journal article Oct 01, 2023

Rapid hyperthyroidism-induced adaptation of salmonid fish in response to environmental pollution

View at Publisher Save 10.1111/jeb.14220
Abstract
Abstract
The streams draining volcanic landscapes are often characterized by a complex series of factors that negatively affect hydrobionts and lead to declines in their populations. However, in a number of cases, a range of rapid adaptive changes ensure the resilience of hydrobiont populations. Here, we present both field and experimental data shedding light on the physiological basis of adaptation to heavy metal contamination in populations of Dolly Varden charr (Salvelinus malma) differing in duration of isolation in volcanic streams. The study reveals that isolated populations have a physiological phenotype that distinguishes them from populations inhabiting clean waters. They are characterized by a hyperthyroid status accompanied by an increased metabolic rate, elevated activity of antioxidant enzymes, decreased ionic conductivity of tissues and reduced stored energy reserves. Our experimental data reveal that hyperthyroidism is an adaptive characteristic enhancing the resistance to heavy metal contamination and shaping the evolution of these populations. The similarity of physiological, developmental and morphological changes in isolated populations suggests a common source and mechanisms underpinning this case of ‘evolutionary rescue’. Thus, populations of S. malma trapped in volcanic streams represent a genuine case of rapid endocrine-driven adaptation to changing environmental stimuli.
Abstract
Volcanic heavy metal pollution leads to severe oxidative stress in landlocked fish populations. We found that fish can rapidly develop toxicosis resistance via adaptive physiological and developmental shifts. Alterations of pituitary–thyroid axis activity underlie these adaptive transformations. Thus, neurally driven endocrine changes provide an evolutionary rescue for fish.
Topics

No keywords indexed for this article. Browse by subject →

References
76
[1]
Atli "Essential metal (Cu, Zn) exposures alter the activity of ATPases in gill, kidney and muscle of Tilapia Oreochromis niloticus" Ecotoxicology (2011) 10.1007/s10646-011-0724-z
[2]
Bell "Evolutionary rescue" Annual Review of Ecology, Evolution, and Systematics (2017) 10.1146/annurev-ecolsys-110316-023011
[3]
Birnie-Gauvin "Life-history strategies in salmonids: The role of physiology and its consequences" Biological Reviews (2021) 10.1111/brv.12753
[4]
Bleau "Effects of acute exposure to mercury chloride and methylmercury on plasma cortisol, T3, T4, glucose, and liver glycogen in rainbow trout (Oncorhynchus mykiss)" Aquatic Toxicology (1996) 10.1016/0166-445x(95)00040-b
[5]
Blong (1984)
[6]
Bolotovskiy "Heterochronic development of lateral plates in the three-spined stickleback induced by thyroid hormone level alterations" PLoS One (2018) 10.1371/journal.pone.0194040
[7]
Brix "Adverse outcome pathways for chronic copper toxicity to fish and amphibians" Environmental Toxicology and Chemistry (2022) 10.1002/etc.5483
[8]
Brix "Investigations into the mechanism of lead toxicity to the freshwater pulmonate snail, Lymnaea stagnalis" Aquatic Toxicology (2012) 10.1016/j.aquatox.2011.11.007
[9]
[10]
Brown "Contaminant effects on the teleost fish thyroid" Environmental Toxicology and Chemistry (2004) 10.1897/03-242
[11]
Brown "The calculation of the acute toxicity of mixtures of poisons to rainbow trout" Water Research (1968) 10.1016/0043-1354(68)90044-4
[12]
Cabej (2018)
[13]
Campinho "Teleost metamorphosis: The role of thyroid hormone" Frontiers in Endocrinology (2019) 10.3389/fendo.2019.00383
[14]
Carlson "Evolutionary rescue in a changing world" Trends in Ecology & Evolution (2014) 10.1016/j.tree.2014.06.005
[15]
Chalov "The principles of ecological classification of rivers in areas of contemporary volcanism (exemplified by Kamchatka)" Geography and Natural Resources (2015) 10.1134/s1875372815010096
[16]
Chu "Synergistic toxicity of multiple heavy metals is revealed by a biological assay using a nematode and its transgenic derivative" Aquatic Toxicology (2002) 10.1016/s0166-445x(02)00017-6
[17]
Dale (2018)
[18]
Deal "The role of the thyroid axis in fish" Frontiers in Endocrinology (2020) 10.3389/fendo.2020.596585
[19]
del Moral (1999)
[20]
Eales "The relationship between ingested thyroid hormones, thyroid homeostasis and iodine metabolism in humans and teleost fish" General and Comparative Endocrinology (2019) 10.1016/j.ygcen.2019.04.012
[21]
Eisler (1993)
[22]
Eliason "Oxygen uptake in Pacific Salmon oncorhynchus spp.: When ecology and physiology meet" Journal of Fish Biology (2015)
[23]
Esin "On the Dolly Varden's Salvelinus malma (Salmonidae) biology in Kamchatkan spawning rivers of the volcanic areas" Journal of Ichthyology (2017) 10.1134/s0032945217010040
[24]
Esin "Natural toxic impact and thyroid signaling interplay orchestrates riverine adaptive divergence of salmonid fish" Journal of Animal Ecology (2021) 10.1111/1365-2656.13429
[25]
Esin "Rapid miniaturization of Salvelinus fish as an adaptation to the volcanic impact" Hydrobiologia (2020) 10.1007/s10750-020-04296-w
[26]
Esin "Unspecific histological and hematological alterations in anadromous and resident Salvelinus malma induced by volcanogenic pollution" Hydrobiologia (2018) 10.1007/s10750-018-3687-8
[27]
Esin "Physiological adaptations in juvenile Dolly Varden Salvelinus malma (Salmonidae) dwelling in polluted rivers of Kamchatkan volcanic territories" Inland Water Biology (2018) 10.1134/s1995082918020049
[28]
Eyckmans "Exposure to waterborne copper reveals differences in oxidative stress response in three freshwater fish species" Aquatic Toxicology (2011) 10.1016/j.aquatox.2011.02.010
[29]
Finlayson "Toxicities of copper, zinc, and cadmium mixtures to juvenile Chinook salmon" Transactions of the American Fisheries Society (1982) 10.1577/1548-8659(1982)111<645:toczac>2.0.co;2
[30]
A SIMPLE METHOD FOR THE ISOLATION AND PURIFICATION OF TOTAL LIPIDES FROM ANIMAL TISSUES

Jordi Folch, M. Lees, G.H. Sloane Stanley

Journal of Biological Chemistry 1957 10.1016/s0021-9258(18)64849-5
[31]
Gairin "Harbours as unique environmental sites of multiple anthropogenic stresses on fish hormonal systems" Molecular and Cellular Endocrinology (2022) 10.1016/j.mce.2022.111727
[32]
Gavrilov "Analysis of methods for determination of lipid peroxidation products in blood serum in the thiobarbituric acid test" Voprosi Medicinskoy Khimii (1987)
[33]
Golovanova "Effects of heavy metals on the physiological and biochemical status of fishes and aquatic invertebrates" Inland Water Biology (2008) 10.1007/s12212-008-1014-1
[34]
Gould (1977)
[35]
Hanken "Miniaturization of body size: Organismal consequences and evolutionary significance" Annual Review of Ecology and Systematics (1993) 10.1146/annurev.es.24.110193.002441
[36]
Holzer "Fish larval recruitment to reefs is a thyroid hormone-mediated metamorphosis sensitive to the pesticide chlorpyrifos" eLife Sciences (2017) 10.7554/elife.27595
[37]
Hontela "Endocrine and metabolic dysfunction in yellow perch, Perca flavescens, exposed to organic contaminants and heavy metals in the St. Lawrence River" Environmental Toxicology and Chemistry: An International Journal (1995) 10.1002/etc.5620140421
[38]
Ince "Assessment of toxic interactions of heavy metals in binary mixtures: A statistical approach" Archives of Environmental Contamination and Toxicology (1999) 10.1007/pl00006607
[39]
Jaishankar "Toxicity, mechanism and health effects of some heavy metals" Interdisciplinary Toxicology (2014) 10.2478/intox-2014-0009
[40]
Jancic "Cadmium effects on the thyroid gland" Vitamins and Hormones (2014) 10.1016/b978-0-12-800095-3.00014-6
[41]
Johnston (2002)
[42]
Kar "Endocrine disruptors in teleosts: Evaluating environmental risks and biomarkers" Aquaculture and Fisheries (2021) 10.1016/j.aaf.2020.07.013
[43]
Khanam "Impact of zinc on thyroid metabolism" Journal of Diabetes, Metabolic Disorders & Control (2018) 10.15406/jdmdc.2018.05.00134
[44]
Kitano "Adaptive divergence in the thyroid hormone signaling pathway in the stickleback radiation" Current Biology (2010) 10.1016/j.cub.2010.10.050
[45]
Kodama "Acute toxicity of zinc to rainbow trout Salmo gairdneri" Bulletin of the Japanese Society for the Science of Fish (1982) 10.2331/suisan.48.1055
[46]
Koroluk "A method for determination of catalase activity" Laboratornoe Delo (1988)
[47]
Kottelat "Paedocypris, a new genus of southeast Asian cyprinid fish with a remarkable sexual dimorphism, comprises the world's smallest vertebrate" Proceedings of the Royal Society B (2006) 10.1098/rspb.2005.3419
[48]
Laudet "The origins and evolution of vertebrate metamorphosis" Current Biology (2011) 10.1016/j.cub.2011.07.030
[49]
Lee "Sustained miniaturization and anatomical innovation in the dinosaurian ancestors of birds" Science (2014) 10.1126/science.1252243
[50]
Lema "Hormones, developmental plasticity, and adaptive evolution: Endocrine flexibility as a catalyst for ‘plasticity-first’ phenotypic divergence" Molecular and Cellular Endocrinology (2020) 10.1016/j.mce.2019.110678

Showing 50 of 76 references

Metrics
4
Citations
76
References
Details
Published
Oct 01, 2023
Vol/Issue
36(10)
Pages
1471-1483
License
View
Funding
Russian Science Foundation Award: 22-24-00724
Cite This Article
Evgeny V. Esin, Elena V. Shulgina, Fedor N. Shkil (2023). Rapid hyperthyroidism-induced adaptation of salmonid fish in response to environmental pollution. Journal of Evolutionary Biology, 36(10), 1471-1483. https://doi.org/10.1111/jeb.14220