Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Ancient homomorphy of molluscan sex chromosomes sustained by reversible sex-biased genes and sex determiner translocation

Nature Ecology & Evolution volume 6, pages 1891–1906 (2022)Cite this article

Subjects

Abstract

Contrary to classic theory prediction, sex-chromosome homomorphy is prevalent in the animal kingdom but it is unclear how ancient homomorphic sex chromosomes avoid chromosome-scale degeneration. Molluscs constitute the second largest, Precambrian-originated animal phylum and have ancient, uncharacterized homomorphic sex chromosomes. Here, we profile eight genomes of the bivalve mollusc family of Pectinidae in a phylogenetic context and show 350 million years sex-chromosome homomorphy, which is the oldest known sex-chromosome homomorphy in the animal kingdom, far exceeding the ages of well-known heteromorphic sex chromosomes such as 130–200 million years in mammals, birds and flies. The long-term undifferentiation of molluscan sex chromosomes is potentially sustained by the unexpected intertwined regulation of reversible sex-biased genes, together with the lack of sexual dimorphism and occasional sex chromosome turnover. The pleiotropic constraint of regulation of reversible sex-biased genes is widely present in ancient homomorphic sex chromosomes and might be resolved in heteromorphic sex chromosomes through gene duplication followed by subfunctionalization. The evolutionary dynamics of sex chromosomes suggest a mechanism for ‘inheritance’ turnover of sex-determining genes that is mediated by translocation of a sex-determining enhancer. On the basis of these findings, we propose an evolutionary model for the long-term preservation of homomorphic sex chromosomes.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Phylogeny-scale profiling of scallop sexual systems and sex chromosomes.
Fig. 2: Discovery of oldest known, 350 Myr sex-chromosome homomorphy in scallop.
Fig. 3: Turnover and macroevolution of scallop sex chromosomes.
Fig. 4: Regulatory flexibility of SBG expression in scallop.
Fig. 5: Divergence of sex chromosome and rSBG duplication across animal groups.
Fig. 6: Evolutionary model for homomorphy maintenance and heteromorphy transition of sex chromosome.

Data availability

All sequencing data have been deposited to the NCBI’s SRA database and GenBank under the project accession number PRJNA796071. The accession numbers are listed in Supplementary Table 2. The genome assemblies and functional annotations of scallop species are also available in the MolluscDB database (http://mgbase.qnlm.ac/page/download/download). Source data are provided with this paper.

Code availability

The software and codes used in this study are publicly available, with corresponding versions indicated in Methods.

References

  1. Charlesworth, B. The evolution of sex chromosomes. Science 251, 1030–1033 (1991).

    Article  CAS  PubMed  Google Scholar 

  2. Wright, A. E., Dean, R., Zimmer, F. & Mank, J. E. How to make a sex chromosome. Nat. Commun. 7, 12087 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Jablonka, E. & Lamb, M. J. The evolution of heteromorphic sex chromosomes. Biol. Rev. Camb. Philos. Soc. 65, 249–276 (1990).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  5. Abbott, J. K., Nordén, A. K. & Hansson, B. Sex chromosome evolution: historical insights and future perspectives. Proc. Biol. Sci. 284, 20162806 (2017).

    PubMed  PubMed Central  Google Scholar 

  6. Daish, T. & Grützner, F. Evolution and meiotic organization of heteromorphic sex chromosomes. Curr. Top. Dev. Biol. 134, 1–48 (2019).

    Article  CAS  PubMed  Google Scholar 

  7. Steinemann, S. & Steinemann, M. Y chromosomes: born to be destroyed. BioEssays 27, 1076–1083 (2005).

    Article  CAS  PubMed  Google Scholar 

  8. Eggert, C. Sex determination: the amphibian models. Reprod. Nutr. Dev. 44, 539–549 (2004).

    Article  PubMed  Google Scholar 

  9. Devlin, R. H. & Nagahama, Y. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208, 191–364 (2002).

    Article  CAS  Google Scholar 

  10. Thiriot-Quievreux, C. Advances in chromosomal studies of gastropod molluscs. J. Molluscan Stud. 69, 187–202 (2003).

    Article  Google Scholar 

  11. Breton, S., Capt, C., Guerra, D. & Stewart, D. in Transitions Between Sexual Systems (ed. Leonard, J. L.) 165–192 (Springer International, 2007).

  12. Otto, S. P. et al. About PAR: the distinct evolutionary dynamics of the pseudoautosomal region. Trends Genet. 27, 358–367 (2011).

    Article  CAS  PubMed  Google Scholar 

  13. Yazdi, H. P. & Ellegren, H. Old but not (so) degenerated—slow evolution of largely homomorphic sex chromosomes in ratites. Mol. Biol. Evol. 31, 1444–1453 (2014).

    Article  CAS  PubMed  Google Scholar 

  14. Kuhl, H. et al. A 180 Myr-old female-specific genome region in sturgeon reveals the oldest known vertebrate sex determining system with undifferentiated sex chromosomes. Philos. Trans. R. Soc. Lond. B 376, 20200089 (2021).

    Article  Google Scholar 

  15. Furman, B. L. S. et al. Sex chromosome evolution: so many exceptions to the rules. Genome Biol. Evol. 12, 750–763 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Bachtrog, D. et al. Sex determination: why so many ways of doing it? PLoS Biol. 12, e1001899 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  17. Charlesworth, D. When and how do sex–linked regions become sex chromosomes? Evolution 75, 569–581 (2021).

    Article  PubMed  Google Scholar 

  18. Vicoso, B. Molecular and evolutionary dynamics of animal sex–chromosome turnover. Nat. Ecol. Evol. 3, 1632–1641 (2019).

    Article  PubMed  Google Scholar 

  19. Palmer, D. H., Rogers, T. F., Dean, R. & Wright, A. E. How to identify sex chromosomes and their turnover. Mol. Ecol. 28, 4709–4724 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  20. Giese, A. C. & Pearse, J. S. (eds) Reproduction of Marine Invertebrates Vol. 4 (Academic Press, 1977).

  21. Zhang, N., Xu, F. & Guo, X. Genomic analysis of the Pacific oyster (Crassostrea gigas) reveals possible conservation of vertebrate sex determination in a mollusc. G3 4, 2207–2217 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  22. Evensen, K. G., Robinson, W. E., Krick, K., Murray, H. M. & Poynton, H. C. Comparative phylotranscriptomics reveals putative sex differentiating genes across eight diverse bivalve species. Comp. Biochem Physiol. D 41, 100952 (2022).

    CAS  Google Scholar 

  23. Budd, G. E. The earliest fossil record of the animals and its significance. Philos. Trans. R. Soc. Lond. B 363, 1425–1434 (2008).

    Article  Google Scholar 

  24. Collin, R. Phylogenetic patterns and phenotypic plasticity of molluscan sexual systems. Integr. Comp. Biol. 53, 723–735 (2013).

    Article  PubMed  Google Scholar 

  25. Wallace, C. Parthenogenesis, sex, and chromosomes in Potamopyrgus. J. Molluscan Stud. 58, 93–107 (1992).

    Article  Google Scholar 

  26. Guo, X. & Allen, S. K. Jr. Sex determination and polyploid gigantism in the dwarf surfclam (Mulinia lateralis Say). Genetics 138, 1199–1206 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Jiao, W. et al. High-resolution linkage and quantitative trait locus mapping aided by genome survey sequencing: building up an integrative genomic framework for a bivalve mollusc. DNA Res. 21, 85–101 (2014).

    Article  CAS  PubMed  Google Scholar 

  28. Plazzi, F. & Passamonti, M. Towards a molecular phylogeny of mollusks: bivalves’ early evolution as revealed by mitochondrial genes. Mol. Phylogenet. Evol. 57, 641–657 (2010).

    Article  CAS  PubMed  Google Scholar 

  29. Serb, J. M. Reconciling morphological and molecular approaches in developing a phylogeny for the Pectinidae (Mollusca: Bivalvia). Dev. Aquac. Fish. Sci. 40, 1–29 (2016).

    Article  Google Scholar 

  30. Baird, G. C. & Brett, C. Regional variation and paleontology of two coral beds in the Middle Devonian Hamilton Group of western New York. J. Paleontol. 57, 417–446 (1983).

    Google Scholar 

  31. Mergl, M., Massa, D. & Plauchut, B. Devonian and Carboniferous brachiopods and bivalves of the Djado sub-basin (north Niger, SW Libya). J. Czech. Geol. Soc. 46, 169–188 (2001).

    Google Scholar 

  32. Sun, W. & Gao, L. Phylogeny and comparative genomic analysis of Pteriomorphia (Mollusca Bivalvia) based on complete mitochondrial genomes. Mar. Biol. Res. 13, 255–268 (2017).

    Article  Google Scholar 

  33. Waller, T. R. New Phylogenies of the Pectinidae (Mollusca: Bivalvia): reconciling morphological and molecular approaches. Dev. Aquac. Fish. Sci. 35, 1–44 (2006).

    Article  Google Scholar 

  34. Alejandrino, A., Puslednik, L. & Serb, J. M. Convergent and parallel evolution in life habit of the scallops (Bivalvia: Pectinidae). BMC Evol. Biol. 11, 164 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  35. Leder, E. H. et al. Female-biased expression on the X chromosome as a key step in sex chromosome evolution in threespine sticklebacks. Mol. Biol. Evol. 27, 1495–1503 (2010).

    Article  CAS  PubMed  Google Scholar 

  36. Meisel, R. P., Malone, J. H. & Clark, A. G. Disentangling the relationship between sex-biased gene expression and X-linkage. Genome Res. 22, 1255–1265 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Albritton, S. E. et al. Sex-biased gene expression and evolution of the x chromosome in nematodes. Genetics 197, 865–883 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Li, L. et al. Construction of AFLP-based genetic linkage map for Zhikong scallop, Chlamys farreri Jones et Preston and mapping of sex-linked markers. Aquaculture 245, 63–73 (2005).

    Article  CAS  Google Scholar 

  39. Boulanger, L. et al. Foxl2 is a female sex-determining gene in the goat. Curr. Biol. 24, 404–408 (2014).

    Article  CAS  PubMed  Google Scholar 

  40. Zhu, L. et al. Sexual dimorphism in diverse metazoans is regulated by a novel class of intertwined zinc fingers. Genes Dev. 14, 1750–1764 (2015).

    Article  Google Scholar 

  41. Goldstone, J. V. et al. Genetic and structural analyses of cytochrome P450 hydroxylases in sex hormone biosynthesis: sequential origin and subsequent coevolution. Mol. Phylogenet. Evol. 94, 676–687 (2016).

    Article  CAS  PubMed  Google Scholar 

  42. Bertho, S. et al. Foxl2 and its relatives are evolutionary conserved players in gonadal sex differentiation. Sex. Dev. 10, 111–129 (2016).

    Article  CAS  PubMed  Google Scholar 

  43. Capt, C. et al. Deciphering the link between doubly uniparental inheritance of mtDNA and sex determination in bivalves: clues from comparative transcriptomics. Genome Biol. Evol. 10, 577–590 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Kirkpatrick, M. How and why chromosome inversions evolve. PLoS Biol. 8, e1000501 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Natri, H. M., Merilä, J. & Shikano, T. The evolution of sex determination associated with a chromosomal inversion. Nat. Commun. 10, 145 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  46. Rubtsov, N. B. et al. Reorganization of the X chromosome in voles of the genus Microtus. Cytogenet. Genome Res. 99, 323–329 (2002).

    Article  CAS  PubMed  Google Scholar 

  47. Kalvari, I. et al. Non-Coding RNA analysis using the Rfam database. Curr. Protoc. Bioinforma. 62, e51 (2018).

    Article  Google Scholar 

  48. The RNAcentral Consortium. RNAcentral: a hub of information for non-coding RNA sequences. Nucleic Acids Res. 47, D221–D229 (2019).

    Article  Google Scholar 

  49. Esnault, C., Maestre, J. & Heidmann, T. Human LINE retrotransposons generate processed pseudogenes. Nat. Genet. 24, 363–367 (2000).

    Article  CAS  PubMed  Google Scholar 

  50. Troskie, R. L., Faulkner, G. J. & Cheetham, S. W. Processed pseudogenes: a substrate for evolutionary innovation: retrotransposition contributes to genome evolution by propagating pseudogene sequences with rich regulatory potential throughout the genome. BioEssays 43, e2100186 (2021).

    Article  PubMed  Google Scholar 

  51. Kostmann, A., Kratochvíl, L. & Rovatsos, M. Poorly differentiated XX/XY sex chromosomes are widely shared across skink radiation. Proc. Biol. Sci. 288, 20202139 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Veyrunes, F. et al. Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. Genome Res. 18, 965–973 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Vicoso, B. & Bachtrog, D. Numerous transitions of sex chromosomes in Diptera. PLoS Biol. 13, e1002078 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  54. Panigrahi, A. & O’Malley, B. W. Mechanisms of enhancer action: the known and the unknown. Genome Biol. 22, 108 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Braendle, C. & Félix, M. A. Sex determination: ways to evolve a hermaphrodite. Curr. Biol. 16, R468–R471 (2006).

    Article  CAS  PubMed  Google Scholar 

  56. Ellegren, H. & Parsch, J. The evolution of sex-biased genes and sex-biased gene expression. Nat. Rev. Genet. 8, 689–698 (2007).

    Article  CAS  PubMed  Google Scholar 

  57. Wang, S. et al. Scallop genome provides insights into evolution of bilaterian karyotype and development. Nat. Ecol. Evol. 1, 120 (2017).

    Article  PubMed  Google Scholar 

  58. Silina, A. V. Is sexual size dimorphism inherent in the scallop Patinopecten yessoensis? Scientifica 2016, 9 (2016).

    Article  Google Scholar 

  59. Yoshimura, T. et al. Sexual dimorphism in shell growth of the oviparous boreal scallop Swiftopecten swiftii (Bivalvia: Pectinidae). J. Molluscan Stud. 85, 253–261 (2019).

    Article  Google Scholar 

  60. Mank, J. E., Nam, K., Brunström, B. & Ellegren, H. Ontogenetic complexity of sexual dimorphism and sex-specific selection. Mol. Biol. Evol. 27, 1570–1578 (2010).

    Article  CAS  PubMed  Google Scholar 

  61. Perry, J. C., Harrison, P. W. & Mank, J. E. The ontogeny and evolution of sex-biased gene expression in Drosophila melanogaster. Mol. Biol. Evol. 31, 1206–1219 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Xu, W. et al. Transcriptomic analysis revealed gene expression profiles during the sex differentiation of Chinese tongue sole (Cynoglossus semilaevis). Comp. Biochem Physiol. D 40, 100919 (2021).

    CAS  Google Scholar 

  63. Ayers, K. L. et al. Identification of candidate gonadal sex differentiation genes in the chicken embryo using RNA-seq. BMC Genomics 16, 704 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  64. Aivatiadou, E., Mattei, E., Ceriani, M., Tilia, L. & Berruti, G. Impaired fertility and spermiogenetic disorders with loss of cell adhesion in male mice expressing an interfering Rap1 mutant. Mol. Biol. Cell. 18, 1530–1542 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Li, J., Xia, F. & Li, W. X. Coactivation of STAT and Ras is required for germ cell proliferation and invasive migration in Drosophila. Dev. Cell 5, 787–798 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Chowdhury, I., Branch, A., Mehrabi, S., Ford, B. D. & Thompson, W. E. Gonadotropin-dependent neuregulin-1 signaling regulates female rat ovarian granulosa cell survival. Endocrinology 158, 3647–3660 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Windley, S. P. & Wilhelm, D. Signaling pathways involved in mammalian sex determination and gonad development. Sex. Dev. 9, 297–315 (2015).

    Article  CAS  PubMed  Google Scholar 

  68. Zhou, Q. et al. Complex evolutionary trajectories of sex chromosomes across bird taxa. Science 346, 1246338 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  69. Vicoso, B., Kaiser, V. B. & Bachtrog, D. Sex-biased gene expression at homomorphic sex chromosomes in emus and its implication for sex chromosome evolution. Proc. Natl Acad. Sci. USA 110, 6453–6458 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Itoh, Y. et al. Dosage compensation is less effective in birds than in mammals. J. Biol. 6, 2 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  71. Mank, J. E. & Ellegren, H. All dosage compensation is local: gene-by-gene regulation of sex-biased expression on the chicken Z chromosome. Heredity 102, 312–320 (2009).

    Article  CAS  PubMed  Google Scholar 

  72. McQueen, H. A. & Clinton, M. Avian sex chromosomes: dosage compensation matters. Chromosome Res. 17, 687–697 (2009).

    Article  CAS  PubMed  Google Scholar 

  73. Emerson, J. J., Kaessmann, H., Betrán, E. & Long, M. Extensive gene traffic on the mammalian X chromosome. Science 303, 537–540 (2004).

    Article  CAS  PubMed  Google Scholar 

  74. Vibranovski, M. D., Zhang, Y. & Long, M. General gene movement off the X chromosome in the Drosophila genus. Genome Res. 19, 897–903 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Baker, R. H., Narechania, A., Johns, P. M. & Wilkinson, G. S. Gene duplication, tissue-specific gene expression and sexual conflict in stalk-eyed flies (Diopsidae). Philos. Trans. R. Soc. Lond. B 367, 2357–2375 (2012).

    Article  Google Scholar 

  76. Edgecombe, J., Urban, L., Todd, E. V. & Gemmell, N. J. Might gene duplication and neofunctionalization contribute to the sexual lability observed in fish? Sex. Dev. 15, 122–133 (2021).

    Article  CAS  PubMed  Google Scholar 

  77. Mank, J. E., Hultin-Rosenberg, L., Zwahlen, M. & Ellegren, H. Pleiotropic constraint hampers the resolution of sexual antagonism in vertebrate gene expression. Am. Nat. 171, 35–43 (2008).

    Article  PubMed  Google Scholar 

  78. Gallach, M. & Betrán, E. Intralocus sexual conflict resolved through gene duplication. Trends Ecol. Evol. 26, 222–228 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  79. Perry, J. C. Duplication resolves conflict. Nat. Ecol. Evol. 2, 597–598 (2018).

    Article  PubMed  Google Scholar 

  80. Yoshimoto, S. et al. Opposite roles of DMRT1 and its W-linked paralogue, DM-W, in sexual dimorphism of Xenopus laevis: implications of a ZZ/ZW-type sex-determining system. Development 137, 2519–2526 (2010).

    Article  CAS  PubMed  Google Scholar 

  81. Wang, Z. et al. Phylogeny and sex chromosome evolution of Palaeognathae. J. Genet. Genom. 49, 109–119 (2021).

    Article  Google Scholar 

  82. Wyman, M. J., Cutter, A. D. & Rowe, L. Gene duplication in the evolution of sexual dimorphism. Evolution 66, 1556–1566 (2012).

    Article  PubMed  Google Scholar 

  83. Rodriguez-Caro, F. et al. Novel doublesex duplication associated with sexually dimorphic development of dogface butterfly wings. Mol. Biol. Evol. 38, 5021–5033 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Bergero, R. & Charlesworth, D. The evolution of restricted recombination in sex chromosomes. Trends Ecol. Evol. 24, 94–102 (2009).

    Article  PubMed  Google Scholar 

  85. Gamble, T. et al. Restriction site–associated DNA sequencing (RAD-seq) reveals an extraordinary number of transitions among gecko sex-determining systems. Mol. Biol. Evol. 32, 1296–1309 (2015).

    Article  CAS  PubMed  Google Scholar 

  86. Jeffries, D. L. et al. A rapid rate of sex-chromosome turnover and non-random transitions in true frogs. Nat. Commun. 9, 4088 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  87. Woram, R. A. et al. Comparative genome analysis of the primary sex-determining locus in salmonid fishes. Genome Res. 13, 272–280 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Perrin, N. Sex reversal: a fountain of youth for sex chromosomes? Evolution 63, 3043–3049 (2009).

    Article  PubMed  Google Scholar 

  89. Xu, L., Wa Sin, S. Y., Grayson, P., Edwards, S. V. & Sackton, T. B. Evolutionary dynamics of sex chromosomes of paleognathous birds. Genome Biol. Evol. 11, 2376–2390 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. VanKuren, N. W. & Long, M. Gene duplicates resolving sexual conflict rapidly evolved essential gametogenesis functions. Nat. Ecol. Evol. 2, 705–712 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  91. Lipinska, A. et al. Sexual dimorphism and the evolution of sex-biased gene expression in the brown alga Ectocarpus. Mol. Biol. Evol. 32, 1581–1597 (2015).

    Article  CAS  PubMed  Google Scholar 

  92. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Darriba, D. et al. ModelTest–NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Mol. Biol. Evol. 37, 291–294 (2020).

    Article  CAS  PubMed  Google Scholar 

  94. Drummond, A. J. & Rambaut, A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  95. Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).

    Article  CAS  PubMed  Google Scholar 

  96. Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Kumar, S., Stecher, G., Suleski, M. & Hedges, S. B. TimeTree: a resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 34, 1812–1819 (2017).

    Article  CAS  PubMed  Google Scholar 

  98. Grasso, T. X. Redefinition, stratigraphy and depositional environments of the Mottville Member (Hamilton Group) in central and eastern New York. Dynamic stratigraphy and depositional environments of the Hamilton Group (middle Devonian) in New York State, Part I. NY State Mus. Bull. 457, 5–31 (1986).

    Google Scholar 

  99. Mergl, M. & Massa, D. Devonian and Lower Carboniferous Brachiopods and Bivalves from Western Libya (Universite Claude Bernard-Lyon I, 1992).

  100. Li, Y. et al. Scallop genome reveals molecular adaptations to semi-sessile life and neurotoxins. Nat. Commun. 8, 1721 (2017).

  101. Sambrook, J., Fritsch, E.F. & Maniatis, T. Molecular Cloning: A Laboratory Manual 2nd edn (Cold Spring Harbor Laboratory Press, 1989).

  102. Belton, J. M. et al. Hi-C: a comprehensive technique to capture the conformation of genomes. Methods 58, 268–276 (2012).

    Article  CAS  PubMed  Google Scholar 

  103. Zeng, Q. et al. High-quality reannotation of the king scallop genome reveals no ‘gene-rich’ feature and evolution of toxin resistance. Comput. Struct. Biotechnol. J. 19, 4954–4960 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Li, C. et al. Draft genome of the Peruvian scallop Argopecten purpuratus. GigaScience 7, giy031 (2018).

  105. Liu, X. et al. Draft genomes of two Atlantic bay scallop subspecies Argopecten irradians irradians and A. i. concentricus. Sci. Data 7, 99 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Ranallo-Benavidez, T. R., Jaron, K. S. & Schatz, M. C. GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. Nat. Commun. 11, 1432 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Koren, S. et al. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 27, 722–736 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Guan, D. et al. Identifying and removing haplotypic duplication in primary genome assemblies. Bioinformatics 36, 2896–2898 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Walker, B. J. et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 19, e112963 (2014).

    Article  Google Scholar 

  112. Durand, N. C. et al. Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Syst. 3, 95–98 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Dudchenko, O. et al. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science 356, 92–95 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Cantarel, B. L. et al. MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res. 18, 188–196 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Stanke, M. et al. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 34, W435–W439 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Korf, I. Gene finding in novel genomes. BMC Bioinform. 5, 59 (2004).

    Article  Google Scholar 

  117. Waterhouse, R. M. et al. BUSCO applications from quality assessments to gene prediction and phylogenomics. Mol. Biol. Evol. 35, 543–548 (2018).

    Article  CAS  PubMed  Google Scholar 

  118. Sonnhammer, E. L., Eddy, S. R. & Durbin, R. Pfam: a comprehensive database of protein domain families based on seed alignments. Proteins 28, 405–420 (1997).

    Article  CAS  PubMed  Google Scholar 

  119. Zhang, L., Bao, Z., Wang, S., Huang, X. & Hu, J. Chromosome rearrangements in Pectinidae (Bivalvia: Pteriomorphia) implied based on chromosomal localization of histone H3 gene in four scallops. Genetica 130, 193–198 (2007).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Van der Auwera, G. A. et al. From FastQ data to high–confidence variant calls: the Genome Analysis Toolkit best practices pipeline. Curr. Protoc. Bioinform. 43, 11.10.1–11.10.33 (2013).

    Article  Google Scholar 

  122. Li, R. et al. FOXL2 and DMRT1L are Yin and Yang genes for determining timing of sex differentiation in the bivalve mollusk Patinopecten yessoensis. Front. Physiol. 9, 1166 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  123. Shi, S. R., Key, M. E. & Kalra, K. L. Antigen retrieval in formalin-fixed, paraffin-embedded tissues: an enhancement method for immunohistochemical staining based on microwave oven heating of tissue sections. J. Histochem. Cytochem. 39, 741–748 (1991).

    Article  CAS  PubMed  Google Scholar 

  124. Darling, A. C., Mau, B., Blattner, F. R. & Perna, N. T. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 14, 1394–1403 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Albertin, C. B. et al. The octopus genome and the evolution of cephalopod neural and morphological novelties. Nature 524, 220–224 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Ip, J. C.-H. et al. Host–endosymbiont genome integration in a deep-sea chemosymbiotic clam. Mol. Biol. Evol. 38, 502–518 (2021).

    Article  CAS  PubMed  Google Scholar 

  127. Kimura, M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111–120 (1980).

    Article  CAS  PubMed  Google Scholar 

  128. Tan, G., Polychronopoulos, D. & Lenhard, B. CNEr: a toolkit for exploring extreme noncoding conservation. PLoS Comput. Biol. 15, e1006940 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Frith, M. C., Hamada, M. & Horton, P. Parameters for accurate genome alignment. BMC Bioinform. 11, 80 (2010).

    Article  Google Scholar 

  130. Kent, W. J. et al. The human genome browser at UCSC. Genome Res. 12, 996–1006 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Kent, W. J. BLAT—the BLAST-like alignment tool. Genome Res. 12, 656–664 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  132. Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y. & Greenleaf, W. J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10, 1213–1218 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  135. Zhang, Y. et al. Model-based analysis of ChIP–Seq (MACS). Genome Biol. 9, R137 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  136. Stark R, & Brown, G. DiffBind: Differential Binding Analysis of ChIP–Seq Peak Data (Bioconductor, 2011).

  137. Sherf, B. A., Navarro, S. L., Hannah, R. & Wood, K. V. Dual-luciferase TM reporter assay: an advanced co-reporter technology integrating firefly and Renilla luciferase assays. Promega Notes 57, 2–9 (1996).

    Google Scholar 

  138. Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).

    Article  CAS  PubMed  Google Scholar 

  139. Chen, S. et al. De novo analysis of transcriptome dynamics in the migratory locust during the development of phase traits. PLoS ONE 5, e15633 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Langfelder, P. & Horvath, S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinform. 9, 559 (2008).

    Article  Google Scholar 

  141. Liu, B.-H. et al. DCGL: an R package for identifying differentially coexpressed genes and links from gene expression microarray data. Bioinformatics 26, 2637–2638 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289–300 (1995).

    Google Scholar 

  143. Shannon, P. et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498–2504 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Wang, Y. P. et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 40, e49 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Mokrina, M., Nagasawa, K., Kanamori, M., Natsuike, M. & Osada, M. Seasonal composition of immature germ cells in the Yesso scallop identified by vasa-like gene (my-vlg) and protein expression, with evidence of irregular germ cell differentiation accompanied with a high mortality event. Aquac. Rep. 19, 100613 (2021).

    Article  Google Scholar 

Download references

Acknowledgements

This research is part of the ongoing M10K+ genome project proposed by M10K+ Consortium and targets sequencing of 10,000 molluscan genomes. We would like to thank J. C. Perry (University of East Anglia) for providing fruit fly transcriptomic resources and Q. Zhou (Zhejiang University) for providing emu genomic resources. We thank Y. Zhang (South China Sea Institute of Oceanology) for assisting the collection of moon scallop samples. We acknowledge the grant support from National Key Research and Development Project (2018YFD0900200), Marine S&T Fund of Shandong Province for Pilot National Laboratory for Marine Science and Technology (Qingdao) (2022QNLM050101-1), National Natural Science Foundation of China (32172967, 32130107), Project of Sanya Yazhouwan Science and Technology City Management Foundation (SKJC-KJ-2019KY01), Key R&D Project of Shandong Province (2020ZLYS10, 2021ZLGX03), China Agriculture Research System of MOF and MARA and Taishan Scholar Project Fund of Shandong Province of China.

Author information

Author notes

  1. These authors contributed equally: Wentao Han, Liangjie Liu, Jing Wang, Huilan Wei, Yuli Li, Lijing Zhang.

Authors and Affiliations

  1. Sars-Fang Centre & MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, China

    Wentao Han, Liangjie Liu, Jing Wang, Huilan Wei, Yuli Li, Lijing Zhang, Zhenyi Guo, Yajuan Li, Tian Liu, Qifan Zeng, Qiang Xing, Ya Shu, Tong Wang, Yaxin Yang, Meiwei Zhang, Ruojiao Li, Jiachen Yu, Zhongqi Pu, Jia Lv, Shanshan Lian, Jingjie Hu, Xiaoli Hu, Zhenmin Bao, Lingling Zhang & Shi Wang

  2. Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China

    Wentao Han, Jing Wang, Yuli Li, Shanshan Lian, Lingling Zhang & Shi Wang

  3. Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China

    Qifan Zeng, Qiang Xing, Xiaoli Hu & Zhenmin Bao

  4. Key Laboratory of Tropical Aquatic Germplasm of Hainan Province, Sanya Oceanographic Institution, Ocean University of China, Sanya, China

    Qifan Zeng, Jingjie Hu, Zhenmin Bao & Shi Wang

  5. Institute of Evolution & Marine Biodiversity, Ocean University of China, Qingdao, China

    Lisui Bao

Authors
  1. Wentao Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Liangjie Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Huilan Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuli Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lijing Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhenyi Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yajuan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Tian Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Qifan Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Qiang Xing
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Ya Shu
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Tong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Yaxin Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Meiwei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Ruojiao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Jiachen Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Zhongqi Pu
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Jia Lv
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Shanshan Lian
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Jingjie Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. Xiaoli Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  23. Zhenmin Bao
    View author publications

    You can also search for this author in PubMed Google Scholar

  24. Lisui Bao
    View author publications

    You can also search for this author in PubMed Google Scholar

  25. Lingling Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  26. Shi Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Lingling Zhang, S.W. and Z.B. conceived and designed the study. Lingling Zhang, S.W. and L.B. coordinated and supervised the whole study. W.H., Yuli Li, Q.Z. and T.W. conducted the genome sequencing and assembly. L.L., Lijing Zhang, J.W., T.L., M.Z. and R.L. prepared the libraries for transcriptome sequencing. W.H., S.W., Lingling Zhang, L.B., J.W. and Yuli Li participated in genome and transcriptome analysis. Z.G. and Lijing Zhang performed the sex marker verification. Yajuan Li and Lijing Zhang prepared the libraries for ATAC-seq. L.L. conducted the dual-luciferase reporter assay. H.W. and Lijing Zhang performed the histological analysis, RT–qPCR and immunohistochemistry experiments. Q.X., Q.Z., Y.S., Y.Y. and J.Y. participated in scallop culture and sample collection. Z.B., J.H., X.H., S.L., J.L. and Z.P. participated in discussions and provided suggestions for manuscript improvement. S.W., Lingling Zhang, W.H., L.B. and J.W. did most of the writing with input from the other authors.

Corresponding authors

Correspondence to Lisui Bao, Lingling Zhang or Shi Wang.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks the anonymous reviewers for their contribution to the peer review of this work. Peer reviewer reports are available.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Table 1 Genome assembly statistics of eight scallop species
Full size table

Extended Data Fig. 1 Chromosomal architecture and synteny comparison of eight scallop species.

(a) The chromosome architectures of P. yessoensis and 7 other scallop species (their chromosomes coloured with reference to P. yessoensis based on gene correspondence). The red star indicates sex chromosome. (b) Chromosome-wide gene synteny comparison between P. yessoensis and 7 other scallop species.

Extended Data Fig. 2 Identification of scallop sex chromosome and sex-determining gene.

(a, b) Searching for sex-related regions among 19 chromosomes of Patinopecten yessoensis and Chlamys farreri. Circle i, the number distribution of female-related 1-kb bins within a 50-kb window. Such bins show significant female-biased read coverage at the p-value threshold of 0.001. The sex-related region is defined by read coverage depth using a 1-kb bin and the threshold of p-value was set at 0.001. Circle ii, the expression profile of female-biased genes across 19 chromosomes. Circle iii, genome-wide distribution of sexually dimorphic SNP loci. Circle iv, the number distribution of male-related 1-kb bins within a 50-kb window. Circle v, the expression profile of male-biased genes across 19 chromosomes. The sex-related region around FOXL2 is indicated by red circle. (c) Circos plot of gene synteny in 19 chromosome pairs between female and male genome assembly of C. farreri. (d) The histogram shows the normalized coverage for female-specific region around the FOXL2 gene of C. farreri. (e) Structural comparison of sex-linked regions among Z and W contigs of female assembly and Z contig of the male assembly in C. farreri.

Extended Data Fig. 3 Phylogenetic and expression analysis of three putative sex-determining genes.

(a–c) Phylogenetic trees of FOXL2, ZNF226l, CYP3A24l and their belonging gene families. (d) Expression profiles of sex-determining genes in mature ovaries and testes of scallops. Differential analysis using the edgeR test with a Bonferroni correction based on n=3 biologically independent samples. The error bars represent the means ± S.E.M. (e & f) Expression profiles of ZNF226l- and CYP3A24l-residing clades, showing ZNF226l and CYP3A24l are the most female-biased copies (indicated by red names).

Extended Data Fig. 4 Gonad histology and FOXL2 expression during early sex differentiation.

(a) The morphology of gonads of P. yessoensis aged 5 to 11 months. (b) Paraffin sections of female and male gonads. Each experiment was repeated twice independently with similar results. In, intestine; Ct, connective tissue; F, follicle; Fc, follicular cell; Sig, sexually indistinguishable gonium; Og, oogonium; Oc, oocyte; Sg, spermatogonium; Sc, spermatocyte. (c) Temporal expression patterns of FOXL2 measured by RT–qPCR profiling of ovaries and testes of scallops. The earliest differential expression of FOXL2 between sexes occurs at around 7 months of age (based on the one-sided t-test), indicating the initiation of sex differentiation. For each month age, at least 8 samples were assayed and all reactions were conducted in triplicate. The error bars represent the means ± S.E.M. (d) Spatial expression patterns of FOXL2 in ovary and testis by immunohistochemistry. FOXL2 protein primarily locates in the germ cells and follicular cells within the follicles in the ovary (top panel) and testis (bottom panel), confirming its role in sex differentiation. Each experiment was repeated twice independently with similar results.

Extended Data Fig. 5 PCR-based validation of female-specific regions in P. yessoensis.

(a) The gonad morphology for 100 assayed females and males. (b, c) PCR products amplified using two sets of female-specific primer pairs (P11 and P14) for 100 female and male individuals sampled from Dalian (Liaoning, P.R China) and 100 individuals sampled from Yantai (Shandong, P.R China). Additional full-scan images are provided in Source Data Extended Fig. 5. Each PCR was repeated twice independently.

Source data

Extended Data Fig. 6 Functional characterization of the FOXL2 enhancer.

Top panel, female-related ATAC peaks in the upstream of FOXL2. Middle panel, plasmid construction from FOXL2-peak1 to FOXL2-peak3 (right to left) used in dual-luciferase assays. Bottom panel, enhancer activities of peaks 1–3 as measured by luciferase assays. The peaks 1–3 showed significant enhancer activity compared to the empty vector pGL3-promoter (based on the two-sided t-test with n=3 biologically independent samples). For boxplot, centre line and box limits represent the median, upper and lower quartiles respectively, whereas whiskers are 1.5x interquartile ranges.

Extended Data Fig. 7 Expression profiling and co-expression network analysis of SBGs during female/male gonad development.

(a) The log-based distribution of male/female expression levels from five gonadal stages across all genes (grey curve) and chr. 15 genes (green curve). (b) The expression patterns of constant female-biased genes, constant male-biased genes and rSBGs across five gonadal development stages. Dash lines show the tendency for female (red) and male (blue) across sex differentiated (D), proliferative (P), growing (G), mature (M) and resting (R) stages. The comparison is based on 1,860 constant female-biased genes, 2,284 constant male-biased genes, and 2,279 rSBGs. For boxplot, centre line and box limits represent the median, upper and lower quartiles respectively, whereas whiskers are 1.5x interquartile ranges. (c) Gene module correspondence between female network (FM1–10) and male network (MM1–8). Notably, the female FM1 module that is significantly enriched with both female-biased genes and rSBGs show the strongest correspondence with the male MM1 module that is significantly enriched with male-biased genes. (d) Network visualization of FM1 (left) and MM1 (right) showing the high intramodular connectivity of rSBGs. Top 30% genes with the highest intramodular connectivity in FM1/MM1 are chosen for network display. Red, blue and purple nodes represent constant female-biased genes, constant male-biased genes and rSBGs, respectively. Node size indicates the intramodular connectivity.

Extended Data Fig. 8 Summary of SBG expression across eight scallop species.

The pie charts show the distribution of SBGs for each scallop species. Histograms show the shared numbers of SBGs by different scallop species. For across-species comparison, the shared genes with consistent female-bias or male-bias are indicated by red and blue bars, whereas those showing the opposite sex-bias patterns are indicated by purple bars.

Extended Data Fig. 9 Sex chromosome-related gene duplication and expressional changes in flatfish, fruit fly and human.

(a–c) Summary of transposed gene duplication rates for autosomes and sex chromosomes in flatfish (ZW-type), fruit fly (XY-type) and human (XY-type), with statistics based on the two-sided Fisher’s exact test. Duplicate gene ratio is calculated by dividing transposed duplicate genes by total genes in specified chromosomes or sex-related regions, that is 0.184 (169/918) for DR and 0.093 (1879/20104) for autosomes in flatfish, 0.024 (48/2000) for DR and 0.017 (179/10737) for autosomes in fruit fly, and 0.034 (28/831) for DR and 0.034 (712/21194) for autosomes in human. (d–f) The Sankey diagrams show the expressional dynamics of duplicated A copies with their parental Z/X copies across various gonad developmental stages of flatfish (48-, 68- and 128-day post hatching), fruit fly (larva, pre-pupa and adult) and human (7, 12 and 17 postconceptional weeks). Pie charts show the proportion of constant SBGs (red or blue) and rSBGs (purple) based on the comparison between Z/X copies and duplicated A copies.

Supplementary information

Supplementary Information

Supplementary Figs. 1–12 and Tables 3–8, 11, 12 and 16.

Reporting Summary

Peer Review File

Supplementary Tables

Supplementary Table 1. Taxon sampling for the phylogeny based on 12S rRNA, 16S rRNA and 28S rRNA. Table 2. Summary of genomic/transcriptomic datasets and accession numbers. Table 9. Distribution of SBGs in adult tissues of P. yessoensis. Table 10. Distribution of SBGs across five gonad developmental stages of P. yessoensis. Table 13. KEGG enrichment analysis of scallop SBGs based on the two-sided chi-square test. Table 14. GO enrichment analysis of scallop SBGs based on the two-sided chi-square test. Table 15. Summary of the co-expression gene networks of scallop. Table 17. Summary of SBGs across eight scallop genomes. Table 18. Summary of sex chromosome-related transposed gene duplication in the DR of emu. Table 19. Summary of sex chromosome-related transposed gene duplication in the DR of chicken. Table 20. Summary of sex chromosome-related transposed gene duplication in the DR of flatfish. Table 21. Summary of sex chromosome-related transposed gene duplication in the DR of fruit fly. Table 22. Summary of sex chromosome-related transposed gene duplication in the DR of human.

Source data

Source Data Fig. 2

Unprocessed gels for Fig. 2d.

Source Data Extended Data Fig. 5

Unprocessed gels for Fig. 5b,c.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Han, W., Liu, L., Wang, J. et al. Ancient homomorphy of molluscan sex chromosomes sustained by reversible sex-biased genes and sex determiner translocation. Nat Ecol Evol 6, 1891–1906 (2022). https://doi.org/10.1038/s41559-022-01898-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-022-01898-6

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing