, T., Bailly-Bechet, M., McLysaght, A., & Marais, G. A. (2012). Mammalian X chromosome inactivation evolved as a dosage-compensation mechanism for dosage-sensitive genes on the X chromosome. Proceedings of the National Academy of Sciences of the United Staes of America, 109, 5346-5351.

Picard, M. A. L., Cosseau, C., Ferré, S., Quack, T., Grevelding, C. G., Couté, Y., & Vicoso, B. (2018). Evolution of gene dosage on the Z-chromosome of schistosome parasites. eLife, 7, e35684.

Picard, M. A. L., Vicoso, B., Roquis, D., Bulla, I., Augusto, R. C., Arancibia, N., Grunau, C., Boissier, J., & Cosseau, C. (2019). Dosage compensation throughout the Schistosoma mansoni lifecycle: specific chromatin landscape of the Z chromosome. Genome Biology and Evolution, 11, 1909-1922.

Prentout, D., Razumova, O., Rhoné, B., Badouin, H., Henri, H., Feng, C., Käfer, J., Karlov, G., & Marais, G. A. (2020). An efficient RNA-seq-based segregation analysis identifies the sex chromosomes of Cannabis sativa. Genome Research, 30, 164-172.

Rice, A. M., & McLysaght, A. (2017). Dosage-sensitive genes in evolution and disease. BMC Biology, 15, 78.

Rovatsos, M., Altmanová, M., Johnson Pokorná, M., & Kratochvíl, L. (2014). Novel X-linked genes revealed by quantitative polymerase chain reaction in the green anole, Anolis carolinensis. G3-Genes Genome Genetics, 4, 2107-2113.

Rovatsos, M., Augstenová, B., Altmanová, M., Sloboda, M., Kodym, P., & Kratochvíl, L. (2018). Triploid colubrid snake provides insight into the mechanism of sex determination in advanced snakes. Sexual Development, 12, 251-255.

Rovatsos, M., Gamble, T., Nielsen, S. V., Georges, A., Ezaz, T., & Kratochvíl, L. (2021). Do male and female heterogamety really differ in expression regulation? Lack of global dosage balance in pygopodid geckos. Philosophical Transactions of the Royal Society B: Biological Sciences, in press. https://doi.org/10.1101/2020.06.03.132241

Rovatsos, M., Pokorná, M., Altmanová, M., & Kratochvíl, L. (2014). Cretaceous park of sex determination: sex chromosomes are conserved across iguanas. Biology Letters, 10, 20131093.

Rovatsos, M., Praschag, P., Fritz, U., & Kratochvíl, L. (2017). Stable Cretaceous sex chromosomes enable molecular sexing in softshell turtles (Testudines: Trionychidae). Scientific Reports, 7, 42150.

Rovatsos, M., Rehák, I., Velenský, P., & Kratochvíl, L. (2019). Shared ancient sex chromosomes in varanids, beaded lizards and alligator lizards. Molecular Biology and Evolution, 36, 1113-1120.

Rovatsos, M., Vukić, J., Altmanová, M., Johnson Pokorná, M., Moravec, J., & Kratochvíl, L. (2016). Conservation of sex chromosomes in lacertid lizards. Molecular Ecology, 25, 3120-3126.

Rovatsos, M., Vukić, J., & Kratochvíl, L. (2016). Mammalian X homolog acts as sex chromosome in lacertid lizards. Heredity, 117, 8-13.

Rupp, S. M., Webster, T. H., Olney, K. C., Hutchins, E. D., Kusumi, K., & Wilson Sayres, M. A. (2017). Evolution of dosage compensation in Anolis carolinensis, a reptile with XX/XY chromosomal sex determination. Genome Biology and Evolution, 9, 231-240.

Smith, C. A., Roeszler, K. N., Ohnesorg, T., Cummins, D. M., Farlie, P. G., Doran, T. J., & Sinclair, A. H. (2009). The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature, 461, 267-271.

Straková, B., Rovatsos, M., Kubička, L., & Kratochvíl, L. (2020). Evolution of sex determination in amniotes: Did stress and sequential hermaphroditism produce environmental determination? BioEssays, 42, e2000050.

Vicoso, B., & Bachtrog, D. (2009). Progress and prospects toward our understanding of the evolution of dosage compensation. Chromosome Research, 17, 585.

Vicoso, B., Emerson, J. J., Zektser, Y., Mahajan, S., & Bachtrog, D. (2013). Comparative sex chromosome genomics in snakes: differentiation, evolutionary strata, and lack of global dosage compensation. PLoS Biology, 11, e1001643.

Wang, Z., Pascual-Anaya, J., Zadissa, A., Li, W., Niimura, Y., Huang, Z., Li, C., White, S., Xiong, Z., Fang, D., Wang, B. O., Ming, Y., Chen, Y., Zheng, Y., Kuraku, S., Pignatelli, M., Herrero, J., Beal, K., Nozawa, M., … Irie, N. (2013). The draft genomes of soft-shell turtle and green sea turtle yield insights into the development and evolution of the turtle-specific body plan. Nature Genetics, 45, 701-706.

Wilson Sayres, M. A., & Makova, K. D. (2011). Genome analyses substantiate male mutation bias in many species. BioEssays, 33, 938-945.

Yntema, C. L., & Mrosovsky, N. (1980). Sexual differentiation in hatching loggerheads (Caretta caretta) incubated at different controlled temperatures. Herpetologica, 36, 33-36.

Zanetti, S., & Puoti, A. (2013). Sex determination in the Caenorhabditis elegans germline. In T. Schedl (ed.), Germ Cell Development in C. elegans. Advances in Experimental Medicine and Biology (vol. 757, pp. 41-69). Springer.

Zhang, Y., & Oliver, B. (2007). Dosage compensation goes global. Current Opinion in Genetics & Development, 17, 113-120.

Zimmer, F., Harrison, P. W., Dessimoz, C., & Mank, J. E. (2016). Compensation of dosage-sensitive genes on the chicken Z chromosome. Genome Biology and Evolution, 8, 1233-1242.

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