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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

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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.

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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.

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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.

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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.

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  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

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  1. Wentao Han
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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.

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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.

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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.

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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

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