Role of Thyroid Hormones in Adaptation to Volcanic Contamination of Freshwater Habitats in Charr of the Genus Salvelinus (Salmonidae)

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Abstract

The balance between phenotypic plasticity and adaptive specialization in response to environmental pressures remains a hot topic in evolutionary biology. In fish, one of the strongest impact factors is the chemical pollution of habitats. In an attempt to assess the consequences of heavy pollution of fresh waters for resident fishes, we studied Kamchatkan charr, which undergo paedomorphosis in the case of isolation in streams of volcanic areas contaminated with heavy metals. Experiments were carried out on the resistance of charr to metal mixtures during normal development and in six experimental groups with therapeutically altered intensity of metabolism and the secretory activity of thyroid gland. Water from volcanically contaminated streams was found to be lethally toxic for embryos and early juveniles of unadapted charr. The success of acclimation to toxic exposure was correlated with an increase in thyroid status. In experiments, the group with significantly elevated thyroid status showed a significant decrease in mortality and attenuation of oxidative stress in solutions of heavy metals. Under natural conditions, hyperthyroidism provokes a redistribution of the charr’s organism resources from somatic growth and morphological differentiation to stress counteracting and accelerated maturation, which is necessary for the long-term survival of the population under conditions of increased risk of individual mortality. Our experiments highlight the role of thyroid hormones in the rapid response to habitat pollution and the subsequent adaptation of fish populations to chronic deterioration.

About the authors

E. V. Esin

Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russia

Email: evgesin@gmail.com
Россия, Москва

E. V. Shulgina

Russian Federal Research Institute of Fisheries and Oceanography, Moscow, Russia

Email: evgesin@gmail.com
Россия, Москва

N. S. Pavlova

Lomonosov Moscow State University, Moscow, Russia

Email: evgesin@gmail.com
Россия, Москва

D. V. Zlenko

Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russia

Author for correspondence.
Email: evgesin@gmail.com
Россия, Москва

References

  1. Голованова И.Л. 2008. Влияние тяжелых металлов на физиолого-биохимический статус рыб и водных беспозвоночных // Биология внутр. вод. № 1. С. 99–108.
  2. Есин Е.В. 2017. Особенности биологии камчатской мальмы Salvelinus malma (Salmonidae) из нерестовых рек вулканических районов // Вопр. ихтиологии. Т. 57. № 2. С. 190–200. https://doi.org/10.7868/S0042875217010064
  3. Есин Е.В., Шульгина Е.В., Широков Д.А. и др. 2018. Физиологическая адаптация молоди гольца Salvelinus malma (Salmonidae) к обитанию в загрязненных реках вулканических территорий Камчатки // Биология внутр. вод. № 2. С. 57–69. https://doi.org/10.7868/S0320965218020079
  4. Лычкова А.Э. 2013. Нервная регуляция функции щитовидной железы // Вестн. РАМН. Т. 68. № 6. С. 49–55. https://doi.org/10.15690/vramn.v68i6.673
  5. Маркевич Г.Н., Есин Е.В. 2018. Эволюция гольцов рода Salvelinus (Salmonidae). 2. Симпатрическая внутриозёрная диверсификация (экологические черты и эволюционные механизмы с примерами из разных групп рыб) // Вопр. ихтиологии. Т. 58. № 3. С. 292–312. https://doi.org/10.7868/S0042875218030074
  6. Чалов С.Р., Есин Е.В. 2015. Принципы экологической классификации рек районов современного вулканизма // География и природ. ресурсы. № 1. С. 80–87.
  7. Birnie-Gauvin K., Bordeleau X., Cooke S.J. et al. 2021. Life-history strategies in salmonids: the role of physiology and its consequences // Biol. Rev. V. 96. № 5. P. 2304–2320. https://doi.org/10.1111/brv.12753
  8. Bleau H., Daniel C., Chevalier G. et al. 1996. Effects of acute exposure to mercury chloride and methylmercury on plasma cortisol, T3, T4, glucose and liver glycogen in rainbow trout (Oncorhynchus mykiss) // Aquat. Toxicol. V. 34. № 3. P. 221–235. https://doi.org/10.1016/0166-445X(95)00040-B
  9. Bolnick D.I., Fitzpatrick B.M. 2007. Sympatric speciation: models and empirical evidence // Annu. Rev. Ecol. Evol. Syst. V. 38. P. 459–487. https://doi.org/10.1146/annurev.ecolsys.38.091206.095804
  10. Brown S.B., Adams B.A., Cyr D.G., Eales J.G. 2004. Contaminant effects on the teleost fish thyroid // Environ. Toxicol. Chem. V. 23. № 7. P. 1680–1701. https://doi.org/10.1897/03-242
  11. Deal C.K., Volkoff H. 2020. The role of the thyroid axis in fish // Front. Endocrinol. V. 11. Article 596585. https://doi.org/10.3389/fendo.2020.596585
  12. Eliason E.J., Farrell A.P. 2015. Oxygen uptake in Pacific salmon Oncorhynchus spp.: when ecology and physiology meet // J. Fish Biol. V. 88. № 1. P. 359–388. https://doi.org/10.1111/jfb.12790
  13. Esin E.V., Markevich G.N., Shkil F.N. 2020. Rapid miniaturization of Salvelinus fish as an adaptation to the volcanic impact // Hydrobiologia. V. 847. № 13. P. 2947–2962. https://doi.org/10.1007/s10750-020-04296-w
  14. Esin E.V., Markevich G.N., Melnik N.O. et al. 2021a. Ambient temperature as a factor contributing to the developmental divergence in sympatric salmonids // PLoS ONE. V. 16. № 10. Article e0258536. https://doi.org/10.1371/journal.pone.0258536
  15. Esin E.V., Markevich G.N., Melnik N.O. et al. 2021b. Natural toxic impact and thyroid signaling interplay orchestrates riverine adaptive divergence of salmonid fish // J. Anim. Ecol. V. 90. № 4. P. 1004–1019. https://doi.org/10.1111/1365-2656.13429
  16. Eyckmans M., Celis N., Horemans N. et al. 2011. Exposure to waterborne copper reveals differences in oxidative stress response in three freshwater fish species // Aquat. Toxicol. V. 103. № 1–2. P. 112–120. https://doi.org/10.1016/j.aquatox.2011.02.010
  17. Gairin E., Dussenne M., Mercader M. et al. 2022. Harbours as unique environmental sites of multiple anthropogenic stresses on fish hormonal systems // Mol. Cell. Endocrinol. V. 555. Article 111727. https://doi.org/10.1016/j.mce.2022.111727
  18. Gorodilov Y.N. 1996. Description of the early ontogeny of the Atlantic salmon, Salmo salar, with a novel system of interval (state) identification // Environ. Biol. Fish. V. 47. № 2. P. 109–127. https://doi.org/10.1007/BF00005034
  19. Holzer G., Besson M., Lambert A. et al. 2017. Fish larval recruitment to reefs is a thyroid hormone-mediated metamorphosis sensitive to the pesticide chlorpyrifos // eLife. V. 6. Article e27595. https://doi.org/10.7554/eLife.27595
  20. Hontela A., Dumont P., Duclos D., Fortin R. 1995. Endocrine and metabolic dysfunction in yellow perch, Perca flavescens, exposed to organic contaminants and heavy metals in the St. Lawrence River // Environ. Toxicol. Chem. V. 14. № 4. P. 725–731. https://doi.org/10.1002/etc.5620140421
  21. Jancic S.A., Stosic B.Z. 2014. Cadmium effects on the thyroid gland // Vitam. Horm. V. 94. P. 391–425. https://doi.org/10.1016/B978-0-12-800095-3.00014-6
  22. Kar S., Sangem P., Anusha N., Senthilkumaran B. 2021. Endocrine disruptors in teleosts: evaluating environmental risks and biomarkers // Aquac. Fish. V. 6. № 1. P. 1–26. https://doi.org/10.1016/j.aaf.2020.07.013
  23. Klemetsen A. 2013. The most variable vertebrate on Earth // J. Ichthyol. V. 53. № 10. P. 781–791. https://doi.org/10.1134/S0032945213100044
  24. Kristjánsson B.K., Skúlason S., Snorrason S.S., Noakes D.L. 2012. Fine-scale parallel patterns in diversity of small benthic Arctic charr (Salvelinus alpinus) in relation to the ecology of lava/groundwater habitats // Ecol. Evol. V. 2. № 6. P. 1099–1112. https://doi.org/10.1002/ece3.235
  25. Lema S.C. 2020. Hormones, developmental plasticity, and adaptive evolution: endocrine flexibility as a catalyst for “plasticity-first” phenotypic divergence // Mol. Cell. Endocrinol. V. 502. Article 110678. https://doi.org/10.1016/j.mce.2019.110678
  26. McAninch E.A., Bianco A.C. 2014. Thyroid hormone signaling in energy homeostasis and energy metabolism // Ann. N. Y. Acad. Sci. V. 1311. № 1. P. 77–87. https://doi.org/10.1111/nyas.12374
  27. Müller G.B. 2021. Evo-devo’s contributions to the extended evolutionary synthesis // Evolutionary developmental biology. Cham: Springer. P. 1127–1138. https://doi.org/10.1007/978-3-319-32979-6_39
  28. Nosil P., Feder J.L. 2012. Genomic divergence during speciation: causes and consequences // Phil. Trans. R. Soc. B. V. 367. № 1587. P. 332–342. https://doi.org/10.1098/rstb.2011.0263
  29. Olsson P.-E., Kling P., Hogstrand C. 1998. Mechanisms of heavy metal accumulation and toxicity in fish // Metal metabolism in aquatic environments. Boston: Springer. P. 321–350. https://doi.org/10.1007/978-1-4757-2761-6_10
  30. Østbye K., Hassve M.H., Peris Tamayo A.-M.T. et al. 2020. “And if you gaze long into an abyss, the abyss gazes also into thee”: four morphs of Arctic charr adapting to a depth-gradient in Lake Tinnsjøen // Evol. Appl. V. 13. № 6. P. 1240–1261. https://doi.org/10.1111/eva.12983
  31. Salisbury S.J., Ruzzante D.E. 2022. Genetic causes and consequences of sympatric morph divergence in Salmonidae: a search for mechanisms // Annu. Rev. Anim. Biosci. V. 10. P. 81–106. https://doi.org/10.1146/annurev-animal-051021-080709
  32. Schlenk D., Handy R., Steinert S. et al. 2008. Biomarkers // The toxicology of fishes. Boca Raton: CRC Press. P. 683–733.
  33. Schluter D. 2000. The ecology of adaptive radiation. Oxford: OUP, 296 p.
  34. Seehausen O., Wagner C.E. 2014. Speciation in freshwater fishes // Annu. Rev. Ecol. Evol. Syst. V. 45. P. 621–651. https://doi.org/10.1146/annurev-ecolsys-120213-091818
  35. Skúlason S., Parsons K.J., Svanbäck R. et al. 2019. A way forward with eco evo devo: an extended theory of resource polymorphism with postglacial fishes as model systems // Biol. Rev. V. 94. № 5. P. 1786–1808. https://doi.org/10.1111/brv.12534
  36. Sreejith P., Oommen O.V. 2008. Tri-iodothyronine alters superoxide dismutase expression in a teleost Anabas testudineus // Indian J. Biochem. Biophys. V. 45. № 6. P. 393–398.
  37. Watson R.A., Mills R., Buckley C.L. et al. 2016. Evolutionary connectionism: algorithmic principles underlying the evolution of biological organisation in evo-devo, evo-eco and evolutionary transitions // Evol. Biol. V. 43. № 4. P. 553–581. https://doi.org/10.1007/s11692-015-9358-z
  38. Wollenberg Valero K.C., Marshall J.C., Bastiaans E. et al. 2019. Patterns, mechanisms and genetics of speciation in reptiles and amphibians // Genes. V. 10. № 9. Article 646. https://doi.org/10.3390/genes10090646

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Copyright (c) 2023 Е.В. Есин, Е.В. Шульгина, Н.С. Павлова, Д.В. Зленко

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