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Morphological and histological changes in the brains of turbot (Scophthalmus maximus) with gonadal development

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Abstract

The brain plays a critical role in controlling reproduction through the hypothalamus-pituitary-gonadal (HPG) axis in vertebrates. Turbot (Scophthalmus maximus) has become an economically important marine fish in Europe and North China. Previous research investigating turbot reproduction has focused on the role of the HPG axis in regulating egg and sperm production. However, the morphology and histology of the organs in the HPG axis have not been studied. In this study, we investigated the morphology and histology of brains in female and male turbot at different stages of gonadal development. The results showed that the brains of both female and male turbot were composed of seven parts that are typical of advanced teleosts: the telencephalon, diencephalon, cerebellum, hypothalamus, pituitary gland, myelencephalon, and olfactory bulbs. The telencephalon was well-developed and contained five distinct lobes, with the contiguous diencephalon at the caudal portion. The torus longitudinales and rostral torus semicircularis of the mesencephalon flattened along the dorsal surface, and the rostral corpus cerebellum was located in the dorsal portion. The actual total brain volume in mature males was significantly greater (p<0.05) than that of females with gonadal development. Notably, the pituitary volume in male turbot significantly increased (p<0.05) from immature to mature stage, but this difference did not occur in females. The data together illustrate a distinct sex difference in the turbot brain during gonadal development, providing insight into their HPG axes.

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References

  • Acevedo-Rodriguez A, Kauffman A S, Cherrington B D, et al. 2018. Emerging insights into hypothalamic-pituitary-gonadal axis regulation and interaction with stress signalling. Journal of Neuroendocrinology, 30(10): e12590

    Article  Google Scholar 

  • Alvariño J M R, Rebollar P G, Olmedo M, et al. 2001. Effects of melatonin implants on reproduction and growth of turbot broodstock. Aquaculture International, 9(6): 477–487, doi: https://doi.org/10.1023/A:1020590111031

    Article  Google Scholar 

  • Bauchot R, Ridet J M, Bauchot M L. 1989. The brain organization of butterflyfishes. Environmental Biology of Fishes, 25(1): 205

    Article  Google Scholar 

  • Bizzarri C, Cappa M. 2020. Ontogeny of hypothalamus-pituitary gonadal axis and minipuberty: an ongoing debate?. Frontiers in Endocrinology, 11: 187.

    Article  Google Scholar 

  • Borella M I, Chehade C, Costa F G, et al. 2019. The brain-pituitary-gonad axis and the gametogenesis. In: Baldisserotto B, Urbinati E C, Cyrino J E P, eds. Biology and Physiology of Freshwater Neotropical Fish. Amsterdam: Academic Press, 315–341

    Google Scholar 

  • Borella M I, Venturieri R, Mancera J M. 2009. Immunocytochemical identification of adenohypophyseal cells in the pirarucu (Arapaima gigas), an Amazonian basal teleost. Fish Physiology and Biochemistry, 35(1): 3–16, doi: https://doi.org/10.1007/s10695-008-9254-x

    Article  Google Scholar 

  • Briñón J G, Médina M, Arévalo R, et al. 1993. Volumetric analysis of the telencephalon and tectum during metamorphosis in a flatfish, the turbot Scophthalmus maximus. Brain, Behavior and Evolution, 41(1): 1–5

    Article  Google Scholar 

  • Broglio C, Rodríguez F, Salas C. 2003. Spatial cognition and its neural basis in teleost fishes. Fish and Fisheries, 4(3): 247–255, doi: https://doi.org/10.1046/j.1467-2979.2003.00128.x

    Article  Google Scholar 

  • Burns J G, Rodd F H. 2008. Hastiness, brain size and predation regime affect the performance of wild guppies in a spatial memory task. Animal Behaviour, 76(3): 911–922, doi: https://doi.org/10.1016/j.anbehav.2008.02.017

    Article  Google Scholar 

  • Demski L S. 2003. In a fish’s mind’s eye: the visual pallium of teleosts. In: Collin S P, Marshall N J, eds. Sensory Processing in Aquatic Environments. New York: Springer, 404–419

    Chapter  Google Scholar 

  • Dwyer A A, Quinton R. 2019. Anatomy and physiology of the hypothalamic-pituitary-gonadal (HPG) axis. In: Llahana S, Follin C, Yedinak C, et al., eds. Advanced Practice in Endocrinology Nursing. Cham: Springer, 839–852

    Chapter  Google Scholar 

  • Eastman J T, Lannoo M J. 2008. Brain and sense organ anatomy and histology of the Falkland Islands mullet, Eleginops maclovinus (Eleginopidae), the sister group of the Antarctic notothenioid fishes (Perciformes: Notothenioidei). Journal of Morphology, 269(1): 84–103, doi: https://doi.org/10.1002/jmor.10571

    Article  Google Scholar 

  • Finger T E. 1988. Organization of chemosensory systems within the brains of bony fishes. In: Atema J, Fay R R, Popper A N, et al., eds. Sensory Biology of Aquatic Animals. New York: Springer, 339–363

    Chapter  Google Scholar 

  • Gonda A, Herczeg G, Merilä J. 2009. Adaptive brain size divergence in nine-spined sticklebacks (Pungitius pungitius)?. Journal of Evolutionary Biology, 22(8): 1721–1726

    Article  Google Scholar 

  • Gonzalez-Voyer A, Winberg S, Kolm N. 2009a. Brain structure evolution in a basal vertebrate clade: evidence from phylogenetic comparative analysis of cichlid fishes. BMC Evolutionary Biology, 9(1): 238, doi: https://doi.org/10.1186/1471-2148-9-238

    Article  Google Scholar 

  • Gonzalez-Voyer A, Winberg S, Kolm N. 2009b. Social fishes and single mothers: brain evolution in African cichlids. Proceedings of the Royal Society B: Biological Sciences, 276(1654): 161–167, doi: https://doi.org/10.1098/rspb.2008.0979

    Article  Google Scholar 

  • Imsland A K, Dragsnes M, Stefansson S O. 2003. Exposure to continuous light inhibits maturation in turbot (Scophthalmus maximus). Aquaculture, 219(1–4): 911–919

    Article  Google Scholar 

  • Ishikawa Y, Yoshimoto M, Yamamoto N, et al. 1999. Different brain morphologies from different genotypes in a single teleost species, the Medaka (Oryzias latipes). Brain, Behavior and Evolution, 53(1): 2–9

    Article  Google Scholar 

  • Ito H, Ishikawa Y, Yoshimoto M, et al. 2007. Diversity of brain morphology in teleosts: brain and ecological niche. Brain, Behavior and Evolution, 69(2): 76–86

    Article  Google Scholar 

  • Kolm N, Gonzalez-Voyer A, Brelin D, et al. 2009. Evidence for small scale variation in the vertebrate brain: mating strategy and sex affect brain size and structure in wild brown trout (Salmo trutta). Journal of Evolutionary Biology, 22(12): 2524–2531, doi: https://doi.org/10.1111/j.1420-9101.2009.01875.x

    Article  Google Scholar 

  • Kotrschal K, Krautgartner W D, Adam H. 1983. Crown cells in the di-encephalon of Acipenser ruthenus (Acipenseridae, Chondrostei). Journal für Hirnforschung, 24(6): 655–657

    Google Scholar 

  • Kotrschal K, van Staaden M J, Huber R. 1998. Fish brains: evolution and anvironmental relationships. Reviews in Fish Biology and Fisheries, 8(4): 373–408, doi: https://doi.org/10.1023/A:1008839605380

    Article  Google Scholar 

  • Lin Fan, Xu Shihong, Ma Daoyuan, et al. 2012. Germ line specific expression of a vasa homologue gene in turbot (Scophthalmus maximus): evidence for vasa localization at cleavage furrows in euteleostei. Molecular Reproduction and Development, 79(11): 803–813, doi: https://doi.org/10.1002/mrd.22120

    Article  Google Scholar 

  • Lin Fan, Zhao Chunyan, Xu Shihong, et al. 2013. Germline-specific and sexually dimorphic expression of a dead end gene homologue in turbot (Scophthalmus maximus). Theriogenology, 80(6): 665–672, doi: https://doi.org/10.1016/j.theriogenology.2013.06.016

    Article  Google Scholar 

  • Liu Yifan, Liu Qinghua, Xu Shihong, et al. 2021. A deep insight of spermatogenesis and hormone levels of aqua-cultured turbot (Scophthalmus maximus). Frontiers in Marine Science, 7: 592880, doi: https://doi.org/10.3389/fmars.2020.592880

    Article  Google Scholar 

  • Loveland J L, Giraldo-Deck L M, Lank D B, et al. 2021. Functional differences in the hypothalamic-pituitary-gonadal axis are associated with alternative reproductive tactics based on an inversion polymorphism. Hormones and Behavior, 127: 104877, doi: https://doi.org/10.1016/j.yhbeh.2020.104877

    Google Scholar 

  • MacManes M D, Austin S H, Lang A S, et al. 2017. Widespread patterns of sexually dimorphic gene expression in an avian hypothalamic-pituitary-gonadal (HPG) axis. Scientific Reports, 7: 45125, doi: https://doi.org/10.1038/srep45125

    Article  Google Scholar 

  • Maharajan K, Muthulakshmi S, Karthik C, et al. 2020. Pyriproxyfen induced impairment of reproductive endocrine homeostasis and gonadal histopathology in zebrafish (Danio rerio) by altered expression of hypothalamus-pituitary-gonadal (HPG) axis genes. Science of the Total Environment, 735: 139496, doi: https://doi.org/10.1016/j.scitotenv.2020.139496

    Article  Google Scholar 

  • Meethal S V, Atwood C S. 2005. The role of hypothalamic-pituitary-gonadal hormones in the normal structure and functioning of the brain. Cellular and Molecular Life Sciences, 62(3): 257–270, doi: https://doi.org/10.1007/s00018-004-4381-3

    Google Scholar 

  • Miwa S, Inui Y. 1987. Histological changes in the pituitary-thyroid axis during spontaneous and artificially-induced metamorphosis of larvae of the flounder Paralichthys olivaceus. Cell and Tissue Research, 249(1): 117–123, doi: https://doi.org/10.1007/BF00215425

    Article  Google Scholar 

  • Northcutt R G. 2006. Connections of the lateral and medial divisions of the goldfish telencephalic pallium. Journal of Comparative Neurology, 494(6): 903–943, doi: https://doi.org/10.1002/cne.20853

    Article  Google Scholar 

  • Pitnick S, Jones K E, Wilkinson G S. 2006. Mating system and brain size in bats. Proceedings of the Royal Society B: Biological Sciences, 273(1587): 719–724, doi: https://doi.org/10.1098/rspb.2005.3367

    Article  Google Scholar 

  • Pollen A A, Dobberfuhl A P, Scace J, et al. 2007. Environmental complexity and social organization sculpt the brain in Lake Tanganyikan cichlid fish. Brain, Behavior and Evolution, 70(1): 21–39

    Article  Google Scholar 

  • Rao P D P, Finger T E. 1984. Asymmetry of the olfactory system in the brain of the winter flounder, Pseudopleuronectes americanus. Journal of Comparative Neurology, 225(4): 492–510, doi: https://doi.org/10.1002/cne.902250403

    Article  Google Scholar 

  • Safi K, Dechmann D K N. 2005. Adaptation of brain regions to habitat complexity: a comparative analysis in bats (Chiroptera). Proceedings of the Royal Society B: Biological Sciences, 272(1559): 179–186, doi: https://doi.org/10.1098/rspb.2004.2924

    Article  Google Scholar 

  • Stoss J H, Røer J E. 2020. Controlled reproduction in turbot (Scopthalmus maximus). In: Reinertsen H, Dahle L A, Jørgensen L, et al., eds. Fish Farming Technology. London: CRC Press

    Google Scholar 

  • Striedter G F, Northcutt R G. 2006. Head size constrains forebrain development and evolution in ray-finned fishes. Evolution and Development, 8: 215–222

    Article  Google Scholar 

  • Ullmann J F P, Cowin G, Collin S P. 2010. Quantitative assessment of brain volumes in fish: comparison of methodologies. Brain, Behavior and Evolution, 76(3–4): 261–270

    Article  Google Scholar 

  • White G E, Brown C. 2015a. Microhabitat use affects brain size and structure in intertidal gobies. Brain, Behavior and Evolution, 85(2): 107–116

    Article  Google Scholar 

  • White G E, Brown C. 2015b. Variation in brain morphology of inter-tidal gobies: a comparison of methodologies used to quantitatively assess brain volumes in fish. Brain, Behavior and Evolution, 85(4): 245–256

    Article  Google Scholar 

  • Xu Wengang, Manabe S, Mushirobira Y, et al. 2020. Changes in expression of reproduction-related hormones in the brain and pituitary during early ovarian differentiation and development in the red spotted grouper Epinephelus akaara, with emphasis on FSHβ and LHβ. Aquaculture, 514: 734497, doi: https://doi.org/10.1016/j.aquaculture.2019.734497

    Article  Google Scholar 

  • Xue Rui, Wang Xueying, Xu Shihong, et al. 2018. Expression profile and localization of vitellogenin mRNA and protein during ovarian development in turbot (Scophthalmus maximus). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 226: 53–63, doi: https://doi.org/10.1016/j.cbpb.2018.08.002

    Article  Google Scholar 

  • Zhao Chunyan, Liu Qinghua, Xu Shihong, et al. 2018a. Identification of type A spermatogonia in turbot (Scophthalmus maximus) using a new cell-surface marker of Lymphocyte antigen 75 (ly75/CD205). Theriogenology, 113: 137–145, doi: https://doi.org/10.1016/j.theriogenology.2017.12.016

    Article  Google Scholar 

  • Zhao Chunyan, Xu Shihong, Feng Chengcheng, et al. 2018b. Characterization and differential expression of three GnRH forms during reproductive development in cultured turbot Schophthalmus maximus. Journal of Oceanology and Limnology, 36(4): 1360–1373, doi: https://doi.org/10.1007/s00343-018-7068-y

    Article  Google Scholar 

  • Zhao Chunyan, Xu Shihong, Liu Yifan, et al. 2017. Gonadogenesis analysis and sex differentiation in cultured turbot (Scophthalmus maximus). Fish Physiology and Biochemistry, 43(1): 265–278, doi: https://doi.org/10.1007/s10695-016-0284-5

    Article  Google Scholar 

  • Zhou Li, Wang Xueying, Liu Qinghua, et al. 2019. Visualization of turbot (Scophthalmus maximus) primordial germ cells in vivo using fluorescent protein mediated by the 3′ untranslated region of nanos3 or vasa gene. Marine Biotechnology, 21(5): 671–682, doi: https://doi.org/10.1007/s10126-019-09911-z

    Article  Google Scholar 

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Funding

The National Natural Science Foundation of China under contract Nos 31802319, 31972784 and 31802269; the Natural Science Foundation of Shandong Province under contract No. ZR2018BC053; the Agricultural Application Technology Innovation Project of Shandong Province under contract No. SD2019YY006; the Advanced Talents Foundation of Qingdao Agricultural University under contract Nos 6631119055 and 6631119032.

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Authors and Affiliations

  1. School of Marine Science and Engineering, Qingdao Agricultural University, Qingdao, 266109, China

    Chunyan Zhao, Bing Li, Yunliang Lu, Yanting Cui & Wenqi Wang

  2. College of Veterinary Medicine, Qingdao Agricultural University, Qingdao, 266109, China

    Liang Chi

  3. CAS Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China

    Yongshuang Xiao & Jun Li

  4. Marine Biology and Biotechnology Laboratory, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, 266237, China

    Yongshuang Xiao & Jun Li

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  1. Chunyan Zhao
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  2. Liang Chi
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  3. Yongshuang Xiao
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  4. Bing Li
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  5. Yunliang Lu
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  7. Wenqi Wang
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  8. Jun Li
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Correspondence to Wenqi Wang or Jun Li.

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Zhao, C., Chi, L., Xiao, Y. et al. Morphological and histological changes in the brains of turbot (Scophthalmus maximus) with gonadal development. Acta Oceanol. Sin. 41, 115–122 (2022). https://doi.org/10.1007/s13131-022-2041-1

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