Cynoglossus semilaevis, commonly known as the Chinese tongue sole, is a popular aquaculture flatfish species.[1] They are native to China's northern coast but have experienced overfishing these past three decades.[1][2] Tongue sole farming began in 2003 and they have since become a popular, expensive seafood.[2] However, tongue soles have created issues for farmers due to their pathogen susceptibility and uneven sex ratio.[2]

Sex determination

Sex & sex reversal

Cynoglossus semilaevis have a female heterogametic sex-determination system, with females being ZW and males being ZZ.[3] Female tongue soles grow up to 2-4 times larger and faster than males. As such, female tongue soles are preferred by farmers and attempts have been made to breed all-female stocks via artificial gynogenesis.[4] In both the wild and in aquaculture, the sex ratio of Cynoglossus semilaevis is male-skewed due to a number of the females becoming pseudomales.[5] Pseudomales have female ZW chromosomes, but become physiologically male.[6] The offspring of pseudomales have a significantly lower growth rate than the offspring of males, and are more likely to become pseudomales themselves, further skewing the sex ratio.[3][5] This change occurs due to a combination of genotypic sex determination and temperature-dependent sex determination.[7] Exposure to higher temperatures during the gonadal sex differentiation stage (~56–62 days post-hatching) makes the sex change more likely, with one study finding that the percentage of females who became pseudomales was increased to 73% when reared at a higher temperature (28°C) as opposed to a 14% sex-reversal rate when reared at an ambient temperature (22°C).[3][8] Furthermore, the offspring of the pseudomales reared at 28°C had a sex-reversal rate of 94% despite being reared at 22°C.[3] This high rate of females becoming pseudomales in the F2 generation was attributed to the offspring inheriting their Z chromosome from their pseudomale father and retaining paternal methylation patterns.[9]

Sex-specific molecular markers

A single SNP, Cyn_Z_6676874, allows certain females to become pseudomales.[10] Females with a thymine at this site can undergo sex reversal, but females with an adenine cannot.[10] There are also three known female-specific molecular markers that can be used to distinguish between the various tongue sole sexes.[5] Two SNPs, SNP_chr_8935925_C_T and SNP_chr_8936186_C_G, and one indel were found to enable accurate differentiation between males, females, and pseudomales.[5]

Gene expression in the gonads

Gene expression in the gonads of males and females are different before sex determination, after sex determination, and after exposure to higher temperatures.[11] Prior to sex determination, males and females have differentially expressed genes (DEGs) related to muscle development.[11] Following sex determination, females have upregulated female-specific genes, figla and foxl2, and downregulation of the male-specific genes, dmrt1 and amh, under both ambient and high-temperature conditions.[11] When exposed to higher temperatures, males, females, and pseudomales have hundreds of DEGs in common that are mainly involved in biological processes and molecular functions.[11]

Pseudomale gonads have more similar gene expression patterns to males than females.[7] DEGs between males and pseudomales played a role in spermatogenesis and energy metabolism.[11] Whereas, DEGS between females and pseudomales were related to steroid hormones, helicase activity, sexual differentiation, and development.[11]

References

  1. 1 2 Hu, Yuanri; Li, Yangzhen; Li, Zhongming; Chen, Changshan; Zang, Jiajian; Li, Yuwei; Kong, Xiangqing (December 2020). "Novel insights into the selective breeding for disease resistance to vibriosis by using natural outbreak survival data in Chinese tongue sole (Cynoglossus semilaevis)". Aquaculture. 529: 735670. doi:10.1016/j.aquaculture.2020.735670. S2CID 224900889.
  2. 1 2 3 Li, Yangzhen; Hu, Yuanri; Yang, Yingming; Zheng, Weiwei; Chen, Changshan; Li, Zhongming (January 2021). "Selective breeding for juvenile survival in Chinese tongue sole (Cynoglossus semilaevis): Heritability and selection response". Aquaculture. 531: 735901. doi:10.1016/j.aquaculture.2020.735901. S2CID 224878642.
  3. 1 2 3 4 Shao, Changwei; Li, Qiye; Chen, Songlin; Zhang, Pei; Lian, Jinmin; Hu, Qiaomu; Sun, Bing; Jin, Lijun; Liu, Shanshan; Wang, Zongji; Zhao, Hongmei; Jin, Zonghui; Liang, Zhuo; Li, Yangzhen; Zheng, Qiumei (April 2014). "Epigenetic modification and inheritance in sexual reversal of fish". Genome Research. 24 (4): 604–615. doi:10.1101/gr.162172.113. ISSN 1088-9051. PMC 3975060. PMID 24487721.
  4. ↑ Chen, Song-Lin; Tian, Yong-Sheng; Yang, Jing-Feng; Shao, Chang-Wei; Ji, Xiang-Shan; Zhai, Jie-Ming; Liao, Xiao-Lin; Zhuang, Zhi-Meng; Su, Peng-Zhi; Xu, Jian-Yong; Sha, Zhen-Xia; Wu, Peng-Fei; Wang, Na (April 2009). "Artificial Gynogenesis and Sex Determination in Half-Smooth Tongue Sole (Cynoglossus semilaevis)". Marine Biotechnology. 11 (2): 243–251. doi:10.1007/s10126-008-9139-0. ISSN 1436-2228. PMID 18779997. S2CID 24780167.
  5. 1 2 3 4 Zhang, Bo; Zhao, Na; Liu, Yangyang; Jia, Lei; Fu, Yan; He, Xiaoxu; Liu, Kefeng; Xu, Zijing; Bao, Baolong (November 2019). "Novel molecular markers for high-throughput sex characterization of Cynoglossus semilaevis". Aquaculture. 513: 734331. doi:10.1016/j.aquaculture.2019.734331. S2CID 199639905.
  6. ↑ Dong, Zhongdian; Zhang, Ning; Liu, Yang; Xu, Wenteng; Cui, Zhongkai; Shao, Changwei; Chen, Songlin (January 2019). "Expression analysis and characterization of zglp1 in the Chinese tongue sole (Cynoglossus semilaevis)". Gene. 683: 72–79. doi:10.1016/j.gene.2018.10.003. PMID 30312653. S2CID 52975569.
  7. 1 2 Liu, Jinxiang; Liu, Xiaobing; Jin, Chaofan; Du, Xinxin; He, Yan; Zhang, Quanqi (29 May 2019). "Transcriptome Profiling Insights the Feature of Sex Reversal Induced by High Temperature in Tongue Sole Cynoglossus semilaevis". Frontiers in Genetics. 10: 522. doi:10.3389/fgene.2019.00522. ISSN 1664-8021. PMC 6548826. PMID 31191622.
  8. ↑ Zhu, Ying; Hu, Qiaomu; Xu, Wenteng; Li, Hailong; Guo, Hua; Meng, Liang; Wei, Min; Lu, Sheng; Shao, Changwei; Wang, Na; Yang, Guanpin; Chen, Songlin (10 May 2017). Liu, Chunming (ed.). "Identification and analysis of the β-catenin1 gene in half-smooth tongue sole (Cynoglossus semilaevis)". PLOS ONE. 12 (5): e0176122. Bibcode:2017PLoSO..1276122Z. doi:10.1371/journal.pone.0176122. ISSN 1932-6203. PMC 5425175. PMID 28489928.
  9. ↑ Chen, Songlin; Zhang, Guojie; Shao, Changwei; Huang, Quanfei; Liu, Geng; Zhang, Pei; Song, Wentao; An, Na; Chalopin, Domitille; Volff, Jean-Nicolas; Hong, Yunhan; Li, Qiye; Sha, Zhenxia; Zhou, Heling; Xie, Mingshu (March 2014). "Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle". Nature Genetics. 46 (3): 253–260. doi:10.1038/ng.2890. ISSN 1061-4036. PMID 24487278. S2CID 205348195.
  10. 1 2 Jiang, Li; Li, Hengde (1 February 2017). "Single Locus Maintains Large Variation of Sex Reversal in Half-Smooth Tongue Sole (Cynoglossus semilaevis)". G3: Genes, Genomes, Genetics. 7 (2): 583–589. doi:10.1534/g3.116.036822. ISSN 2160-1836. PMC 5295603. PMID 28007836.
  11. 1 2 3 4 5 6 Wang, Qian; Liu, Kaiqiang; Feng, Bo; Zhang, Zhihua; Wang, Renkai; Tang, Lili; Li, Wensheng; Li, Qiye; Piferrer, Francesc; Shao, Changwei (22 November 2019). "Transcriptome of Gonads From High Temperature Induced Sex Reversal During Sex Determination and Differentiation in Chinese Tongue Sole, Cynoglossus semilaevis". Frontiers in Genetics. 10: 1128. doi:10.3389/fgene.2019.01128. ISSN 1664-8021. PMC 6882949. PMID 31824559.
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