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Mathematical modelling to assess the impact of stress on temperature-dependent sex determination in teleost fish

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Abstract

Temperature-dependent sex determination (TSD) is an environmental phenomenon in which the temperature during the embryonic or larval stages influences the determination of sex. It is mainly observed in teleost fish, where high water temperatures can induce a female-to-male transition. The exact mechanism by which environmental changes affect TSD is poorly understood, but cortisol, a stress hormone, is considered a potential factor. Although excessive secretion of cortisol is known to cause side effects, it can lead to a switch in sex hormones, potentially resulting in TSD. In this paper, we investigate the mechanism of TSD in teleost fish. To assess the impact of stress caused by changes in water temperature on TSD, we established a mathematical model for hormonal dynamics that incorporates cortisol. First, we conducted a stability analysis to qualitatively examine the sex determination. The temperature dependence was modeled using the Eyring–Polanyi equation, and we examined corresponding hormonal changes with water temperature. Furthermore, we theoretically investigated the role of a cortisol inhibitor in preventing side effects during TSD.

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References

  1. Pen, I., Uller, T., Feldmeyer, B., Harts, A., While, G.M., Wapstra, E.: Climate-driven population divergence in sex-determining systems. Nature 468(7322), 436–438 (2010)

    Article  Google Scholar 

  2. Bull, J.J.: Sex determination in reptiles. Q. Rev. Biol. 55(1), 3–21 (1980)

    Article  Google Scholar 

  3. Ewert, M.A., Jackson, D.R., Nelson, C.E.: Patterns of temperature-dependent sex determination in turtles. J. Exp. Zool. 270(1), 3–15 (1994)

    Article  Google Scholar 

  4. Janzen, F.J., Paukstis, G.L.: Environmental sex determination in reptiles: ecology, evolution, and experimental design. Q. Rev. Biol. 66(2), 149–179 (1991)

    Article  Google Scholar 

  5. Lang, J.W., Andrews, H.V.: Temperature-dependent sex determination in crocodilians. J. Exp. Zool. 270(1), 28–44 (1994)

    Article  Google Scholar 

  6. Yamamoto, E.: Studies on sex-manipulation and production of cloned populations in hirame, Paralichthys olivaceus (Temminck et Schlegel). Aquaculture 173(1–4), 235–246 (1999)

    Article  Google Scholar 

  7. Kitano, T., Takamune, K., Kobayashi, T., Nagahama, Y., Abe, S.: Suppression of p450 aromatase gene expression in sex-reversed males produced by rearing genetically female larvae at a high water temperature during a period of sex differentiation in the Japanese flounder (Paralichthys olivaceus). J. Mol. Endocrinol. 23(2), 167–176 (1999)

    Article  Google Scholar 

  8. Kitano, T., Takamune, K., Nagahama, Y., Abe, S.-I.: Aromatase inhibitor and 17\(\alpha \)-methyltestosterone cause sex-reversal from genetical females to phenotypic males and suppression of p450 aromatase gene expression in japanese flounder (paralichthys olivaceus). Mol. Reprod. Dev. Incorp. Gamete Res. 56(1), 1–5 (2000)

    Article  Google Scholar 

  9. Yamaguchi, T., Yoshinaga, N., Yazawa, T., Gen, K., Kitano, T.: Cortisol is involved in temperature-dependent sex determination in the Japanese flounder. Endocrinology 151(8), 3900–3908 (2010)

    Article  Google Scholar 

  10. Hattori, R.S., Fernandino, J.I., Kishii, A., Kimura, H., Kinno, T., Oura, M., Somoza, G.M., Yokota, M., Strüssmann, C.A., Watanabe, S.: Cortisol-induced masculinization: does thermal stress affect gonadal fate in pejerrey, a teleost fish with temperature-dependent sex determination? PLoS ONE 4(8), 6548 (2009)

    Article  Google Scholar 

  11. García-Cruz, E.L., Yamamoto, Y., Hattori, R.S., Vasconcelos, L.M., Yokota, M., Strüssmann, C.A.: Crowding stress during the period of sex determination causes masculinization in pejerrey Odontesthes bonariensis, a fish with temperature-dependent sex determination. Compar. Biochem. Physiol. Part A Mol. Integr. Physiol. 245, 110701 (2020)

    Article  Google Scholar 

  12. Shen, Z.-G., Wang, H.-P.: Molecular players involved in temperature-dependent sex determination and sex differentiation in teleost fish. Genet. Sel. Evol. 46(1), 26 (2014)

    Article  Google Scholar 

  13. Todd, E.V., Liu, H., Muncaster, S., Gemmell, N.J.: Bending genders: the biology of natural sex change in fish. Sex. Dev. 10(5–6), 223–241 (2016)

    Article  Google Scholar 

  14. Pandian, T.: Environmental Sex Differentiation in Fish. CRC Press, Boca Raton (2014)

    Book  Google Scholar 

  15. Goikoetxea, A., Todd, E.V., Gemmell, N.J.: Stress and sex: does cortisol mediate sex change in fish? Reproduction 154(6), R149–R160 (2017)

    Article  Google Scholar 

  16. Whirledge, S., Cidlowski, J.A.: Glucocorticoids, stress, and fertility. Minerva Endocrinol. 35(2), 109 (2010)

    Google Scholar 

  17. Honeycutt, J., Deck, C., Miller, S., Severance, M., Atkins, E., Luckenbach, J., Buckel, J.A., Daniels, H.V., Rice, J., Borski, R., et al.: Warmer waters masculinize wild populations of a fish with temperature-dependent sex determination. Sci. Rep. 9(1), 6527 (2019)

    Article  Google Scholar 

  18. Yamaguchi, T., Yoshinaga, N., Yazawa, T., Gen, K., Kitano, T.: Cortisol is involved in temperature-dependent sex determination in the Japanese flounder. Endocrinology 151(8), 3900–3908 (2010)

    Article  Google Scholar 

  19. Yamaguchi, S.: Time required for sex change in teleost fishes: hormonal dynamics shaped by selection. J. Theor. Biol. 407, 339–348 (2016)

    Article  MathSciNet  Google Scholar 

  20. Yamaguchi, S., Iwasa, Y.: Temperature-dependent sex determination, realized by hormonal dynamics with enzymatic reactions sensitive to ambient temperature. J. Theor. Biol. 453, 146–155 (2018)

    Article  Google Scholar 

  21. Lienhard, G.E.: Enzymatic catalysis and transition-state theory. Science 180(4082), 149–154 (1973)

    Article  Google Scholar 

  22. Gulyamov, G., Erkaboev, U., Gulyamov, A.: Influence of temperature on the oscillations of longitudinal magnetoresistance in semiconductors with a nonparabolic dispersion law. Indian J. Phys. 93(5), 639–645 (2019)

    Article  Google Scholar 

  23. Gulyamov, G., Erkaboev, U., Gulyamov, A.: Magnetic quantum effects in electronic semiconductors at microwave-radiation absorption (2019)

  24. Erkaboev, U., Gulyamov, G., Mirzaev, J., Rakhimov, R., Sayidov, N.: Calculation of the fermi-dirac function distribution in two-dimensional semiconductor materials at high temperatures and weak magnetic fields. NANO 16(09), 2150102 (2021)

    Article  Google Scholar 

  25. Fostier, A., Jalabert, B., Billard, R., Breton, B., Zohar, Y.: 7 the gonadal steroids. In: Fish Physiology vol. 9, pp. 277–372. Elsevier, (1983)

  26. Stacey, N.: Hormones, pheromones and reproductive behavior. Fish Physiol. Biochem. 28, 229–235 (2003)

    Article  Google Scholar 

  27. Crews, D., Bergeron, J.M., Bull, J.J., Flores, D., Tousignant, A., Skipper, J.K., Wibbels, T.: Temperature-dependent sex determination in reptiles: proximate mechanisms, ultimate outcomes, and practical applications. Dev. Genet. 15(3), 297–312 (1994)

    Article  Google Scholar 

  28. Crews, D.: Temperature-dependent sex determination: the interplay of steroid hormones and temperature. Zoolog. Sci. 13(1), 1–13 (1996)

    Article  MathSciNet  Google Scholar 

  29. Guiguen, Y., Fostier, A., Piferrer, F., Chang, C.-F.: Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish. Gen. Comp. Endocrinol. 165(3), 352–366 (2010)

    Article  Google Scholar 

  30. LaSalle, J.P.: The Stability of Dynamical Systems, vol. 25. SIAM, New Delhi (1976)

    Book  Google Scholar 

  31. Li, M.Y., Muldowney, J.S.: A geometric approach to global-stability problems. SIAM J. Math. Anal. 27(4), 1070–1083 (1996)

    Article  MathSciNet  Google Scholar 

  32. Freedman, H.I., Ruan, S., Tang, M.: Uniform persistence and flows near a closed positively invariant set. J. Dyn. Diff. Equat. 6(4), 583–600 (1994)

    Article  MathSciNet  Google Scholar 

  33. Takahashi, H., Sakamoto, T., Hyodo, S., Shepherd, B.S., Kaneko, T., Grau, E.G.: Expression of glucocorticoid receptor in the intestine of a euryhaline teleost, the mozambique tilapia (Oreochromis mossambicus): effect of seawater exposure and cortisol treatment. Life Sci. 78(20), 2329–2335 (2006)

    Article  Google Scholar 

  34. Chrousos, G.P., Detera-Wadleigh, S.D., Karl, M.: Syndromes of glucocorticoid resistance. Ann. Intern. Med. 119(11), 1113–1124 (1993)

    Article  Google Scholar 

  35. Maule, A.G., Schreck, C.B., Kaattari, S.L.: Changes in the immune system of coho salmon (Oncorhynchus kisutch) during the Parr-to-Smolt transformation and after implantation of cortisol. Can. J. Fish. Aquat. Sci. 44(1), 161–166 (1987)

    Article  Google Scholar 

  36. Hur, J.W., Lim, H.K., Chang, Y.J.: Effects of repetitive temperature changes on the stress response and growth of olive flounder, Paralichthys olivaceus. J. Appl. Anim. Res. 33(1), 49–54 (2008)

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (2022R1A5A1033624 and RS-2023-00210403).

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Authors and Affiliations

  1. Department of Mathematics, College of Natural Sciences, Pusan National University, Busan, 46241, South Korea

    Jong Hyuk Byun & Il Hyo Jung

  2. Interdisplinary Biology Laboratory (iBLab), Division of Natural Science, Graduate School of Science, Nagoya University, Nagoya, 4648602, Japan

    Yong Dam Jeong

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Byun, J.H., Jung, I.H. & Jeong, Y.D. Mathematical modelling to assess the impact of stress on temperature-dependent sex determination in teleost fish. J. Appl. Math. Comput. 70, 997–1021 (2024). https://doi.org/10.1007/s12190-024-01988-7

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