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Hydrogen Sulfide-Toxic Habitats

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Abstract

Hydrogen sulfide (H2S) is a potent respiratory toxicant that is lethal to most metazoans (including fishes) in micromolar concentrations, as demonstrated by mass kills following environmental spills. Nevertheless, a number of teleosts have adapted to, and thrive in, habitats with high ambient H2S concentrations as found, for example, at marine hydrothermal vents (“black smokers”), cold seeps, or in freshwater sulfide springs. Livebearing fishes (Poeciliidae) dominate amongst freshwater fishes inhabiting sulfide spring in the New World and are the most studied group of freshwater sulfide-dwellers. In this chapter, we identify targets of directional selection in sulfidic habitats and demonstrate how these affect different levels of biological organization (e.g., cellular functioning and molecular evolution, morphology and organ evolution, whole body performance and eco-physiological traits, life histories). We highlight multifarious selective regimes arising from correlated abiotic stressors (like hypoxia) and altered ecological parameters (like truncated ecological communities and altered predatory regimes). Finally, we discuss the evidence for replicated ecological speciation as a result of independent evolutionary transitions in different lineages of poeciliids into sulfide waters, and we summarize studies examining the question of how local adaptation translates into the emergence of reproductive isolation due to selection against non-adapted individuals migrating between habitat types.

Keywords

Reproductive Isolation Hydrothermal Vent Cold Seep Offspring Size Routine Metabolic Rate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
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Notes

Acknowledgments

We would like to thank the American Livebearers Association, the Erwin Riesch-Stiftung, the Freunde und Förderer der Goethe-Universität Frankfurt, the German Academic Exchange Service (DAAD), the German Ichthyological Society (GfI), the German Research Foundation (DFG), the Herrmann Willkomm-Stiftung, the Human Frontier Science Program (HFSP), the National Geographic Society, the National Science Foundation of the USA (NSF, IOS-1121832), and the Swiss National Science Foundation for financial support over many years. Our research was only possible due to the collaborative support and substantial help rendered by L Arias-Rodriguez and JR Indy (Villahermosa), FJ Garcia-Léon (La Paz), I Schlupp (Oklahoma), as well as a large number of undergraduate, graduate, and postdoctoral researchers that have circled through our labs.

References

  1. Abel DC, Koenig CC, Davis WP (1987) Emersion in the mangrove forest fish Rivulus marmoratus: a unique response to hydrogen sulfide. Environ Biol Fish 18:67–72Google Scholar
  2. Affonso EG, Rantin FT (2005) Respiratory responses of the air-breathing fish Hoplosternum littorale to hypoxia and hydrogen sulfide. Comp Biochem Physiol Part C: Toxicol Pharmacol 141:275–280Google Scholar
  3. Alvarez J (1948) Descripción de una nueva especie de Mollienisia capturada en Baños del Azufre, Tabasco (Pisces, Poeciliidae). An Esc Nac Cienc Biol 5:275–281Google Scholar
  4. Andersson MB (1994) Sexual selection. Princeton University Press, Princeton, NJGoogle Scholar
  5. Bagarinao T (1992) Sulfide as an environmental factor and toxicant: tolerance and adaptations in aquatic organisms. Aquat Toxicol 24:21–62Google Scholar
  6. Bagarinao T, Vetter RD (1989) Sulfide tolerance and detoxification in shallow-water marine fishes. Mar Biol 103:291–302Google Scholar
  7. Bashey F (2008) Competition as a selective mechanism for larger offspring size in guppies. Oikos 117:104–113Google Scholar
  8. Beinart RA, Sanders JG, Faure B, Sylva SP, Lee RW, Becker EL, Gartman A, Luther GW, Seewald JS, Fisher CR, Girguis PR (2012) Evidence for the role of endosymbionts in regional-scale habitat partitioning by hydrothermal vent symbioses. Proc Natl Acad Sci U S A 109:E3241–E3250Google Scholar
  9. Bierbach D, Klein M, Sassmannshausen V, Schlupp I, Riesch R, Parzefall J, Plath M (2012) Divergent evolution of male aggressive behaviour another reproductive isolation barrier in extremophile poeciliid fishes? Int J Evol Biol 2012:148745PubMedCentralPubMedGoogle Scholar
  10. Bierbach D, Schulte M, Herrmann N, Zimmer C, Arias-Rodriguez L, Indy JR, Riesch R, Plath M (2013) Predator avoidance in extremophile fish. Life 3:161–180PubMedCentralPubMedGoogle Scholar
  11. Biscoito M (2006) Chordata, Chondrichthyes & Osteichthyes. In: Desbruyères D, Segonzac M, Bright M (eds) Handbook of deep-sea hydrothermal vent fauna. Denisia 18:489–490Google Scholar
  12. Biscoito M, Segonzac M, Almeida AJ, Desbruyeres D, Geistdoerfer P, Turnipseed M, Van Dover C (2002) Fishes from the hydrothermal vents and cold seeps – an update. Cah Biol Mar 43:359–362Google Scholar
  13. Blackburn DG (1999) Viviparity and oviparity: evolution and reproductive strategies. In: Knobil TE, Neill JD (eds) Encyclopedia of reproduction. Academic Press, New York, NY, pp 994–1003Google Scholar
  14. Blackburn DG (2005) Evolutionary origins of viviparity in fishes. In: Grier HJ, Uribe MC (eds) Viviparous fishes. New Life Publications, Homestead, FL, pp 287–301Google Scholar
  15. Brauner CJ, Ballantyne CL, Randall DJ, Val AL (1995) Air breathing in the armoured catfish (Hoplosternum littorale) as an adaptation to hypoxic, acidic, and hydrogen sulphide rich waters. Can J Zool 73:739–744Google Scholar
  16. Brockelman WY (1975) Competition, the fitness of offspring, and optimal clutch size. Am Nat 109:677–699Google Scholar
  17. Cavanaugh CM, Gardiner SL, Jones ML, Jannasch HW, Waterbury JB (1981) Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science 213:340–342PubMedGoogle Scholar
  18. Chen KY, Morris JC (1972) Kinetics of oxidation of aqueous sulfide by oxygen. Environ Sci Technol 6:529–537Google Scholar
  19. Cheney DL, Seyfarth RM (1990) How monkeys see the world. University of Chicago Press, Chicago, ILGoogle Scholar
  20. Cline JD, Richards FA (1969) Oxygenation of hydrogen sulfide in seawater at constant salinity, temperature and pH. Environ Sci Technol 3:838–843Google Scholar
  21. Coad BW (1980) A re-description of Aphanius ginaonis (Holly, 1929) from southern Iran (Osteichthyes: Cyprinodontiformes). J Nat Hist 14:33–40Google Scholar
  22. Cohen DM, Rosenblatt RH, Moser HG (1990) Biology and description of a bythitid fish from deep-sea thermal vents in the tropical eastern Pacific. Deep-Sea Res 37:267–283Google Scholar
  23. 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 40:533–539PubMedGoogle Scholar
  24. Eifert C, Farnworth M, Schulz–Mirbach T, Riesch R, Bierbach D, Klaus S, Wurster A, Tobler M, Streit B, Indy JR, Arias–Rodriguez L, Plath M (2014) Brain size variation in extremophile fish: local adaptation vs. phenotypic plasticity. J Zool Lond (online first)Google Scholar
  25. Elmer KR, Meyer A (2011) Adaptation in the age of ecological genomics: insights from parallelism and convergence. Trends Ecol Evol 26:298–306PubMedGoogle Scholar
  26. Geiger SP, Torres JJ, Crabtree RE (2000) Air breathing and gill ventilation frequencies in juvenile tarpon, Megalops atlanticus: responses to changes in dissolved oxygen, temperature, hydrogen sulfide, and pH. Environ Biol Fishes 59:181–190Google Scholar
  27. Gordon MS, Rosen DE (1962) A cavernicolous form of the poeciliid fish Poecilia sphenops from Tabasco, Mexico. Copeia 1962:360–368Google Scholar
  28. Greenway R, Arias-Rodriguez L, Diaz P, Tobler M (2014) Patterns of macroinvertebrate and fish diversity in freshwater sulphide springs. Diversity 6:597–632Google Scholar
  29. Grieshaber MK, Völkel S (1998) Animal adaptations for tolerance and exploitation of poisonous sulfide. Annu Rev Physiol 60:33–53PubMedGoogle Scholar
  30. Hamilton A (2001) Phylogeny of Limia (Teleostei: Poeciliidae) based on NADH dehydrogenase subunit 2 sequences. Mol Phylogenet Evol 19:277–289PubMedGoogle Scholar
  31. Hildebrandt TM, Grieshaber MK (2008) Three enzymatic activities catalyze the oxidation of sulfide to thiosulfate in mammalian and invertebrate mitochondria. FEBS J 275:3352–3361PubMedGoogle Scholar
  32. Jahn A, Janas U, Theede H, Szaniawska A (1997) Significance of body size in sulphide detoxification in the Baltic clam Macoma balthica (Bivalvia, Tellinidae) in the Gulf of Gdansk. Mar Ecol Prog Ser 154:175–183Google Scholar
  33. Jannasch HW, Taylor CD (1984) Deep-sea microbiology. Annu Rev Microbiol 38:487–514PubMedGoogle Scholar
  34. Jørgensen C, Auer SK, Reznick DN (2011) A model for optimal offspring size in fish, including live-bearing and parental effects. Am Nat 177:E119–E135PubMedGoogle Scholar
  35. Jourdan J, Bierbach D, Riesch R, Dzienko J, Karau N, Oranth A, Stadler S, Schießl A, Wigh A, Arias-Rodriguez L, Indy JR, Klaus S, Zimmer C, Plath M (2014) Microhabitat use, population densities, and size distributions of sulfur cave-dwelling Poecilia mexicana. PeerJ 2:e490PubMedCentralPubMedGoogle Scholar
  36. Kelley JL (2008) Assessment of predation risk by prey fishes. In: Magnhagen C, Braithwaite VA, Forsgren E, Kapoor BG (eds) Fish behaviour. Science Publishers, Enfield, NH, pp 269–301Google Scholar
  37. Kelley JL, Magurran AE (2003) Effects of relaxed predation pressure on visual predator recognition in the guppy. Behav Ecol Sociobiol 54:225–232Google Scholar
  38. Kirkpatrick M (2001) Reinforcement during ecological speciation. Proc R Soc Lond B 268:2616Google Scholar
  39. Lagoutte E, Mimoun S, Andriamihaja M, Chaumontet C, Blachier F, Bouillaud F (2010) Oxidation of hydrogen sulfide remains a priority in mammalian cells and causes reverse electron transfer in colonocytes. Biochim Biophys Acta 1797:1500–1511PubMedGoogle Scholar
  40. Langecker TG, Wilkens H, Parzefall J (1996) Studies on the trophic structure of an energy rich Mexican cave (Cueva de las Sardinas) containing sulfurous water. Mem Biospeol 23:121–125Google Scholar
  41. Langerhans RB, DeWitt TJ (2004) Shared and unique features of evolutionary diversification. Am Nat 164:335–349PubMedGoogle Scholar
  42. Langerhans RB, Riesch R (2013) Speciation by selection: a framework for understanding ecology’s role in speciation. Curr Zool 59:31–52Google Scholar
  43. Li L, Rose P, Moore PK (2011) Hydrogen sulfide and cell signaling. Annu Rev Pharmacol Toxicol 51:169–187PubMedGoogle Scholar
  44. Little CTS, Vrijenhoek RC (2003) Are hydrothermal vent animals living fossils? Trends Ecol Evol 18:582–588Google Scholar
  45. Losos JB (2011) Convergence, adaptation, and constraint. Evolution 65:1827–1840PubMedGoogle Scholar
  46. Lozano-Vilano ML, Contreras-Balderas S (1999) Cyprinodon bobmilleri: new species of pupfish from Nuevo León, México (Pisces: Cyprinodontidae). Copeia 1999:382–387Google Scholar
  47. Marcia M, Ermler U, Peng G, Michel H (2009) The structure of Aquifex aeolicus sulfide:quinone oxidoreductase, a basis to understand sulfide detoxification and respiration. Proc Natl Acad Sci U S A 106:9625–9630PubMedCentralPubMedGoogle Scholar
  48. Micheli F, Peterson CH, Mullineaux LS et al (2002) Predation structures communities at deep-sea hydrothermal vents. Ecol Monogr 72:365–382Google Scholar
  49. Miller RR (1975) Five new species of Mexican poeciliid fishes of the genera Poecilia, Gambusia, and Poeciliopsis. Occ Pap Mus Zool Univ Mich 672:1–44Google Scholar
  50. Møller PR, Gravlund P (2003) Phylogeny of the eelpout genus Lycodes (Pisces, Zoarcidae) as inferred from mitochondrial cytochrome b and 12S rDNA. Mol Phylogenet Evol 26:369–388PubMedGoogle Scholar
  51. Munroe TA, Hashimoto J (2008) A new Western Pacific Tonguefish (Pleuronectiformes: Cynoglossidae): the first Pleuronectiform discovered at active hydrothermal vents. Zootaxa 1839:43–59Google Scholar
  52. Munroe TA, Tyler J, Tunnicliffe V (2011) Description and biological observations on a new species of deepwater symphurine tonguefish (Pleuronectiformes: Cynoglossidae: Symphurus) collected at Volcano–19, Tonga Arc, West Pacific Ocean. Zootaxa 3061:53–66Google Scholar
  53. Nosil P (2012) Ecological speciation. Oxford University Press, OxfordGoogle Scholar
  54. Palacios M, Arias-Rodriguez L, Plath M, Eifert C, Lerp H, Lamboj A, Voelkel G, Tobler M (2013) The rediscovery of a long described species reveals additional complexity in speciation patterns of poeciliid fishes in sulfide springs. PLoS One 8:e71069PubMedCentralPubMedGoogle Scholar
  55. Parzefall J (1974) Rückbildung aggressiver Verhaltensweisen bei einer Höhlenform von Mollienesia sphenops (Pisces, Poeciliidae). Z Tierpsychol 35:66–84PubMedGoogle Scholar
  56. Parzefall J (1979) Zur Genetik und biologischen Bedeutung des Aggressionsverhaltens von Poecilia sphenops (Pisces, Poeciliidae). Z Tierpsychol 50:399–422Google Scholar
  57. Parzefall J (1993) Schooling behaviour in population-hybrids of Astyanax fasciatus and Poecilia mexicana (Pisces, Characidae and Poeciliidae). In: Schröder H, Bauer J, Schartl M (eds) Trends in ichthyology. Blackwell Science, Oxford, pp 297–303Google Scholar
  58. Pfenninger M, Lerp H, Tobler M, Passow C, Kelley JL, Funke E, Greshake B, Erkoc UK, Berberich T, Plath M (2014) Parallel evolution of cox-genes in H2S-tolerant fish as key adaptation to a toxic environment. Nat Commun 5:3873PubMedGoogle Scholar
  59. Plath M (2008) Male mating behavior and costs of sexual harassment for females in cavernicolous and extremophile populations of Atlantic mollies (Poecilia mexicana). Behaviour 145:73–98Google Scholar
  60. Plath M, Schlupp I (2008) Parallel evolution leads to reduced shoaling behavior in two cave dwelling populations of Atlantic mollies (Poecilia mexicana, Poeciliidae, Teleostei). Environ Biol Fish 82:289–297Google Scholar
  61. Plath M, Tobler M (2010) Subterranean fishes of Mexico (Poecilia mexicana, Poeciliidae). In: Trajano E, Bichuette ME, Kapoor BG (eds) The biology of subterranean fishes. Science Publishers, Enfield, NH, pp 283–332Google Scholar
  62. Plath M, Parzefall J, Schlupp I (2003) The role of sexual harassment in cave and surface dwelling populations of the Atlantic molly, Poecilia mexicana (Poeciliidae, Teleostei). Behav Ecol Sociobiol 54:303–309Google Scholar
  63. Plath M, Heubel KU, Garcia de Leon FJ, Schlupp I (2005) Cave molly females (Poecilia mexicana, Poeciliidae, Teleostei) like well-fed males. Behav Ecol Sociobiol 58:144–151Google Scholar
  64. Plath M, Brümmer A, Parzefall J, Schlupp I (2006) Size–dependent male mating behaviour and sexual harassment in a population of Atlantic mollies (Poecilia mexicana) from a sulphur creek. Acta Ethol 9:15–21Google Scholar
  65. Plath M, Hauswaldt JS, Moll K, Tobler M, García de León FJ, Schlupp I, Tiedemann R (2007a) Local adaptation and pronounced genetic differentiation in an extremophile fish, Poecilia mexicana, inhabiting a Mexican cave with toxic hydrogen sulphide. Mol Ecol 16:967–976PubMedGoogle Scholar
  66. Plath M, Tobler M, Riesch R, García de León FJ, Giere O, Schlupp I (2007b) Survival in an extreme habitat: the roles of behaviour and energy limitation. Naturwissenschaften 94:991–996PubMedGoogle Scholar
  67. Plath M, Riesch R, Oranth A, Dzienko J, Karau N, Schießl A, Stadler S, Wigh A, Zimmer C, Arias-Rodriguez L, Schlupp I, Tobler M (2010) Complementary effect of natural and sexual selection against immigrants maintains differentiation between locally adapted fish. Naturwissenschaften 97:769–774PubMedGoogle Scholar
  68. Plath M, Pfenninger M, Lerp H, Riesch R, Eschenbrenner C, Slattery PA, Bierbach D, Herrmann N, Schulte M, Arias-Rodriguez L, Indy JR, Passow C, Tobler M (2013) Genetic differentiation and selection against migrants in evolutionarily replicated extreme environments. Evolution 67:2647–2661PubMedGoogle Scholar
  69. Powell E (1989) Oxygen, sulfide and diffusion: why thiobiotic meiofauna must be sulfide-insensitive first-order respirers. J Mar Res 47:887–932Google Scholar
  70. Reiffenstein RJ, Hulbert WC, Roth SH (1992) Toxicology of hydrogen sulfide. Annu Rev Pharmacol Toxicol 32:109–134PubMedGoogle Scholar
  71. Riesch R, Plath M, Schlupp I, Tobler M, Langerhans RB (2014) Colonisation of toxic environments drives predictable life-history evolution in livebearing fishes (Poeciliidae). Ecol Lett 17:65–71PubMedGoogle Scholar
  72. Riesch R, Duwe V, Herrmann N, Padur L, Ramm A, Scharnweber K, Schulte M, Schulz-Mirbach T, Ziege M, Plath M (2009) Variation along the shy–bold continuum in extremophile fishes (Poecilia mexicana, Poecilia sulphuraria). Behav Ecol Sociobiol 63:1515–1526Google Scholar
  73. Riesch R, Oranth A, Dzienko J, Karau N, Schießl A, Stadler S, Wigh A, Zimmer C, Arias-Rodriguez L, Schlupp I, Plath M (2010a) Extreme habitats are not refuges: poeciliids suffer from increased aerial predation risk in sulphidic southern Mexican habitats. Biol J Linn Soc 101:417–426Google Scholar
  74. Riesch R, Plath M, García de León F, Schlupp I (2010b) Convergent life-history shifts: toxic environments result in big babies in two clades of poeciliids. Naturwissenschaften 97:133–141PubMedGoogle Scholar
  75. Riesch R, Plath M, Schlupp I (2010c) Toxic hydrogen sulfide and dark caves: life-history adaptations in a livebearing fish (Poecilia mexicana, Poeciliidae). Ecology 91:1494–1505PubMedGoogle Scholar
  76. Riesch R, Plath M, Schlupp I (2011a) Toxic hydrogen sulphide and dark caves: pronounced male life-history divergence among locally adapted Poecilia mexicana (Poeciliidae). J Evol Biol 24:596–606PubMedGoogle Scholar
  77. Riesch R, Schlupp I, Langerhans RB, Plath M (2011b) Shared and unique patterns of embryo development in extremophile poeciliids. PLoS One 6:e27377PubMedCentralPubMedGoogle Scholar
  78. Riesch R, Schlupp I, Schleucher E, Hildenbrand P, Köhler A, Arias-Rodriguez L, Plath M (2011c) Reduced starvation resistance and increased metabolic rates in an unusual cave organism: the cave molly (Poecilia mexicana, Poeciliidae). Bull Fish Biol 13:41–56Google Scholar
  79. Roach KA, Tobler M, Winemiller KO (2011) Hydrogen sulfide, bacteria, and fish: a unique, subterranean food chain. Ecology 92:2056–2062PubMedGoogle Scholar
  80. Rollinson N, Hutchings JA (2013a) The relationship between offspring size and fitness: integrating theory and empiricism. Ecology 94:315–324PubMedGoogle Scholar
  81. Rollinson N, Hutchings JA (2013b) Environmental quality predicts optimal egg size in the wild. Am Nat 182:76–90PubMedGoogle Scholar
  82. Rosales Lagarde L (2012) Investigations of karst brackish-sulfidic springs and their role in sulfidic springs and their hydrogeology, subsurface water-rock interactions, and speleogenesis at the northern Sierra de Chiapas, Mexico. PhD dissertation, New Mexico Institute of Mining and Technology, Socorro, NMGoogle Scholar
  83. Rosenblatt RH, Cohen DM (1986) Fishes living in deepsea thermal vents in the tropical eastern Pacific, with descriptions of a new genus and two new species of eelpouts (Zoarcidae). Trans San Diego Soc Nat Hist 21:71–79Google Scholar
  84. Schoonen MAA, Barnes HL (1988) An approximation of the second dissociation constant for H2S. Geochim Cosmochim Acta 52:649–654Google Scholar
  85. Seghers BH (1974) Geographic variation in the responses of guppies (Poecilia reticulata) to aerial predators. Oecologia 14:93–98Google Scholar
  86. Servedio MR (2007) Male versus female mate choice: sexual selection and the evolution of species recognition via reinforcement. Evolution 61:2772–2789PubMedGoogle Scholar
  87. Shahak Y, Hauska G (2008) Sulfide oxidation from cyanobacteria to humans: sulfide-quinone oxidoreductase (SQR). In: Hell R, Dahl C, Knaff DB, Leustek T (eds) Advances in photosynthesis and respiration. Springer, Berlin, pp 319–335Google Scholar
  88. Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Am Nat 108:499–506Google Scholar
  89. Steindachner F (1863) Beiträge zur Kenntniss der Sciaenoiden Brasiliens und der Cyprinodonten Mejicos. Sitzungsberichte der Mathematisch-Naturwissen-schaftlichen Classe der Kaiserlichen Akademie der Wissenschaften 48:162–185Google Scholar
  90. Stipanuk MH (2004) Sulfur amino acid metabolism: pathways for production and removal of homocysteine amd cysteine. Annu Rev Nutr 24:539–577PubMedGoogle Scholar
  91. Stipanuk MH, Ueki I (2011) Dealing with methionine/homocysteine sulfur: cysteine metabolism to taurine and inorganic sulfur. J Inherit Metab Dis 34:17–32PubMedCentralPubMedGoogle Scholar
  92. Szabó C (2007) Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov 6:917–935PubMedGoogle Scholar
  93. Teimori A (2013) The evolutionary history and taxonomy of Aphanius (Teleostei: Cyprinodontidae) species in Iran and the Persian Gulf region. Doctoral dissertation, Ludwig-Maximilians-University Munich, MunichGoogle Scholar
  94. Templeton CN, Shriner WM (2004) Multiple selection pressures influence Trinidadian guppy (Poecilia reticulata) antipredator behavior. Behav Ecol 15:673–678Google Scholar
  95. Theissen U, Hoffmeister M, Grieshaber M, Martin W (2003) Single eubacterial origin of eukaryotic sulfide:quinone oxidoreductase, a mitochondrial enzyme conserved from the early evolution of eukaryotes during anoxic and sulfidic times. Mol Biol Evol 20:1564–1574PubMedGoogle Scholar
  96. Tobler M (2008) Divergence in trophic ecology characterizes colonization of extreme habitats. Biol J Linn Soc 95:517–528Google Scholar
  97. Tobler M, Hastings L (2011) Convergent patterns of body shape differentiation in four different clades of poeciliid fishes inhabiting sulfide springs. Evol Biol 38:412–421Google Scholar
  98. Tobler M, Plath M (2009a) Threatened fishes of the world: Gambusia eurystoma Miller, 1975 (Poeciliidae). Environ Biol Fish 85:251Google Scholar
  99. Tobler M, Plath M (2009b) Threatened fishes of the world: Poecilia sulphuraria (Alvarez, 1948) (Poeciliidae). Environ Biol Fish 85:333–334Google Scholar
  100. Tobler M, Plath M (2011) Living in extreme environments. In: Evans JP, Pilastro A, Schlupp I (eds) Ecology and evolution of poeciliid fishes. University of Chicago Press, Chicago, IL, pp 120–127Google Scholar
  101. Tobler M, Schlupp I, Heubel K, Riesch R, García de León FJ, Giere O, Plath M (2006) Life on the edge: hydrogen sulfide and the fish communities of a Mexican cave and surrounding waters. Extremophiles 10:577–585PubMedGoogle Scholar
  102. Tobler M, Schlupp I, García de León FJ, Glaubrecht M, Plath M (2007) Extreme habitats as refuge from parasite infections? Evidence from an extremophile fish. Acta Oecol 31:270–275Google Scholar
  103. Tobler M, DeWitt TJ, Schlupp I, García de León FJ, Herrmann R, Feulner PGD, Tiedemann R, Plath M (2008a) Toxic hydrogen sulfide and dark caves: phenotypic and genetic divergence across two abiotic environmental gradients in Poecilia mexicana. Evolution 62:2643–2659PubMedGoogle Scholar
  104. Tobler M, Riesch R, García de León F, Schlupp I, Plath M (2008b) A new and morphologically distinct population of cavernicolous Poecilia mexicana (Poeciliidae: Teleostei). Environ Biol Fish 82:101–108Google Scholar
  105. Tobler M, Riesch R, García de León FJ, Schlupp I, Plath M (2008c) Two endemic and endangered fishes, Poecilia sulphuraria (Alvarez, 1948) and Gambusia eurystoma Miller, 1975 (Poeciliidae, Teleostei) as only survivors in a small sulphidic habitat. J Fish Biol 72:523–533Google Scholar
  106. Tobler M, Riesch R, Tobler CM, Plath M (2009a) Compensatory behaviour in response to sulphide-induced hypoxia affects time budgets, feeding efficiency, and predation risk. Evol Ecol Res 11:935–948Google Scholar
  107. Tobler M, Riesch R, Tobler CM, Schulz-Mirbach T, Plath M (2009b) Natural and sexual selection against immigrants maintains differentiation among micro-allopatric populations. J Evol Biol 22:2298–2304PubMedGoogle Scholar
  108. Tobler M, Palacios M, Chapman LJ, Mitrofanov I, Bierbach D, Plath M, Arias-Rodriguez L, García de León FJ, Mateos M (2011) Evolution in extreme environments: replicated phenotypic differentiation in livebearing fish inhabiting sulfidic springs. Evolution 65:2213–2228PubMedGoogle Scholar
  109. Tobler M, Henpita C, Bassett B, Kelley JL, Shaw J (2014a) H2S exposure elicits differential expression of candidate genes in fish from sulfidic and non-sulfidic environments. Comp Biochem Physiol A 175:7–14Google Scholar
  110. Tobler M, Plath M, Riesch R, Schlupp I, Grasse A, Munimanda GK, Setzer C, Penn DJ, Moodley Y (2014b) Selection from parasites favors immunogenetic diversity but not divergence among locally adapted host populations. J Evol Biol 27:960–974PubMedGoogle Scholar
  111. Tunnicliffe V, Barross JA, Gebruk AV, Giere O, Holland ME, Koschinsky A, Reysenbach A-L, Shank TM, Summitt AM (2003) Group report: what are the interactions between biotic processes at vents and physical, chemical, and geological conditions? In: Halbach P, Tunnicliffe V, Hein J (eds) Energy and mass transfer in marine hydrothermal systems. Dahlem University Press, Berlin, pp 250–270Google Scholar
  112. Tunnicliffe V, Koop BF, Tyler J, So S (2010) Flatfish at seamount hydrothermal vents show strong genetic divergence between volcanic arcs. Mar Ecol 31:158–167Google Scholar
  113. Tunnicliffe V, Tyler J, Dower JF (2013) Population ecology of the tonguefish Symphurus thermophilus (Pisces; Pleuronectiformes; Cynoglossidae) at sulphur-rich hydrothermal vents on volcanoes of the northern Mariana Arc. Deep Sea Res II Top Stud Oceanogr 92:172–182Google Scholar
  114. U.S. EPA (U.S. Environmental Protection Agency) (2013) ECOTOX database. http://cfpub.epa.gov/ecotox/. Consulted on 23 Sept 2013
  115. Van Dover CL (2000) The ecology of deep-sea hydrothermal vents. Princeton University Press, Princeton, NJGoogle Scholar
  116. Vrijenhoek RC, Duhaime M, Jones WJ (2007) Subtype variation among bacterial endosymbionts of tubeworms (Annelida: Siboglinidae) from the Gulf of California. Biol Bull 212:180–184PubMedGoogle Scholar
  117. Winemiller KO (1989) Development of dermal lip protuberances for aquatic surface respiration in South American characid fishes. Copeia 1989:382–390Google Scholar
  118. Winemiller KO, Leslie M, Roche R (1990) Phenotypic variation in male guppies from natural inland populations: an additional test of Haskins’ sexual selection/predation hypthesis. Environ Biol Fishes 29:173–191Google Scholar
  119. Wolff T (2005) Composition and endemism of the deep-sea hydrothermal vent fauna. Cah Biol Mar 46:97–104Google Scholar

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© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.School of Biological Sciences, Centre for Ecology, Evolution and BehaviourRoyal Holloway University of LondonEghamUK
  2. 2.Division of BiologyKansas State UniversityManhattanUSA
  3. 3.College of Animal Science and Technology, Northwest A&F UniversityYanglingPR China

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