Volume 44 Issue 4
Jul.  2023
Turn off MathJax
Article Contents
Jiang-Hui Zhang, Rui Long, Yang-Yang Jing, Pan Zhang, Yuan Xu, Wei Xiong, Yan-Qiu Zhu, Yi-Ping Luo. Loss of behavioral stress response in blind cavefish reduces energy expenditure. Zoological Research, 2023, 44(4): 678-692. doi: 10.24272/j.issn.2095-8137.2022.354
Citation: Jiang-Hui Zhang, Rui Long, Yang-Yang Jing, Pan Zhang, Yuan Xu, Wei Xiong, Yan-Qiu Zhu, Yi-Ping Luo. Loss of behavioral stress response in blind cavefish reduces energy expenditure. Zoological Research, 2023, 44(4): 678-692. doi: 10.24272/j.issn.2095-8137.2022.354

Loss of behavioral stress response in blind cavefish reduces energy expenditure

doi: 10.24272/j.issn.2095-8137.2022.354
Data related to this paper have been deposited in Figshare: https://doi.org/10.6084/m9.figshare.20781154.v2.
Supplementary data to this article can be found online.
The authors declare that they have no competing interests.
J.H.Z. and Y.P.L. conceived the ideas and designed the methodology; J.H.Z., R.L., Y.Y.J., P.Z., Y.X., W.X., and Y.Q.Z. collected the data; J.H.Z. analyzed the data and drafted the manuscript. Y.P.L. critically reviewed the manuscript. All authors read and approved the final version of the manuscript.
Funds:  This study was supported by the National Natural Science Foundation of China (32070438)
More Information
  • Corresponding author: E-mail: luoguo@swu.edu.cn
  • Received Date: 2023-03-03
  • Accepted Date: 2023-04-27
  • Published Online: 2023-04-28
  • Publish Date: 2023-07-18
  • The stress response is essential for animal self-defense and survival. However, species may exhibit stress response variation depending on their specific environmental and selection pressures. Blind cavefish dwell in cave environments, which differ markedly in stressors and resource availability compared to surface aquatic environments. However, whether blind cavefish exhibit differences in stress response as an adaptation to their cave environments remains unclear. Here, we investigated differences in stress response in six closely related Triplophysa species, including three blind cavefish (T. longibarbata, T. jiarongensis, and T. rosa) and three normal-sighted river fish (T. nasobarbatula, T. dongsaiensis, and T. bleekeri). Results showed that blind cavefish exhibited a range of distinct behavioral responses compared to sighted river fish, including greater levels of activity, shorter duration of freezing, absence of erratic movements or thrashing behavior, and opposite behavioral trends over time. Furthermore, the cavefish species demonstrated attenuated increases in metabolic rate in response to stressors related to novel environments. Cave-dwelling T. rosa also exhibited lower basal hypothalamic-pituitary-inter-renal (HPI) axis-related gene expression levels and stress hormone concentrations compared to river-dwelling T. bleekeri. These results suggest that blind cavefish may have lost their behavioral stress response, potentially mediated by a reduction in basal activity of the HPI axis, thus enabling the conservation of energy by reducing unnecessary expenditure in energy-limited caves.
  • Data related to this paper have been deposited in Figshare: https://doi.org/10.6084/m9.figshare.20781154.v2.
    Supplementary data to this article can be found online.
    The authors declare that they have no competing interests.
    J.H.Z. and Y.P.L. conceived the ideas and designed the methodology; J.H.Z., R.L., Y.Y.J., P.Z., Y.X., W.X., and Y.Q.Z. collected the data; J.H.Z. analyzed the data and drafted the manuscript. Y.P.L. critically reviewed the manuscript. All authors read and approved the final version of the manuscript.
  • loading
  • [1]
    Alfonso S, Zupa W, Manfrin A, et al. 2020. Stress coping styles: Is the basal level of stress physiological indicators linked to behaviour of sea bream?. Applied Animal Behaviour Science, 231: 105085. doi: 10.1016/j.applanim.2020.105085
    [2]
    Alsop D, Vijayan MM. 2008. Development of the corticosteroid stress axis and receptor expression in zebrafish. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 294(3): R711−R719. doi: 10.1152/ajpregu.00671.2007
    [3]
    Barton BA. 2002. Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integrative and Comparative Biology, 42(3): 517−525. doi: 10.1093/icb/42.3.517
    [4]
    Bates D, Mächler M, Bolker B, et al. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1): 1−48.
    [5]
    Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society:Series B (Methodological), 57(1): 289−300. doi: 10.1111/j.2517-6161.1995.tb02031.x
    [6]
    Bijlsma R, Loeschcke V. 2005. Environmental stress, adaptation and evolution: an overview. Journal of Evolutionary Biology, 18(4): 744−749. doi: 10.1111/j.1420-9101.2005.00962.x
    [7]
    Blaser R, Gerlai R. 2006. Behavioral phenotyping in zebrafish: Comparison of three behavioral quantification methods. Behavior Research Methods, 38(3): 456−469. doi: 10.3758/BF03192800
    [8]
    Bonga SEW. 1997. The stress response in fish. Physiological Reviews, 77(3): 591−625. doi: 10.1152/physrev.1997.77.3.591
    [9]
    Brandon RN. 1978. Adaptation and evolutionary theory. Studies in History and Philosophy of Science Part A, 9(3): 181−206. doi: 10.1016/0039-3681(78)90005-5
    [10]
    Breed MD, Moore J. 2015. Animal behavior. In: Carter M, Shieh J. Guide to Research Techniques in Neuroscience. Amsterdam: Elsevier, 39–71.
    [11]
    Burnham KP, Anderson DR. 2004. Multimodel inference: Understanding AIC and BIC in model selection. Sociological Methods & Research, 33(2): 261−304.
    [12]
    Burnham KP, Anderson DR, Huyvaert KP. 2011. AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behavioral Ecology and Sociobiology, 65(1): 23−35. doi: 10.1007/s00265-010-1029-6
    [13]
    Carbillet J, Rey B, Palme R, et al. 2022. Covariation between glucocorticoids, behaviour and immunity supports the pace-of-life syndrome hypothesis: an experimental approach. Proceedings of the Royal Society B:Biological Sciences, 289(1975): 20220464. doi: 10.1098/rspb.2022.0464
    [14]
    Careau V, Thomas D, Humphries MM, et al. 2008. Energy metabolism and animal personality. Oikos, 117(5): 641−653. doi: 10.1111/j.0030-1299.2008.16513.x
    [15]
    Chabot D, Steffensen JF, Farrell AP. 2016. The determination of standard metabolic rate in fishes. Journal of Fish Biology, 88(1): 81−121. doi: 10.1111/jfb.12845
    [16]
    Chin JSR, Gassant CE, Amaral PM, et al. 2018. Convergence on reduced stress behavior in the Mexican blind cavefish. Developmental Biology, 441(2): 319−327. doi: 10.1016/j.ydbio.2018.05.009
    [17]
    Chin JSR, Loomis CL, Albert LT, et al. 2020. Analysis of stress responses in Astyanax larvae reveals heterogeneity among different populations. Journal of Experimental Zoology B: Molecular and Developmental Evolution, 334(7–8): 486–496.
    [18]
    Conrad JL, Weinersmith KL, Brodin T, et al. 2011. Behavioural syndromes in fishes: a review with implications for ecology and fisheries management. Journal of Fish Biology, 78(2): 395−435. doi: 10.1111/j.1095-8649.2010.02874.x
    [19]
    Demin KA, Taranov AS, Ilyin NP, et al. 2021. Understanding neurobehavioral effects of acute and chronic stress in zebrafish. Stress, 24(1): 1−18. doi: 10.1080/10253890.2020.1724948
    [20]
    Duboué ER, Hong E, Eldred KC, et al. 2017. Left habenular activity attenuates fear responses in larval zebrafish. Current Biology, 27(14): 2154−2162.e3. doi: 10.1016/j.cub.2017.06.017
    [21]
    Ellis T, Yildiz HY, López-Olmeda J, et al. 2012. Cortisol and finfish welfare. Fish Physiology and Biochemistry, 38(1): 163−188. doi: 10.1007/s10695-011-9568-y
    [22]
    Faught E, Vijayan MM. 2016. Mechanisms of cortisol action in fish hepatocytes. Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology, 199: 136−145. doi: 10.1016/j.cbpb.2016.06.012
    [23]
    Feng CG, Tong C, Zhang RY, et al. 2017. Biodiversity and distribution patterns of Triplophysa species in the northeastern margin of the Tibetan Plateau. Biodiversity Science, 25(1): 53−61. (in Chinese)
    [24]
    Freckleton RP, Harvey PH, Pagel M. 2002. Phylogenetic analysis and comparative data: a test and review of evidence. The American Naturalist, 160(6): 712−726. doi: 10.1086/343873
    [25]
    Gibert J, Deharveng L. 2002. Subterranean ecosystems: A truncated functional biodiversity: This article emphasizes the truncated nature of subterranean biodiversity at both the bottom (no primary producers) and the top (very few strict predators) of food webs and discusses the implications of this truncation both from functional and evolutionary perspectives. BioScience, 52(6): 473−481. doi: 10.1641/0006-3568(2002)052[0473:SEATFB]2.0.CO;2
    [26]
    Godwin J, Sawyer S, Perrin F, et al. 2012. Adapting the open field test to assess anxiety-related behavior in zebrafish. In: Kalueff AV, Stewart AM. Zebrafish Protocols for Neurobehavioral Research, Neuromethods. Totowa: Humana Press, 181–189.
    [27]
    Gormally BMG, Romero LM. 2020. What are you actually measuring? A review of techniques that integrate the stress response on distinct time-scales. Functional Ecology, 34(10): 2030−2044. doi: 10.1111/1365-2435.13648
    [28]
    Gould TD, Dao DT, Kovacsics CE. 2009. The open field test. In: Gould TD. Mood and Anxiety Related Phenotypes in Mice: Characterization Using Behavioral Tests. Totowa: Humana Press, 1–20.
    [29]
    Harianto J, Carey N, Byrne M. 2019. respR—An R package for the manipulation and analysis of respirometry data. Methods in Ecology and Evolution, 10(6): 912−920. doi: 10.1111/2041-210X.13162
    [30]
    Heinen-Kay JL, Langerhans RB. 2013. Predation-associated divergence of male genital morphology in a livebearing fish. Journal of Evolutionary Biology, 26(10): 2135−2146. doi: 10.1111/jeb.12229
    [31]
    Huang J, Peng ZG, Wang ZJ. 2013. Comparison of the gross anatomy of the brains between Triplophysa bleekeri and Triplophysa rosa. Journal of Southwest China Normal University (Natural Science Edition), 38(3): 94–100. (in Chinese)
    [32]
    Hurlimann ML, Martin JGA, Bize P. 2019. Evidence of phenotypic correlation between exploration activity and resting metabolic rate among populations across an elevation gradient in a small rodent species. Behavioral Ecology and Sociobiology, 73(9): 131. doi: 10.1007/s00265-019-2740-6
    [33]
    Jeffery WR. 2005. Adaptive evolution of eye degeneration in the Mexican blind cavefish. Journal of Heredity, 96(3): 185−196. doi: 10.1093/jhered/esi028
    [34]
    Jiang DL, Wu YB, Huang D, et al. 2017. Effects of nutritional history on stress response in gibel carp (Carassius auratus gibelio) and largemouth bass (Micropterus salmoides). Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology, 210: 9−17. doi: 10.1016/j.cbpb.2017.05.002
    [35]
    Kalueff AV, Gebhardt M, Stewart AM, et al. 2013. Towards a comprehensive catalog of zebrafish behavior 1.0 and beyond. Zebrafish, 10(1): 70−86. doi: 10.1089/zeb.2012.0861
    [36]
    Killen SS, Christensen EAF, Cortese D, et al. 2021. Guidelines for reporting methods to estimate metabolic rates by aquatic intermittent-flow respirometry. Journal of Experimental Biology, 224(18): jeb242522. doi: 10.1242/jeb.242522
    [37]
    Killen SS, Marras S, Metcalfe NB, et al. 2013. Environmental stressors alter relationships between physiology and behaviour. Trends in Ecology & Evolution, 28(11): 651−658.
    [38]
    Kimura M, Ota T. 1971. Theoretical aspects of population genetics. Monographs in Population Biology, 4: 1−219.
    [39]
    Koolhaas JM, De Boer SF, Buwalda B, et al. 2007. Individual variation in coping with stress: a multidimensional approach of ultimate and proximate mechanisms. Brain, Behavior and Evolution, 70(4): 218−226. doi: 10.1159/000105485
    [40]
    Koolhaas JM, De Boer SF, Coppens CM, et al. 2010. Neuroendocrinology of coping styles: Towards understanding the biology of individual variation. Frontiers in Neuroendocrinology, 31(3): 307−321. doi: 10.1016/j.yfrne.2010.04.001
    [41]
    Koolhaas JM, Korte SM, De Boer SF, et al. 1999. Coping styles in animals: current status in behavior and stress-physiology. Neuroscience & Biobehavioral Reviews, 23(7): 925−935.
    [42]
    Kowalko JE, Rohner N, Rompani SB, et al. 2013. Loss of schooling behavior in cavefish through sight-dependent and sight-independent mechanisms. Current Biology, 23(19): 1874−1883. doi: 10.1016/j.cub.2013.07.056
    [43]
    Krishnan J, Rohner N. 2017. Cavefish and the basis for eye loss. Philosophical Transactions of the Royal Society B:Biological Sciences, 372(1713): 20150487. doi: 10.1098/rstb.2015.0487
    [44]
    Kültz D. 2005. Molecular and evolutionary basis of the cellular stress response. Annual Review of Physiology, 67: 225−257. doi: 10.1146/annurev.physiol.67.040403.103635
    [45]
    Lan JH, Gan X, Wu TJ, et al. 2013. Cave Fishes of Guangxi, China. Beijing: Science Press. (in Chinese)
    [46]
    Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the $2^{-\Delta\Delta {C_T}} $ 2-ddct method. Methods, 25(4): 402−408. doi: 10.1006/meth.2001.1262
    [47]
    Martins CIM, Castanheira MF, Engrola S, et al. 2011. Individual differences in metabolism predict coping styles in fish. Applied Animal Behaviour Science, 130(3–4): 135–143.
    [48]
    Mathot KJ, Dingemanse NJ, Nakagawa S. 2019. The covariance between metabolic rate and behaviour varies across behaviours and thermal types: meta-analytic insights. Biological Reviews, 94(3): 1056−1074. doi: 10.1111/brv.12491
    [49]
    Matsunaga W, Watanabe E. 2010. Habituation of medaka (Oryzias latipes) demonstrated by open-field testing. Behavioural Processes, 85(2): 142−150. doi: 10.1016/j.beproc.2010.06.019
    [50]
    Moberg GP, Mench JA. 2000. The Biology of Animal Stress: Basic Principles and Implications for Animal Welfare. New York: CABI Pub.
    [51]
    Moran D, Softley R, Warrant EJ. 2014. Eyeless Mexican cavefish save energy by eliminating the circadian rhythm in metabolism. PLoS One, 9(9): e107877. doi: 10.1371/journal.pone.0107877
    [52]
    Moran NP, Sánchez-Tójar A, Schielzeth H, et al. 2021. Poor nutritional condition promotes high-risk behaviours: a systematic review and meta-analysis. Biological Reviews, 96(1): 269−288. doi: 10.1111/brv.12655
    [53]
    Nesan D, Kamkar M, Burrows J, et al. 2012. Glucocorticoid receptor signaling is essential for mesoderm formation and muscle development in zebrafish. Endocrinology, 153(3): 1288−1300. doi: 10.1210/en.2011-1559
    [54]
    Patton P, Windsor S, Coombs S. 2010. Active wall following by Mexican blind cavefish (Astyanax mexicanus). Journal of Comparative Physiology A, 196(11): 853−867. doi: 10.1007/s00359-010-0567-8
    [55]
    Petitjean Q, Jean S, Gandar A, et al. 2019. Stress responses in fish: From molecular to evolutionary processes. Science of the Total Environment, 684: 371−380. doi: 10.1016/j.scitotenv.2019.05.357
    [56]
    Peuß R, Box AC, Chen SY, et al. 2020. Adaptation to low parasite abundance affects immune investment and immunopathological responses of cavefish. Nature Ecology & Evolution, 4(10): 1416−1430.
    [57]
    Pierre C, Pradère N, Froc C, et al. 2020. A mutation in monoamine oxidase (MAO) affects the evolution of stress behavior in the blind cavefish Astyanax mexicanus. Journal of Experimental Biology, 223(18): jeb226092.
    [58]
    Pikulkaew S, Benato F, Celeghin A, et al. 2011. The knockdown of maternal glucocorticoid receptor mRNA alters embryo development in zebrafish. Developmental Dynamics, 240(4): 874−889. doi: 10.1002/dvdy.22586
    [59]
    Prut L, Belzung C. 2003. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. European Journal of Pharmacology, 463(1–3): 3–33.
    [60]
    R Core Team. 2021. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria.
    [61]
    Réale D, Dingemanse NJ, Kazem AJN, et al. 2010. Evolutionary and ecological approaches to the study of personality. Philosophical Transactions of the Royal Society B:Biological Sciences, 365(1560): 3937−3946. doi: 10.1098/rstb.2010.0222
    [62]
    Rendahl H. 1933. Studien über innerasiatische Fische. Arkiv Fö r Zoologi Stockholm, 25A(11): 1−51.
    [63]
    Revell LJ. 2012. Phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3(2): 217−223. doi: 10.1111/j.2041-210X.2011.00169.x
    [64]
    Riddle MR, Aspiras AC, Gaudenz K, et al. 2018. Insulin resistance in cavefish as an adaptation to a nutrient-limited environment. Nature, 555(7698): 647−651. doi: 10.1038/nature26136
    [65]
    Sanders BM. 1993. Stress proteins in aquatic organisms: an environmental perspective. Critical Reviews in Toxicology, 23(1): 49−75. doi: 10.3109/10408449309104074
    [66]
    Sapolsky RM, Romero LM, Munck AU. 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews, 21(1): 55−89.
    [67]
    Schreck CB, Tort L. 2016. The concept of stress in fish. Fish Physiology, 35: 1−34.
    [68]
    Schulte PM. 2014. What is environmental stress? Insights from fish living in a variable environment. Journal of Experimental Biology, 217(1): 23−34. doi: 10.1242/jeb.089722
    [69]
    Shams S, Seguin D, Facciol A, et al. 2017. Effect of social isolation on anxiety-related behaviors, cortisol, and monoamines in adult zebrafish. Behavioral Neuroscience, 131(6): 492−504. doi: 10.1037/bne0000220
    [70]
    Shi CC, Yao M, Lv X, et al. 2018. Body and organ metabolic rates of a cave fish, Triplophysa rosa: influence of light and ontogenetic variation. Journal of Comparative Physiology B, 188(6): 947−955. doi: 10.1007/s00360-018-1178-x
    [71]
    Sih A, Bell AM, Johnson JC, et al. 2004. Behavioral syndromes: an integrative overview. The Quarterly Review of Biology, 79(3): 241−277. doi: 10.1086/422893
    [72]
    Snyder S, Nadler LE, Bayley JS, et al. 2016. Effect of closed v. intermittent-flow respirometry on hypoxia tolerance in the shiner perch Cymatogaster aggregata. Journal of Fish Biology, 88(1): 252–264.
    [73]
    Sokolova IM. 2013. Energy-limited tolerance to stress as a conceptual framework to integrate the effects of multiple stressors. Integrative and Comparative Biology, 53(4): 597−608. doi: 10.1093/icb/ict028
    [74]
    Sokolova IM, Frederich M, Bagwe R, et al. 2012. Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Marine Environmental Research, 79: 1−15. doi: 10.1016/j.marenvres.2012.04.003
    [75]
    Svendsen MBS, Bushnell PG, Steffensen JF. 2016. Design and setup of intermittent-flow respirometry system for aquatic organisms. Journal of Fish Biology, 88(1): 26−50. doi: 10.1111/jfb.12797
    [76]
    Tabin JA, Aspiras A, Martineau B, et al. 2018. Temperature preference of cave and surface populations of Astyanax mexicanus. Developmental Biology, 441(2): 338–344.
    [77]
    Tsalafouta A, Papandroulakis N, Gorissen M, et al. 2014. Ontogenesis of the HPI axis and molecular regulation of the cortisol stress response during early development in Dicentrarchus labrax. Scientific Reports, 4(1): 5525.
    [78]
    Tsalafouta A, Sarropoulou E, Papandroulakis N, et al. 2018. Characterization and expression dynamics of key genes involved in the gilthead sea bream (Sparus aurata) cortisol stress response during early ontogeny. Marine Biotechnology, 20(5): 611−622. doi: 10.1007/s10126-018-9833-5
    [79]
    Volavka J, Bilder R, Nolan K. 2004. Catecholamines and aggression: the role of COMT and MAO polymorphisms. Annals of the New York Academy of Sciences, 1036(1): 393−398.
    [80]
    West GB, Brown JH, Enquist BJ. 1997. A general model for the origin of allometric scaling laws in biology. Science, 276(5309): 122−126. doi: 10.1126/science.276.5309.122
    [81]
    Wickham H. 2016. ggplot2: Elegant Graphics for Data Analysis. 2nd ed. Cham: Springer.
    [82]
    Wong K, Elegante M, Bartels B, et al. 2010. Analyzing habituation responses to novelty in zebrafish (Danio rerio). Behavioural Brain Research, 208(2): 450−457. doi: 10.1016/j.bbr.2009.12.023
    [83]
    Wong RY, French J, Russ JB. 2019. Differences in stress reactivity between zebrafish with alternative stress coping styles. Royal Society Open Science, 6(5): 181797. doi: 10.1098/rsos.181797
    [84]
    Yan YL. 2017. The Origin and Evolution of Cave-dwelling Group of Triplophysa Fishes (Teleostei, Cypriniformes, Nemacheilidae). Master thesis, Southwest University, Chongqing. (in Chinese)
    [85]
    Yoshizawa M. 2015. Behaviors of cavefish offer insight into developmental evolution. Molecular Reproduction and Development, 82(4): 268−280. doi: 10.1002/mrd.22471
    [86]
    Zhao QY, Shao F, Li YP, et al. 2022. Novel genome sequence of Chinese cavefish (Triplophysa rosa) reveals pervasive relaxation of natural selection in cavefish genomes. Molecular Ecology, 31(22): 5831−5845. doi: 10.1111/mec.16700
    [87]
    Zhao QY, Zhang RY, Xiao YQ, et al. 2020. Comparative transcriptome profiling of the loaches Triplophysa bleekeri and Triplophysa rosa reveals potential mechanisms of eye degeneration. Frontiers in Genetics, 10: 1334. doi: 10.3389/fgene.2019.01334
  • ZR-2022-354-Supplementary Materials.pdf
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(8)  / Tables(3)

    Article Metrics

    Article views (1756) PDF downloads(383) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return