Adaption to extreme environments: a perspective from fish genomics

  • Yingnan Wang
  • Baocheng GuoEmail author


Fishes exhibit greater species diversity than any other group of vertebrates. They are found in most bodies of water, including those that pose extreme challenges, such as sulfide springs, rivers contaminated with heavy metals and organic pollutants, and caves without light. Adaptation to these extreme environments usually occurs rapidly, which has stimulated much interest in uncovering the genetic basis of such rapid adaptation. Since the sequencing of the zebrafish genome in 2001, rapid development of high-throughput sequencing technology has facilitated the additional sequencing of ~ 210 ray-finned fish genomes to date. As a result of this wealth of resources, much attention has been focused on the genetic basis of adaptation in fishes, particularly in extreme environments. The goal of this review is to summarize recent advances in fish genomics, with a specific focus on the use of genomic data to understand the genetic basis of adaptation to extreme environments in fishes. The results highlight that fishes often adapt to extreme environments through phenotypic and physiological changes that have a confirmed or inferred genetic basis. Moreover, such changes are usually rapid and repeated when parallel adaptation to similar extreme environments occurs. Specifically, parallel genetic changes are usually observed at both the intra- and interspecific level. The advances in fish genomics provide the opportunity to understand how evolutionary changes feed back into ecosystems that are facing extreme environmental changes, as well as to advance our understanding of the repeatability and predictability of evolutionary response (of fishes) to extreme environmental changes.


Adaptation Comparative genomics Extreme environment Parallelism Population genomics 



This work was supported by CAS Pioneer Hundred Talents Program, the Second Tibetan Plateau Scientific Expedition and Research (STEP) program (Grant No. 2019QZKK0501), and the National Natural Science Foundation of China (Grant No. 31672273) to B.G.


  1. Avise JC, Selander RK (1972) Evolutionary genetics of cave-dwelling fishes of the genus Astyanax. Evolution 26:1–19CrossRefPubMedGoogle Scholar
  2. Barron MG, Carls MG, Heintz R, Rice SD (2004) Evaluation of fish early life-stage toxicity models of chronic embryonic exposures to complex polycyclic aromatic hydrocarbon mixtures. Toxicol Sci 78:60–67CrossRefPubMedGoogle Scholar
  3. Borowsky R (2018) Cavefishes. Curr Biol 28:R60–R64CrossRefPubMedGoogle Scholar
  4. Bradic M, Beerli P, Garcia-de Leon FJ, Esquivel-Bobadilla S, Borowsky RL (2012) Gene flow and population structure in the Mexican blind cavefish complex (Astyanax mexicanus). BMC Evol Biol 12:9CrossRefPubMedPubMedCentralGoogle Scholar
  5. Chapman LJ, Hulen KG (2001) Implications of hypoxia for the brain size and gill morphometry of mormyrid fishes. J Zool 254:461–472CrossRefGoogle Scholar
  6. Cherr GN, Fairbairn E, Whitehead A (2017) Impacts of petroleum-derived pollutants on fish development. Annu Rev Anim Biosci 5:185–203CrossRefPubMedGoogle Scholar
  7. Coghill LM, Darrin Hulsey C, Chaves-Campos J, Garcia de Leon FJ, Johnson SG (2014) Next generation phylogeography of cave and surface Astyanax mexicanus. Mol Phylogenet Evol 79:368–374CrossRefPubMedGoogle Scholar
  8. Cooper CE, Brown GC (2008) The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: chemical mechanism and physiological significance. J Bioenerg Biomembr 40:533CrossRefPubMedGoogle Scholar
  9. Danulat E, Kempe S (1992) Nitrogenous waste excretion and accumulation of urea and ammonia in Chalcalburnus tarichi (Cyprinidae), endemic to the extremely alkaline Lake Van (Eastern Turkey). Fish Physiol Biochem 9:377–386CrossRefPubMedGoogle Scholar
  10. Denison MS, Soshilov AA, He G, DeGroot DE, Zhao B (2011) Exactly the same but different: promiscuity and diversity in the molecular mechanisms of action of the aryl hydrocarbon (dioxin) receptor. Toxicol Sci 124:1–22CrossRefPubMedPubMedCentralGoogle Scholar
  11. Engel AS (2007) Observations on the biodiversity of sulfidic karst habitats. J Cave Karst Stud 69:187–206Google Scholar
  12. Evans DH (2008) Teleost fish osmoregulation: what have we learned since August Krogh, Homer Smith, and Ancel Keys. Am J Physiol Regul Integr Comp Physiol 295:R704–713CrossRefPubMedGoogle Scholar
  13. Ford AG, Dasmahapatra KK, Ruber L, Gharbi K, Cezard T, Day JJ (2015) High levels of interspecific gene flow in an endemic cichlid fish adaptive radiation from an extreme lake environment. Mol Ecol 24:3421–3440CrossRefPubMedPubMedCentralGoogle Scholar
  14. Friedman JR, Condon NE, Drazen JC (2012) Gill surface area and metabolic enzyme activities of demersal fishes associated with the oxygen minimum zone off California. Limnol Oceanog 57:1701–1710CrossRefGoogle Scholar
  15. Graham JH (1993) Species diversity of fishes in naturally acidic lakes in New Jersey. Trans Am Fish Soc 122:1043–1057CrossRefGoogle Scholar
  16. Greenway R, Arias-Rodriguez L, Diaz P, Tobler M (2014) Patterns of macroinvertebrate and fish diversity in freshwater sulphide springs. Diversity 6:597–632CrossRefGoogle Scholar
  17. Gross JB, Borowsky R, Tabin CJ (2009) A novel role for Mc1r in the parallel evolution of depigmentation in independent populations of the cavefish Astyanax mexicanus. PLoS Genet 5:e1000326CrossRefPubMedPubMedCentralGoogle Scholar
  18. Hamilton PB, Rolshausen G, Uren Webster TM, Tyler CR (2017) Adaptive capabilities and fitness consequences associated with pollution exposure in fish. Philos Trans R Soc Lond B Biol Sci. CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hirata T et al (2003) Mechanism of acid adaptation of a fish living in a pH 3.5 lake. Am J Physiol Regul Integr Comp Physiol 284:R1199–R1212CrossRefPubMedGoogle Scholar
  20. Jurgens MD, Crosse J, Hamilton PB, Johnson AC, Jones KC (2016) The long shadow of our chemical past—high DDT concentrations in fish near a former agrochemicals factory in England. Chemosphere 162:333–344CrossRefPubMedGoogle Scholar
  21. Kaneko T, Hasegawa S, Uchida K, Ogasawara T, Oyagi A, Hirano T (1999) Acid tolerance of Japanese dace (a cyprinid teleost) in Lake Osorezan, a remarkable acid lake. Zool Sci 16:871–877CrossRefGoogle Scholar
  22. Kavembe GD, Meyer A, Wood CM (2016a) Fish populations in East African saline lakes. In: Schagerl M (ed) Soda Lakes of East Africa. Springer, Berlin, pp 227–257Google Scholar
  23. Kavembe GD, Kautt AF, Machado-Schiaffino G, Meyer A (2016b) Eco-morphological differentiation in Lake Magadi tilapia, an extremophile cichlid fish living in hot, alkaline and hypersaline lakes in East Africa. Mol Ecol 25:1610–1625CrossRefPubMedGoogle Scholar
  24. Kelley JL, Arias-Rodriguez L, Patacsil Martin D, Yee MC, Bustamante CD, Tobler M (2016) Mechanisms underlying adaptation to life in hydrogen sulfide-rich environments. Mol Biol Evol 33:1419–1434CrossRefPubMedPubMedCentralGoogle Scholar
  25. King MC, Wilson AC (1975) Evolution at two levels in humans and chimpanzees. Science 188:107–116CrossRefGoogle Scholar
  26. Kowalko JE et al (2013) Convergence in feeding posture occurs through different genetic loci in independently evolved cave populations of Astyanax mexicanus. Proc Natl Acad Sci USA 110:16933–16938CrossRefPubMedGoogle Scholar
  27. Langecker TG, Schmale H, Wilkens H (1993) Transcription of the opsin gene in degenerate eyes of cave-dwelling Astyanax fasciatus (Teleostei, Characidae) and of its conspecific epigean ancestor during early ontogeny. Cell Tissue Res 273:183–192CrossRefGoogle Scholar
  28. Laporte M et al (2016) RAD sequencing reveals within-generation polygenic selection in response to anthropogenic organic and metal contamination in North Atlantic Eels. Mol Ecol 25:219–237CrossRefPubMedGoogle Scholar
  29. Larsson DG (2014) Pollution from drug manufacturing: review and perspectives. Philos Trans R Soc Lond B Biol Sci. CrossRefPubMedPubMedCentralGoogle Scholar
  30. Laverty G, Skadhauge E (2015) Hypersaline environments. In: Riesch R, Tobler M, Plath M (eds) Extremophile fishes: ecology, evolution and physiology of teleosts in extreme environments, 1st edn. Springer, Heidelberg, New York, London, pp 85–106Google Scholar
  31. Levin LA (2005) Ecology of cold seep sediments: interactions of fauna with flow, chemistry and microbes. In: Gibson RN, Atkinson RJA, Gordon JDM (eds) Oceanography and marine biology. CRC Press, Boca Raton, pp 11–56Google Scholar
  32. Lewin HA et al (2018) Earth BioGenome Project: sequencing life for the future of life. Proc Natl Acad Sci U S A 115:4325–4333CrossRefPubMedPubMedCentralGoogle Scholar
  33. Li Z, Guo B, Li J, He S, Chen Y (2008) Bayesian mixed models and divergence time estimation of Chinese cavefishes (Cyprinidae: Sinocyclocheilus). Chin Sci Bull 53:2342–2352CrossRefGoogle Scholar
  34. Li HL, Gu XH, Li BJ, Chen CH, Lin HR, Xia JH (2017) Genome-wide QTL analysis identified significant associations between hypoxia tolerance and mutations in the GPR132 and ABCG4 genes in Nile Tilapia. Mar Biotechnol 19:441–453CrossRefPubMedGoogle Scholar
  35. Lind EE, Grahn M (2011) Directional genetic selection by pulp mill effluent on multiple natural populations of three-spined stickleback (Gasterosteus aculeatus). Ecotoxicology 20:503–512CrossRefPubMedPubMedCentralGoogle Scholar
  36. McGaugh SE et al (2014) The cavefish genome reveals candidate genes for eye loss. Nat Commun 5:5307CrossRefPubMedPubMedCentralGoogle Scholar
  37. Meng F, Braasch I, Phillips JB, Lin X, Titus T, Zhang C, Postlethwait JH (2013) Evolution of the eye transcriptome under constant darkness in Sinocyclocheilus cavefish. Mol Biol Evol 30:1527–1543CrossRefPubMedPubMedCentralGoogle Scholar
  38. Nacci D, Proestou D, Champlin D, Martinson J, Waits ER (2016) Genetic basis for rapidly evolved tolerance in the wild: adaptation to toxic pollutants by an estuarine fish species. Mol Ecol 25:5467–5482CrossRefPubMedGoogle Scholar
  39. Nilsson GE (2007) Gill remodeling in fish—a new fashion or an ancient secret? J Exp Biol 210:2403–2409CrossRefPubMedGoogle Scholar
  40. Olsson PE, Kille P (1997) Functional comparison of the metal-regulated transcriptional control regions of metallothionein genes from cadmium-sensitive and tolerant fish species. Biochim Biophys Acta 1350:325–334CrossRefPubMedGoogle Scholar
  41. Osterberg JS, Cammen KM, Schultz TF, Clark BW, Di Giulio RT (2018) Genome-wide scan reveals signatures of selection related to pollution adaptation in non-model estuarine Atlantic killifish (Fundulus heteroclitus). Aquat Toxicol 200:73–82CrossRefPubMedGoogle Scholar
  42. Palacios M et al (2013) The rediscovery of a long described species reveals additional complexity in speciation patterns of poeciliid fishes in sulfide springs. PLoS ONE 8:e71069CrossRefPubMedPubMedCentralGoogle Scholar
  43. Pfenninger M et al (2014) Parallel evolution of cox genes in H2S-tolerant fish as key adaptation to a toxic environment. Nat Commun 5:3873CrossRefPubMedGoogle Scholar
  44. Pfenninger M, Patel S, Arias-Rodriguez L, Feldmeyer B, Riesch R, Plath M (2015) Unique evolutionary trajectories in repeated adaptation to hydrogen sulphide-toxic habitats of a neotropical fish (Poecilia mexicana). Mol Ecol 24:5446–5459CrossRefPubMedGoogle Scholar
  45. Pietri R, Roman-Morales E, Lopez-Garriga J (2011) Hydrogen sulfide and hemeproteins: knowledge and mysteries. Antioxid Redox Signal 15:393–404CrossRefPubMedPubMedCentralGoogle Scholar
  46. Plath M, Tobler M, Riesch RD (2015) Extremophile fishes: an introduction. In: Riesch R, Tobler M, Plath M (eds) Extremophile fishes. Springer, Berlin, pp 1–7Google Scholar
  47. Protas ME et al (2006) Genetic analysis of cavefish reveals molecular convergence in the evolution of albinism. Nat Genet 38:107–111CrossRefPubMedGoogle Scholar
  48. Protas M, Conrad M, Gross JB, Tabin C, Borowsky R (2007) Regressive evolution in the Mexican cave tetra, Astyanax mexicanus. Curr Biol 17:452–454CrossRefPubMedPubMedCentralGoogle Scholar
  49. Randall DJ, Wood CM, Perry SF, Bergman H, Maloiy GM, Mommsen TP, Wright PA (1989) Urea excretion as a strategy for survival in a fish living in a very alkaline environment. Nature 337:165–166CrossRefPubMedGoogle Scholar
  50. Reid NM et al (2016) The genomic landscape of rapid repeated evolutionary adaptation to toxic pollution in wild fish. Science 354:1305–1308CrossRefPubMedPubMedCentralGoogle Scholar
  51. Riddle MR et al (2018) Insulin resistance in cavefish as an adaptation to a nutrient-limited environment. Nature 555:647–651CrossRefPubMedPubMedCentralGoogle Scholar
  52. Rolshausen G et al (2015) Do stressful conditions make adaptation difficult? Guppies in the oil-polluted environments of southern Trinidad. Evol Appl 8:854–870CrossRefPubMedPubMedCentralGoogle Scholar
  53. Rosenblum EB, Parent CE, Brandt EE (2014) The molecular basis of phenotypic convergence. Annu Rev Ecol Evol Syst 45:203–226CrossRefGoogle Scholar
  54. Sloman KA et al (2006) Tribute to R.G. Boutilier: the effect of size on the physiological and behavioural responses of oscar, Astronotus ocellatus, to hypoxia. J Exp Biol 209:1197–1205CrossRefPubMedGoogle Scholar
  55. Smith CR, Baco AR (2003) Ecology of whale falls at the deep-sea floor. Oceanog Mar Biol 41:311–354Google Scholar
  56. Soares D, Niemiller ML (2013) Sensory adaptations of fishes to subterranean environments. BioScience 63:274–283CrossRefGoogle Scholar
  57. Sollid J, Nilsson GE (2006) Plasticity of respiratory structures—adaptive remodeling of fish gills induced by ambient oxygen and temperature. Respir Physiol Neurobiol 154:241–251CrossRefPubMedGoogle Scholar
  58. Sollid J, De Angelis P, Gundersen K, Nilsson GE (2003) Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. J Exp Biol 206:3667–3673CrossRefPubMedGoogle Scholar
  59. Tobler M, Franssen CM, Plath M (2008) Male-biased predation of a cave fish by a giant water bug. Naturwissenschaften 95:775–779CrossRefPubMedGoogle Scholar
  60. Tobler M et al (2011) Evolution in extreme environments: replicated phenotypic differentiation in livebearing fish inhabiting sulfidic springs. Evolution 65:2213–2228CrossRefPubMedGoogle Scholar
  61. Tobler M, Kelley JL, Plath M, Riesch R (2018) Extreme environments and the origins of biodiversity: adaptation and speciation in sulphide spring fishes. Mol Ecol 27:843–859CrossRefPubMedGoogle Scholar
  62. Uren Webster TM, Bury N, van Aerle R, Santos EM (2013) Global transcriptome profiling reveals molecular mechanisms of metal tolerance in a chronically exposed wild population of brown trout. Environ Sci Technol 47:8869–8877CrossRefPubMedPubMedCentralGoogle Scholar
  63. Valko M, Morris H, Cronin MTD (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208CrossRefGoogle Scholar
  64. Van Dover C (2000) The ecology of deep-sea hydrothermal vents. Princeton University Press, PrincetonGoogle Scholar
  65. Wang K et al (2019) Morphology and genome of a snailfish from the Mariana Trench provide insights into deep-sea adaptation. Nat Ecol Evol 3:823–833CrossRefPubMedGoogle Scholar
  66. Williams LM, Oleksiak MF (2011) Evolutionary and functional analyses of cytochrome P4501A promoter polymorphisms in natural populations. Mol Ecol 20:5236–5247CrossRefPubMedPubMedCentralGoogle Scholar
  67. Williams RJ et al (2009) A national risk assessment for intersex in fish arising from steroid estrogens. Environ Toxicol Chem 28:220–230CrossRefPubMedGoogle Scholar
  68. Wood CM (2011) An introduction to metals in fish physiology and toxicology. In: Wood CM, Farrell AP, Brauner CJ (eds) Fish physiology: homeostasis and toxicology of essential metals, 1st edn, vol 31A. Academic Press, London, pp 1–51Google Scholar
  69. Wirgin I, Roy NK, Loftus M, Chambers RC, Franks DG, Hahn ME (2011) Mechanistic basis of resistance to PCBs in Atlantic tomcod from the Hudson River. Science 331:1322–1325CrossRefPubMedPubMedCentralGoogle Scholar
  70. Wright PA, Wood CM (1985) An analysis of branchial ammonia excretion in the freshwater rainbow trout: effects of environmental pH change and sodium uptake blockade. J Exp Biol 114:329–353Google Scholar
  71. Xiao H, Chen SY, Liu ZM, Zhang RD, Li WX, Zan RG, Zhang YP (2005) Molecular phylogeny of Sinocyclocheilus (Cypriniformes: Cyprinidae) inferred from mitochondrial DNA sequences. Mol Phylogenet Evol 36:67–77CrossRefPubMedGoogle Scholar
  72. Xu J et al (2013a) Transcriptome sequencing and analysis of wild Amur Ide (Leuciscus waleckii) inhabiting an extreme alkaline-saline lake reveals insights into stress adaptation. PLoS ONE 8:e59703CrossRefPubMedPubMedCentralGoogle Scholar
  73. Xu J et al (2013b) Gene expression changes leading extreme alkaline tolerance in Amur ide (Leuciscus waleckii) inhabiting soda lake. BMC Genomics 14:682CrossRefPubMedPubMedCentralGoogle Scholar
  74. Xu J et al (2017) Genomic basis of adaptive evolution: the survival of Amur Ide (Leuciscus waleckii) in an extremely alkaline environment. Mol Biol Evol 34:145–159CrossRefPubMedGoogle Scholar
  75. Yang J et al (2016) The Sinocyclocheilus cavefish genome provides insights into cave adaptation. BMC Biol 14:1CrossRefPubMedPubMedCentralGoogle Scholar
  76. Ye X, Randall DJ (1991) The effect of water pH on swimming performance in rainbow trout (Salmo gairdneri, Richardson). Fish Physiol Biochem 9:15–21CrossRefPubMedGoogle Scholar
  77. Yokoyama R, Yokoyama S (1990) Isolation, DNA sequence and evolution of a color visual pigment gene of the blind cave fish Astyanax fasciatus. Vis Res 30:807–816CrossRefPubMedGoogle Scholar
  78. Yoshizawa M, O'Quin KE, Jeffery WR (2013) QTL clustering as a mechanism for rapid multi-trait evolution. Commun Integr Biol 6:e24548CrossRefPubMedPubMedCentralGoogle Scholar
  79. Zhang X, Wen H, Wang H, Ren Y, Zhao J, Li Y (2017) RNA-Seq analysis of salinity stress-responsive transcriptome in the liver of spotted sea bass (Lateolabrax maculatus). PLoS ONE 12(3):e0173238CrossRefPubMedPubMedCentralGoogle Scholar
  80. Zhao Y, Zhang C (2009) Endemic fishes of Sinocyclocheilus (Cypriniformes: Cyprinidae) in China—species diversity, cave adaptation, systematics and zoogeography. Science Press, HendersonGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Key Laboratory of Zoological Systematics and Evolution, Institute of ZoologyChinese Academy of SciencesBeijingChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Center for Excellence in Animal Evolution and GeneticsChinese Academy of SciencesKunmingChina

Personalised recommendations