Advertisement

Ageing impacts phenotypic flexibility in an air-acclimated amphibious fish

  • Giulia S. Rossi
  • Paige V. Cochrane
  • Louise Tunnah
  • Patricia A. WrightEmail author
Original Paper

Abstract

The ability to tolerate environmental change may decline as fishes age. We tested the hypothesis that ageing influences the scope for phenotypic flexibility in the mangrove rivulus (Kryptolebias marmoratus), an amphibious fish that transitions between two vastly different environments, water and land. We found that older fish (4–6 years old) exhibited marked signs of ageing; older fish were reproductively senescent, had reduced fin regenerative capacity and body condition, and exhibited atrophy of both oxidative and glycolytic muscle fibers relative to younger adult fish (1–2 years old). However, age did not affect routine O2 consumption. We then acclimated adult fish (1–6 years) to water (control) or air for 10 days to assess the scope for phenotypic flexibility in response to terrestrial exposure. In support of our hypothesis, we found that older air-acclimated fish had a diminished scope for gill remodeling relative to younger fish. We also found that older fish exhibited poorer terrestrial locomotor performance relative to younger adult fish, particularly when acclimated to air. Our results indicate that ageing diminishes skeletal muscle integrity and locomotor performance of amphibious fishes, and may, therefore, impair terrestrial foraging ability, predator avoidance, or dispersal across the terrestrial environment. Remarkably, older fish voluntarily left water to a similar degree as younger fish despite the age-related deterioration of traits important for terrestrial life.

Keywords

Amphibious fish Ageing Phenotypic flexibility Gill remodeling Locomotor performance 

Notes

Acknowledgements

We thank Mike Davies, Matt Cornish, Nicole Carpenter, and numerous undergraduate volunteers for animal care. We also thank the reviewers for their helpful commentary.

Author contributions

All authors contributed to the conception and design of the study. GSR, PVC, and LT conducted the experiments, analyzed the data, and wrote the draft manuscript. All authors edited the manuscript.

Funding

Funding was provided by Natural Sciences and Engineering Research Council of Canada (NSERC) (Grant number 04218) graduate scholarships to G.S.R., P.V.C., and L.T., and an NSERC Discovery Grant to P.A.W.

Compliance with ethical standards

Conflict of interest

The authors declare no competing or financial interests.

Supplementary material

360_2019_1234_MOESM1_ESM.docx (2.1 mb)
Supplementary material 1 (DOCX 2107 kb)

References

  1. Blanchard TS, Whitehead A, Dong YW, Wright PA (2019) Phenotypic flexibility in respiratory traits is associated with improved aerial respiration in an amphibious fish out of water. J Exp Biol 222:jeb186486CrossRefGoogle Scholar
  2. Borowiec BG, Darcy KL, Gillette DM, Scott GR (2015) Distinct physiological strategies are used to cope with constant hypoxia and intermittent hypoxia in killifish (Fundulus heteroclitus). J Exp Biol 218:1198–1211CrossRefGoogle Scholar
  3. Brunt EM, Turko AJ, Scott GR, Wright PA (2016) Amphibious fish jump better on land after acclimation to a terrestrial environment. J Exp Biol 219:3204–3207CrossRefGoogle Scholar
  4. Casellas J (2011) Inbred mouse strains and genetic stability: a review. Animal 5:1–7CrossRefGoogle Scholar
  5. Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905CrossRefGoogle Scholar
  6. Comfort A (1961) The longevity and mortality of a fish (Lebistes reticularis Peters) in captivity. Gerontologia 5:209–222CrossRefGoogle Scholar
  7. Cooper CA, Litwiller SL, Murrant CL, Wright PA (2012) Cutaneous vasoregulation during short- and long-term aerial acclimation in the amphibious mangrove rivulus, Kryptolebias marmoratus. Comp Biochem Physiol B 161:268–274CrossRefGoogle Scholar
  8. Daxboeck C, Heming TA (1982) Bimodal respiration in the intertidal fish Xiphister astropurpureus (Kittlitz). Mar Behav Physiol 9:23–34CrossRefGoogle Scholar
  9. Ding L, Kuhne WW, Hinton DE, Song J, Dynan WS (2010) Quantifiable biomarkers of normal aging in the Japanese medaka fish (Oryzias latipes). PLoS One 5:e13287CrossRefGoogle Scholar
  10. Du TY, Standen EM (2017) Phenotypic plasticity of muscle fiber type in the pectoral fins of Polypterus senegalus reared in a terrestrial environment. J Exp Biol 220:3406–3410CrossRefGoogle Scholar
  11. Du SJ, Frenkel V, Kindschi G, Zohar Y (2001) Visualizing normal and defective bone development in zebrafish embryos using the fluorescent chromophore calcein. Dev Biol 238:239–246CrossRefGoogle Scholar
  12. Frick NT, Wright PA (2002) Nitrogen metabolism and excretion in the mangrove killifish Rivulus marmoratus II. Significant ammonia volatilization in a teleost during air exposure. J Exp Biol 205:91–100Google Scholar
  13. Froehlich JM, Fowler ZG, Galt NJ, Smith DL, Biga PR (2013) Sarcopenia and piscines: the case for indeterminate-growing fish as unique genetic model organisms in aging and longevity research. Front Genet 4:159CrossRefGoogle Scholar
  14. Froese R (2006) Cube law, condition factor and weight-length relationships: history, meta-analysis and recommendations. J Appl Ichthyol 22:241–253CrossRefGoogle Scholar
  15. Fu C, Cau ZD, Fu SJ (2013) The effects of caudal fin amputation on metabolic interaction between digestion and locomotion in juveniles of three cyprinid fish species with different metabolic modes. Comp Biochem Physiol A 164:456–465CrossRefGoogle Scholar
  16. Gasparini C, Marino IAM, Boschetto C, Pilastro A (2010) Effect of male age on sperm traits and sperm competition success in the guppy (Poecilia reticulata). J Evol Biol 23:124–135CrossRefGoogle Scholar
  17. Gavin TP, Ruster RS, Carrithers JA, Zwetsloot KA, Kraus RM, Evans CA, Knapp DJ, Drew JL, McCartney JS, Garry JP, Hickner RC (2007) No difference in the skeletal muscle angiogenic response to aerobic exercise training between young and aged men. J Physiol 585:231–239CrossRefGoogle Scholar
  18. Gavin TP, Kraus RM, Carrithers JP, Robert G, Hickner C (2014) Ageing and the skeletal muscle angiogenic response to exercise in women. J Gerontol 70:1189–1197CrossRefGoogle Scholar
  19. Gems D, Partridge L (2013) Genetics of longevity in model organisms: debates and paradigm shifts. Annu Rev Physiol 75:621–644CrossRefGoogle Scholar
  20. Gerhard GS, Kauffman EJ, Wang X, Stewart R, Moore JL, Kasales CJ, Demidenko E, Cheng KC (2002) Life spans and senescent phenotypes in two strains of Zebrafish (Danio rerio). Exp Gerontol 37:1055–1068CrossRefGoogle Scholar
  21. Gilmour KM, Perry SF (2018) Conflict and compromise: using reversible remodeling to manage competing physiological demands at the fish gill. Physiology (Bethesda) 33:412–422Google Scholar
  22. Gordon MS, Boëtius I, Evans DH, McCarthy R, Oglesby LC (1969) Aspects of the physiology of terrestrial life in amphibious fishes. J Exp Biol 50:141–149Google Scholar
  23. Hartmann N, Reichwald K, Wittig I, Drose S, Schmeisser S, Luck C, Hahn C, Graf M, Gausmann U, Terzibasi E, Cellerino A, Ristow M, Brandt U, Platzer M, Englert C (2011) Mitochondrial DNA copy number and function decrease with age in the short-lived fish Nothobranchius furzeri. Aging Cell 10:824–831CrossRefGoogle Scholar
  24. Hughes KA, Reynolds RM (2005) Evolutionary and mechanistic theories of aging. Annu Rev Entomol 50:421–445CrossRefGoogle Scholar
  25. Johnston IA, Dunn J (1987) Temperature acclimation and metabolism in ectotherms with particular reference to teleost fish. Symp Soc Exp Biol 41:67–93Google Scholar
  26. Johnston IA, Abercromby M, Vieira VLA, Sigursteindóttir RJ, Kristjánsson B, Sibthorpe D, Skúlason S (2004) Rapid evolution of muscle fibre number in post-glacial populations of Arctic charr. J Exp Biol 207:4343–4360CrossRefGoogle Scholar
  27. Kim Y, Nam HG, Valenzano DR (2016) The short-lived African turquoise killifish: an emerging experimental model for ageing. Dis Mod Mech 9:115–129CrossRefGoogle Scholar
  28. Kirkwood TB (1977) Evolution of ageing. Nature 270:301–304CrossRefGoogle Scholar
  29. Kirkwood TB (2005) Understanding the odd science of aging. Cell 120:437–447CrossRefGoogle Scholar
  30. Koslow JA, Bell J, Virtue P, Smith DC (1995) Fecundity and its variation in orange roughy: effects of population density, condition, egg size, and senescence. J Fish Biol 47:1063–1080CrossRefGoogle Scholar
  31. Kotrschal A, Taborsky B (2010) Environmental change enhances cognitive abilities in fish. PLoS Biol 8:e1000351CrossRefGoogle Scholar
  32. Kwak S-E, Lee J-H, Zhang D, Song W (2018) Angiogenesis: focusing on the effects of exercise in ageing and cancer. J Exerc Nutrition Biochem 22:21–26CrossRefGoogle Scholar
  33. Lähteenvuo J, Rosenzweig A (2012) Effects of aging on angiogenesis. Circ Res 110:1252–1264CrossRefGoogle Scholar
  34. Lam K, Tsui T, Nakano K, Randall DJ (2006) Physiological adaptations of fishes to tropical intertidal environments. In: Val AL, Almeida-Val VMF, Randall DJ (eds) The physiology of tropical fishes. Academic Press, San Diego, pp 502–581Google Scholar
  35. Lemaître J-F, Berger V, Bonenfant C, Douhard M, Gamelon M, Plard F, Gaillard J-M (2015) Early-late life trade-offs and the evolution of ageing in the wild. Proc R Soc B 282:20150209CrossRefGoogle Scholar
  36. Lertkiatmongkol P, Liao D, Mei H, Hu Y, Newman PJ (2016) Endothelial functions of platelet/endothelial cell adhesion molecule-1 (CD31). Curr Opin Hematol 23:253–259CrossRefGoogle Scholar
  37. Lins LSF, Trojahn S, Sockell A, Yee M-C, Tatarenkov A, Bustamante CD, Earley RL, Kelley JL (2018) Whole-genome sequencing reveals the extent of heterozygosity in a preferentially self-fertilizing hermaphroditic vertebrate. Genome 61:241–247CrossRefGoogle Scholar
  38. Livingston MD, Bhargav VV, Turko AJ, Wilson JM, Wright PA (2018) Widespread use of emersion and cutaneous ammonia excretion in Aplocheiloid killifishes. Proc R Soc B 285:20181496CrossRefGoogle Scholar
  39. Maynard S, Fang EF, Scheibye-Knudsen M, Croteau DL, Bohr VA (2015) DNA damage, DNA, repair, aging, and neurodegeneration. Cold Spring Harb Perspect Med 5:025130CrossRefGoogle Scholar
  40. Moczek AP, Sultan S, Foster S, Ledón-Rettig C, Dworkin I, Nijhout HF, Abouheif E, Pfennig DW (2011) The role of developmental plasticity in evolutionary innovation. Proc R Soc Lond B Biol Sci 278:2705–2713CrossRefGoogle Scholar
  41. Montgomery RA, Vucetich JA, Peterson RO, Roloff GJ, Millenbah KF (2012) The influence of winter severity, predation and senescence on moose habitat use. J Anim Ecol 82:301–309CrossRefGoogle Scholar
  42. Ong KJ, Stevens ED, Wright PA (2007) Gill morphology of the mangrove killifish (Kryptolebias marmoratus) is plastic and changes in response to terrestrial air exposure. J Exp Biol 210:1109–1115CrossRefGoogle Scholar
  43. Partridge L (2010) The new biology of ageing. Phil Trans R Soc B 365:147–154CrossRefGoogle Scholar
  44. Pfennig DW, Rice AM, Martin RA (2006) Ecological opportunity and phenotypic plasticity interact to promote character displacement and species coexistence. Ecology 87:769–779CrossRefGoogle Scholar
  45. Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP (2010) Phenotypic plasticity’s impacts on diversification and speciation. Trends Ecol Evol 25:459–467CrossRefGoogle Scholar
  46. Piersma T, van Gils JA (2011) The flexible phenotype: towards a body-centred integration of physiology, ecology and behaviour. Oxford University Press, Oxford, pp 82–87Google Scholar
  47. Poss KD, Wilson LG, Keating MT (2002) Heart regeneration in zebrafish. Science 298:2188–2190CrossRefGoogle Scholar
  48. Recidoro AM, Roof AC, Schmitt M, Worton LE, Petrie T, Strand N, Ausk BJ, Srinivasan S, Moon RT, Gardiner EM, Kaminsky W, Bain SD, Allan CH, Gross TS, Kwon RY (2014) Botulinum toxin induces muscle paralysis and inhibits bone regeneration in zebrafish. J Bone Min Res 29:2346–2356CrossRefGoogle Scholar
  49. Regan KS, Jonz MG, Wright PA (2011) Neuroepithelial cells and the hypoxia emersion response in the amphibious fish Kryptolebias marmoratus. J Exp Biol 214:2560–2568CrossRefGoogle Scholar
  50. Reznick DN, Ghalambor C, Nunney L (2002) The evolution of senescence in fish. Mech Ageing Dev 123:773–789CrossRefGoogle Scholar
  51. Reznick DN, Bryant MJ, Roff D, Ghalambor CK, Ghalambor DE (2004) Effect of extrinsic mortality on the evolution of senescence in guppies. Nature 431:1095–1099CrossRefGoogle Scholar
  52. Rodela TM, Wright PA (2006) Metabolic and neuroendocrine effects on diurnal urea excretion in the mangrove killifish Rivulus marmoratus. J Exp Biol 209:2704–2712CrossRefGoogle Scholar
  53. Rossi GS, Turko AJ, Wright PA (2018) Oxygen drives skeletal muscle remodeling in an amphibious fish out of water. J Exp Biol 221:jeb18025Google Scholar
  54. Rossi GR, Tunnah L, Martin KE, Turko AJ, Taylor DS, Currie S, Wright PA (2019) Mangrove fishes rely on emersion behaviour and physiological tolerance to persist in sulfidic environments. Physiol Biochem Zool 92:316–325CrossRefGoogle Scholar
  55. Sayer MDJ, Davenport J (1991) Amphibious fish: Why do they leave water? Rev Fish Biol Fish 1:159–181CrossRefGoogle Scholar
  56. Scarnecchia DL, Ryckman LF, Lim Y, Power GJ, Schmitz BJ, Firehammer JA (2007) Life-history and the costs of reproduction in Northern Great Plains Paddlefish (Polyodon spathula) as a potential framework for other Acipenseriform fishes. Rev Fish Sci 15:211–263CrossRefGoogle Scholar
  57. Sîrbulescu RF, Ilies I, Zupanc GK (2009) Structural and functional regeneration after spinal cord injury in the weakly electric teleost fish, Apteronotus leptorhynchus. J Comp Physiol A 195:699–714CrossRefGoogle Scholar
  58. Styga JM, Houslay TM, Wilson AJ, Earley RL (2018) Ontogeny of the morphology-performance axis in an amphibious fish (Kryptolebias marmoratus). J Exp Zool 327:620–634CrossRefGoogle Scholar
  59. Sullivan GM, Feinn R (2012) Using effect size—or why the p value is not enough. J Grad Med Educ 4:279–282CrossRefGoogle Scholar
  60. Sutton AO, Turko AJ, McLaughlin RL, Wright PA (2018) Behavioural and physiological responses of an amphibious, euryhaline mengrove fish to acute salinity exposure. Copeia 106:305–311CrossRefGoogle Scholar
  61. Tatarenkov A, Ring BC, Elder JF, Bechler DL, Avise JC (2010) Genetic composition of laboratory stocks of the self-fertilizing fish Kryptolebias marmoratus: a valuable resource for experimental research. PLoS One 5:e12863CrossRefGoogle Scholar
  62. Taylor DS (1990) Adaptive specializations of the cyprinodont fish Rivulus marmoratus. Fla Sci 53:239–248Google Scholar
  63. Taylor DS (1992) Diet of the killifish Rivulus marmoratus collected from land crab burrows, with further ecological notes. Env Biol Fish 33:389–393CrossRefGoogle Scholar
  64. Taylor DS (2012) Twenty-four years in the mud: what have we learned about the natural history and ecology of the mangrove rivulus, Kryptolebias marmoratus? Integr Comp Biol 52:724–736CrossRefGoogle Scholar
  65. Terzibasi E, Valenzano DR, Benedetti M, Roncaglia P, Cattaneo A, Domenici L, Cellerino A (2008) Large differences in aging phenotype between strains of the short-lived annual fish Nothobranchius furzeri. PLoS One 3:e3866CrossRefGoogle Scholar
  66. Thorpe JE (1994) Reproductive strategies in Atlantic salmon, Salmo salar L. Aquacult Fish Manage 25:77–87Google Scholar
  67. Tozzini ET, Baumgart M, Battistoni G, Cellerino A (2012) Adult neurogenesis in the short-lived teleost Nothobranchius furzeri: localization of neurogenic niches, molecular characterization and effects of aging. Aging Cell 11:241–251CrossRefGoogle Scholar
  68. Turko AJ, Earley RL, Wright PA (2011) Behaviour drives morphology: voluntary emersion patterns shape gill structure in genetically identical mangrove rivulus. Anim Behav 82:39–47CrossRefGoogle Scholar
  69. Turko AJ, Cooper CA, Wright PA (2012) Gill remodelling during terrestrial acclimation reduces aquatic respiratory function of the amphibious fish Kryptolebias marmoratus. J Exp Biol 215:3973–3980CrossRefGoogle Scholar
  70. Turko AJ, Robertson CE, Bianchini K, Freeman M, Wright PA (2014) The amphibious fish Kryptolebias marmoratus uses different strategies to maintain oxygen delivery during aquatic hypoxia and air exposure. J Exp Biol 217:3988–3995CrossRefGoogle Scholar
  71. Turko AJ, Kültz D, Fudge D, Croll RP, Smith FM, Stoyek MR, Wright PA (2017) Skeletal stiffening in an amphibious fish out of water is a response to increased body weight. J Exp Biol 220:3621–3631CrossRefGoogle Scholar
  72. Turko AJ, Tatarenkov A, Currie S, Earley RL, Platek A, Taylor DS, Wright PA (2018) Emersion behaviour underlies variation in gill morphology and aquatic respiratory function in the amphibious fish Krytolebias marmoratus. J Exp Biol 221:168039CrossRefGoogle Scholar
  73. Turko AJ, Maini P, Wright PA, Standen EM (2019) Gill remodeling during terrestrial acclimation in the amphibious fish Polypterus senegalus. J Morphol 280:329–338CrossRefGoogle Scholar
  74. Valdesalici S, Cellerino A (2003) Extremely short lifespan in the annual fish Nothobranchius furzeri. Proc Biol Sci 270(Suppl 2):S189–S191Google Scholar
  75. Valenzano DR, Terzibasi E, Cattaneo A, Domenici L, Cellerino A (2006) Temperature affects longevity and age-related locomotor and cognitive decay in the short-lived fish Nothobranchius furzeri. Aging Cell 5:275–278CrossRefGoogle Scholar
  76. Vijg J, Campisi J (2008) Puzzles, promises and a cure for ageing. Nature 454:1065–1071CrossRefGoogle Scholar
  77. Weatherley A, Gill H (1987) Biology of fish growth. Academic Press, San DiegoGoogle Scholar
  78. Wendler S, Hartmann N, Hoppe B, Englert C (2015) Age-dependent decline in fin regenerative capacity in the short-lived fish Nothobranchius furzeri. Aging Cell 14:857–866CrossRefGoogle Scholar
  79. Wright PA (2012) Environmental physiology of the mangrove rivulus, Kryptolebias marmoratus, a cutaneously breathing fish that survives for weeks out of water. Integr Comp Biol 52:792–800CrossRefGoogle Scholar
  80. Wright PA, Turko AJ (2016) Amphibious fishes: evolution and phenotypic plasticity. J Exp Biol 219:2245–2259CrossRefGoogle Scholar
  81. Turko AJ, Doherty JE, Lin-Liao I, Levesque K, Kruth P, Holden JM, Early RL, Wright PA (submitted) Prolonged survival out of water is linked to a generally slow pace of life in a selfing amphibious fishGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Integrative BiologyUniversity of GuelphGuelphCanada

Personalised recommendations