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Adaption to extreme environments: a perspective from fish genomics

Abstract

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.

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References

  • Avise JC, Selander RK (1972) Evolutionary genetics of cave-dwelling fishes of the genus Astyanax. Evolution 26:1–19

    PubMed  Google Scholar 

  • 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 78:60–67

    CAS  PubMed  Google Scholar 

  • Borowsky R (2018) Cavefishes. Curr Biol 28:R60–R64

    CAS  PubMed  Google Scholar 

  • 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 12:9

    PubMed  PubMed Central  Google Scholar 

  • Chapman LJ, Hulen KG (2001) Implications of hypoxia for the brain size and gill morphometry of mormyrid fishes. J Zool 254:461–472

    Google Scholar 

  • Cherr GN, Fairbairn E, Whitehead A (2017) Impacts of petroleum-derived pollutants on fish development. Annu Rev Anim Biosci 5:185–203

    CAS  PubMed  Google Scholar 

  • 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 79:368–374

    PubMed  Google Scholar 

  • 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 40:533

    CAS  PubMed  Google Scholar 

  • 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 9:377–386

    CAS  PubMed  Google Scholar 

  • 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 124:1–22

    CAS  PubMed  PubMed Central  Google Scholar 

  • Engel AS (2007) Observations on the biodiversity of sulfidic karst habitats. J Cave Karst Stud 69:187–206

    CAS  Google Scholar 

  • 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:R704–713

    CAS  PubMed  Google Scholar 

  • 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 24:3421–3440

    PubMed  PubMed Central  Google Scholar 

  • 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 57:1701–1710

    CAS  Google Scholar 

  • Graham JH (1993) Species diversity of fishes in naturally acidic lakes in New Jersey. Trans Am Fish Soc 122:1043–1057

    Google Scholar 

  • Greenway R, Arias-Rodriguez L, Diaz P, Tobler M (2014) Patterns of macroinvertebrate and fish diversity in freshwater sulphide springs. Diversity 6:597–632

    Google Scholar 

  • 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:e1000326

    PubMed  PubMed Central  Google Scholar 

  • 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. https://doi.org/10.1098/rstb.2016.0042

    Article  PubMed  PubMed Central  Google Scholar 

  • 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–R1212

    CAS  PubMed  Google Scholar 

  • 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 162:333–344

    CAS  PubMed  Google Scholar 

  • 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 16:871–877

    Google Scholar 

  • 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 227–257

    Google Scholar 

  • 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 25:1610–1625

    CAS  PubMed  Google Scholar 

  • 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 33:1419–1434

    CAS  PubMed  PubMed Central  Google Scholar 

  • King MC, Wilson AC (1975) Evolution at two levels in humans and chimpanzees. Science 188:107–116

    CAS  PubMed  Google Scholar 

  • 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 110:16933–16938

    CAS  PubMed  Google Scholar 

  • 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 273:183–192

    Google Scholar 

  • 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 25:219–237

    CAS  PubMed  Google Scholar 

  • Larsson DG (2014) Pollution from drug manufacturing: review and perspectives. Philos Trans R Soc Lond B Biol Sci. https://doi.org/10.1098/rstb.2013.0571

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 85–106

    Google Scholar 

  • 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 11–56

    Google Scholar 

  • Lewin HA et al (2018) Earth BioGenome Project: sequencing life for the future of life. Proc Natl Acad Sci U S A 115:4325–4333

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 53:2342–2352

    CAS  Google Scholar 

  • 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 19:441–453

    CAS  PubMed  Google Scholar 

  • Lind EE, Grahn M (2011) Directional genetic selection by pulp mill effluent on multiple natural populations of three-spined stickleback (Gasterosteus aculeatus). Ecotoxicology 20:503–512

    CAS  PubMed  PubMed Central  Google Scholar 

  • McGaugh SE et al (2014) The cavefish genome reveals candidate genes for eye loss. Nat Commun 5:5307

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 30:1527–1543

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 25:5467–5482

    CAS  PubMed  Google Scholar 

  • Nilsson GE (2007) Gill remodeling in fish—a new fashion or an ancient secret? J Exp Biol 210:2403–2409

    PubMed  Google Scholar 

  • 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 1350:325–334

    CAS  PubMed  Google Scholar 

  • 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 200:73–82

    CAS  PubMed  Google Scholar 

  • 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:e71069

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pfenninger M et al (2014) Parallel evolution of cox genes in H2S-tolerant fish as key adaptation to a toxic environment. Nat Commun 5:3873

    CAS  PubMed  Google Scholar 

  • 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 24:5446–5459

    PubMed  Google Scholar 

  • Pietri R, Roman-Morales E, Lopez-Garriga J (2011) Hydrogen sulfide and hemeproteins: knowledge and mysteries. Antioxid Redox Signal 15:393–404

    CAS  PubMed  PubMed Central  Google Scholar 

  • Plath M, Tobler M, Riesch RD (2015) Extremophile fishes: an introduction. In: Riesch R, Tobler M, Plath M (eds) Extremophile fishes. Springer, Berlin, pp 1–7

    Google Scholar 

  • Protas ME et al (2006) Genetic analysis of cavefish reveals molecular convergence in the evolution of albinism. Nat Genet 38:107–111

    CAS  PubMed  Google Scholar 

  • Protas M, Conrad M, Gross JB, Tabin C, Borowsky R (2007) Regressive evolution in the Mexican cave tetra, Astyanax mexicanus. Curr Biol 17:452–454

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 337:165–166

    CAS  PubMed  Google Scholar 

  • Reid NM et al (2016) The genomic landscape of rapid repeated evolutionary adaptation to toxic pollution in wild fish. Science 354:1305–1308

    CAS  PubMed  PubMed Central  Google Scholar 

  • Riddle MR et al (2018) Insulin resistance in cavefish as an adaptation to a nutrient-limited environment. Nature 555:647–651

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rolshausen G et al (2015) Do stressful conditions make adaptation difficult? Guppies in the oil-polluted environments of southern Trinidad. Evol Appl 8:854–870

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rosenblum EB, Parent CE, Brandt EE (2014) The molecular basis of phenotypic convergence. Annu Rev Ecol Evol Syst 45:203–226

    Google Scholar 

  • 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 209:1197–1205

    PubMed  Google Scholar 

  • Smith CR, Baco AR (2003) Ecology of whale falls at the deep-sea floor. Oceanog Mar Biol 41:311–354

    Google Scholar 

  • Soares D, Niemiller ML (2013) Sensory adaptations of fishes to subterranean environments. BioScience 63:274–283

    Google Scholar 

  • Sollid J, Nilsson GE (2006) Plasticity of respiratory structures—adaptive remodeling of fish gills induced by ambient oxygen and temperature. Respir Physiol Neurobiol 154:241–251

    CAS  PubMed  Google Scholar 

  • 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 206:3667–3673

    PubMed  Google Scholar 

  • Tobler M, Franssen CM, Plath M (2008) Male-biased predation of a cave fish by a giant water bug. Naturwissenschaften 95:775–779

    CAS  PubMed  Google Scholar 

  • Tobler M et al (2011) Evolution in extreme environments: replicated phenotypic differentiation in livebearing fish inhabiting sulfidic springs. Evolution 65:2213–2228

    PubMed  Google Scholar 

  • 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 27:843–859

    CAS  PubMed  Google Scholar 

  • 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 47:8869–8877

    CAS  PubMed  PubMed Central  Google Scholar 

  • Valko M, Morris H, Cronin MTD (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208

    CAS  PubMed  Google Scholar 

  • Van Dover C (2000) The ecology of deep-sea hydrothermal vents. Princeton University Press, Princeton

    Google Scholar 

  • Wang K et al (2019) Morphology and genome of a snailfish from the Mariana Trench provide insights into deep-sea adaptation. Nat Ecol Evol 3:823–833

    PubMed  Google Scholar 

  • Williams LM, Oleksiak MF (2011) Evolutionary and functional analyses of cytochrome P4501A promoter polymorphisms in natural populations. Mol Ecol 20:5236–5247

    CAS  PubMed  PubMed Central  Google Scholar 

  • Williams RJ et al (2009) A national risk assessment for intersex in fish arising from steroid estrogens. Environ Toxicol Chem 28:220–230

    CAS  PubMed  Google Scholar 

  • 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 1–51

    Google Scholar 

  • 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 331:1322–1325

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 114:329–353

    CAS  Google Scholar 

  • 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 36:67–77

    CAS  PubMed  Google Scholar 

  • 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:e59703

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu J et al (2013b) Gene expression changes leading extreme alkaline tolerance in Amur ide (Leuciscus waleckii) inhabiting soda lake. BMC Genomics 14:682

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 34:145–159

    CAS  PubMed  Google Scholar 

  • Yang J et al (2016) The Sinocyclocheilus cavefish genome provides insights into cave adaptation. BMC Biol 14:1

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ye X, Randall DJ (1991) The effect of water pH on swimming performance in rainbow trout (Salmo gairdneri, Richardson). Fish Physiol Biochem 9:15–21

    CAS  PubMed  Google Scholar 

  • 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 30:807–816

    CAS  PubMed  Google Scholar 

  • Yoshizawa M, O'Quin KE, Jeffery WR (2013) QTL clustering as a mechanism for rapid multi-trait evolution. Commun Integr Biol 6:e24548

    PubMed  PubMed Central  Google Scholar 

  • 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):e0173238

    PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Zhang C (2009) Endemic fishes of Sinocyclocheilus (Cypriniformes: Cyprinidae) in China—species diversity, cave adaptation, systematics and zoogeography. Science Press, Henderson

    Google Scholar 

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Acknowledgements

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.

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Correspondence to Baocheng Guo.

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Wang, Y., Guo, B. Adaption to extreme environments: a perspective from fish genomics. Rev Fish Biol Fisheries 29, 735–747 (2019). https://doi.org/10.1007/s11160-019-09577-9

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Keywords

  • Adaptation
  • Comparative genomics
  • Extreme environment
  • Parallelism
  • Population genomics