Advertisement

Age-associated liver alterations in wild populations of Austrolebias minuano, a short-lived Neotropical annual killifish

  • Robson S. Godoy
  • Luis Esteban K. Lanés
  • Vinicius Weber
  • Cristina Stenert
  • Héctor G. Nóblega
  • Guendalina T. Oliveira
  • Leonardo MaltchikEmail author
Research Article

Abstract

Aging processes have become an attractive field for researchers and annual fish have been used as biological models. However, the study on the changes in age-associated markers during the normal aging in wild populations of annual fish remains open. Austrolebias is a genus of Neotropical annual killifishes, distributed mainly in ephemeral pools across grassland floodplains of temperate South America and represent an emerging biological model for aging research, but studies investigating rapid aging and senescence in this genus of annual fish are almost non-existent. This study was undertaken to examine the changes in age-associated liver markers at the different developmental stages in wild populations of Austrolebias minuano. We demonstrate that A. minuano has a number of liver alterations of different severities throughout the life cycle, suggesting that these changes tend to increase with age. Our results revealed that > 70% of the analyzed livers presented alterations. Thus, our study should instigate new approaches on aging using Neotropical annual fish, and could be useful to improve the knowledge already provided by consecrated biological aging models as e.g. Nothobranchius killifishes.

Keywords

Annual fish Neoplasia Steatosis Temporary ponds Liver diseases 

Notes

Acknowledgements

The authors are grateful to private landowners for granting access to their properties, Lagoa do Peixe National Park administration for granting research permits and ICMBio for obtaining the license. The authors also thank Marlon Ferraz for providing the map of the study area. The annual killifish collections complied with current Brazilian law (SISBIO 43251-1) and the histological procedures were authorized by the PUCRS Ethic Committee (CEUA PUCRS 8271).

References

  1. Ackerman HD, Gerhard GS (2018) Piscine polemics: small tropical fish species as models for aging research. In: Ram JL, Conn MP (eds) Conn’s handbook of models for human aging, 2nd edn. Academic Press, Massachusetts, pp 361–375CrossRefGoogle Scholar
  2. Baumgart M, Di Cicco E, Rossi G, Cellerino A, Tozzini ET (2015) Comparison of captive lifespan, age-associated liver neoplasias and age dependent gene expression between two annual fish species: nothobranchius furzeri and Nothobranchius korthause. Biogerontology 16:63–69CrossRefGoogle Scholar
  3. Belote DF, Costa WJEM (2004) Reproductive behavior patterns in three species of the South American annual fish genus Austrolebias Costa, 1998 (Cyprinodontiformes, Rivulidae). Bol Mus Nac 514:1–7Google Scholar
  4. Berois N, Arezo MJ, De Sá RO (2014) The neotropical genus Austrolebias: an emerging model of annual killifishes. Cell Dev Biol 3:1000136Google Scholar
  5. Blažek R, Polačik M, Reichard M (2013) Rapid growth, early maturation and short generation time in African annual fishes. EvoDevo 4:24CrossRefGoogle Scholar
  6. Blažek R, Polačik M, Kačer P, Cellerino A, Řežucha R, Methling C, Vrtílek M (2017) Repeated intraspecific divergence in life span and aging of African annual fishes along an aridity gradient. Evolution 71:386–402CrossRefGoogle Scholar
  7. Cellerino A, Valenzano DR, Reichard M (2016) From the bush to the bench: the annual Nothobranchius fishes as a new model system in biology. Biol Rev Camb Philos Soc 91:511–533CrossRefGoogle Scholar
  8. Comfort A (1961) The longevity and mortality of a fish (Lebistes reticulatus Peters) in captivity. Gerontology 5:209–222CrossRefGoogle Scholar
  9. Cooper EL, Zapata A, García-barrutia M, Ramírez JA (1983) Aging changes in lymphopoietic and myelopoietic organs of the annual cyprinodont fish, Nothobranchius guentheri. Exp Gerontol 18:29–38CrossRefGoogle Scholar
  10. Da Rocha CAM, Moreira-Nunes CA, Da Rocha SM, Da Silva MAS, Burbano RRA (2018) Review on occurrence of neoplasia in fish. Acta Fish 5:19–24Google Scholar
  11. Davis T, Skinner JW, Faragher RG, Jones CJ, Kipling D (2005) Replicative senescence in sheep fibroblasts is a p53 dependent process. Exp Gerontol 40:17–26CrossRefGoogle Scholar
  12. Di Cicco E, Tozzini ET, Rossi G, Cellerino A (2011) The short-lived annual fish Nothobranchius furzeri shows a typical teleost aging process reinforced by high incidence of age-dependent neoplasias. Exp Gerontol 46:249–256CrossRefGoogle Scholar
  13. Egami N (1980) Environment and aging: an approach to the analysis of aging mechanisms using poikilothermic vertebrates. Adv Exp Med Biol 129:249–259CrossRefGoogle Scholar
  14. García D, Loureiro M, Tassino B (2008) Reproductive behavior in the annual fish Austrolebias reicherti Loureiro & García 2004 (Cyprinodontiformes: Rivulidae). Neotrop Ichthyol 6:243–248CrossRefGoogle Scholar
  15. Genade T, Benedetti M, Tozzini TE, Roncaglia P, Valenzano DR, Cattaneo A, Cellerino A (2005) Annual fishes of the genus Nothobranchius as a model system for aging research. Aging Cell 4:223–233CrossRefGoogle Scholar
  16. Gerhard GS (2007) Small laboratory fish as models for aging research. Ageing Res Rev 6:64–72CrossRefGoogle Scholar
  17. 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
  18. Gonçalves CDS, Souza UP, Volcan MV (2011) The opportunistic feeding and reproduction strategies of the annual fish Cynopoecilus melanotaenia (Cyprinodontiformes: Rivulidae) inhabiting ephemeral habitats on southern Brazil. Neotrop Ichthyol 9:191–200CrossRefGoogle Scholar
  19. Guarente L, Kenyon C (2000) Genetic pathways that regulate ageing in model organisms. Nature 408:255–262CrossRefGoogle Scholar
  20. Hastings R, Li NC, Lacy PS, Patel H, Herbert KE, Stanley AG, Williams B (2004) Rapid telomere attrition in cardiac tissue of the ageing Wistar rat. Exp Gerontol 39:855–857CrossRefGoogle Scholar
  21. Herrera M, Jagadeeswaran P (2004) Annual fish as a genetic model for aging. J Gerontol A 59:101–107CrossRefGoogle Scholar
  22. Hsu CY, Chiu YC (2009) Ambient temperature influences aging in an annual fish (Nothobranchius rachovii). Aging Cell 8:726–773CrossRefGoogle Scholar
  23. Hsu CY, Chiu YC, Hsu WL, Chan YP (2008) Age-related markers assayed at different developmental stages of the annual fish Nothobranchius rachovii. J Gerontol A 63:1267–1276CrossRefGoogle Scholar
  24. Hu CK, Brunet A (2018) The African turquoise killifish: a research organism to study vertebrate aging and diapause. Aging Cell 17:e12757CrossRefGoogle Scholar
  25. IBGE (2004) Mapa da vegetação do Brasil e mapa dos biomas do Brasil. http://www.ibge.gov.br. Accessed 8 Aug 2018
  26. Johnson TE (2003) Advantages and disadvantages of Caenorhabditis elegans for aging research. Exp Gerontol 38:1329–1332CrossRefGoogle Scholar
  27. Jones OR, Vaupel JW (2017) Senescence is not inevitable. Biogerontology 18:965–971CrossRefGoogle Scholar
  28. Katic M, Kahn CR (2005) The role of insulin and IGF-1 signaling in longevity. Cell Mol Life Sci 62:320–343CrossRefGoogle Scholar
  29. Keppeler FW, Lanés LEK, Rolon AS, Stenert C, Maltchik L (2013) The diet of Cynopoecilus fulgens Costa, 2002 (Cyprinodontiformes: Rivulidae) in Southern Brazil wetlands. Ital J Zool 80:291–302CrossRefGoogle Scholar
  30. Keppeler FW, Lanés LEK, Rolon AS, Stenert C, Lehmann P, Reichard M, Maltchik L (2015) The morphology–diet relationship and its role in the coexistence of two species of annual fishes. Ecol Freshw Fish 24:77–90CrossRefGoogle Scholar
  31. Keppeler FW, Cruz DA, Dalponti G, Mormul RP (2016) The role of deterministic factors and stochasticity on the trophic interactions between birds and fish in temporary floodplain ponds. Hydrobiologia 773:225–240CrossRefGoogle Scholar
  32. Kirkwood TBL, Austad SN (2000) Why do we age? Nature 408:233–238CrossRefGoogle Scholar
  33. Kishi S (2004) Functional aging and gradual senescence in zebrafish. Ann N Y Acad Sci 1019:521–526CrossRefGoogle Scholar
  34. Lanés LEK, Keppeler FW, Maltchik L (2012) Abundance, sex-ratio, length-weight relation, and condition factor of non-annual killifish Atlantirivulus riograndensis (Actinopterygii: Cyprinodontiformes: Rivulidae) in Lagoa do Peixe National Park, a ramsar site of southern Brazil. Acta Ichtyol Pisc 42(3):247–252CrossRefGoogle Scholar
  35. Lanés LEK, Keppeler FW, Maltchik L (2014) Abundance variations and life history traits of two sympatric species of neotropical annual fish (Cyprinodontiformes: Rivulidae) in temporary ponds of southern Brazil. J Nat Hist 48:1971–1988CrossRefGoogle Scholar
  36. Lanés LEK, Rolon AS, Stenert C, Maltchik L (2015) Effects of an artificial and annual opening of a natural sandbar on the fish community in a coastal lagoon system: a case study in Lagoa do Peixe floodplains, southern Brazil. J Appl Ichthyol 31:321–327CrossRefGoogle Scholar
  37. Lanés LEK, Godoy RS, Maltchik L, Polačik M, Blažek R, Vrtílek M, Reichard M (2016) Seasonal dynamics in community structure, abundance, body size and sex ratio in two species of Neotropical annual fishes. J Fish Biol 89:2345–2364CrossRefGoogle Scholar
  38. Lanés LEK, Reichard M, de Moura RG, Godoy RS, Maltchik L (2018) Environmental predictors for annual fish assemblages in subtropical grasslands of South America: the role of landscape and habitat characteristics. Environ Biol Fish 101:963–977CrossRefGoogle Scholar
  39. Liu RK, Walford RL (1972) The effect of lowered body temperature on lifespan and immune and non-immune processes. Gerontologia 18:363–388CrossRefGoogle Scholar
  40. Liu RK, Walford RL (1975) Mid-life temperature-transfer effects on lifespan of annual fish. J. Gerontol 30:129–131CrossRefGoogle Scholar
  41. Liu RK, Leung BE, Walford RL (1975) Effect of temperature-transfer on growth of laboratory populations of a South American annual fish Cynolebias bellottii. Growth 39:337–343Google Scholar
  42. Loureiro M, de Sá RO, Serra SW, Alonso F, Lanés LEK, Volcan MV, Calviño P, Nielsen D, Duarte A, Garcia G (2018) Review of the family Rivulidae (Cyprinodontiformes, Aplocheiloidei) and a molecular and morphological phylogeny of the annual fish genus Austrolebias Costa 1998. Neotrop Ichthyol 16(3):e180007CrossRefGoogle Scholar
  43. Lucas-Sanchéz A, Almaiada-Pagán PF, Mendiola P, Costa J (2014) Nothobranchius as a model for aging studies. A review. Aging Dis 5:281–291Google Scholar
  44. Markofsky J, Milstoc M (1979) Aging changes in the liver of the male annual cyprinodont fish, Nothobranchius guentheri. Exp Gerontol 14:11–20CrossRefGoogle Scholar
  45. Masoro EJ, Austad EN (2010) Handbook of the biology of aging. Academic Press, CambridgeGoogle Scholar
  46. Muck J, Kean S, Valenzano DR (2018) The short-lived African turquoise killifish (Nothobranchius furzeri): a new model system for research on aging. In: Ram JL, Conn MP (eds) Conn’s handbook of models for human aging, 2nd edn. Academic Press, Massachusetts, pp 377–386CrossRefGoogle Scholar
  47. Nasir L, Devlin P, Mckevitt T, Rutteman G, Argyle DJ (2001) Telomere lengths and telomerase activity in dog tissues: a potential model system to study human telomere and telomerase biology. Neoplasia 3:351–359CrossRefGoogle Scholar
  48. Passos C, Tassino B, Reyes F, Rosenthal GG (2013) Seasonal variation in female mate choice and operational sex ratio in wild populations of an annual fish. Austrolebias reicherti, PLoS ONE, p e101649Google Scholar
  49. Passos C, Tassino B, Reyes F, Rosenthal GG (2014) Intra- and intersexual selection on male body size in the annual killifish Austrolebias. Behav Process 96:20–26CrossRefGoogle Scholar
  50. Passos C, Tassino B, Rosenthal GG, Reichard M (2015) Reproductive behavior and sexual selection in annual fishes. In: Berois N, García G, De Sá R (eds) Annual fishes: life history strategy, diversity, and evolution, 1st edn. CRC Press, Boca Raton, pp 201–223Google Scholar
  51. Patnaik BK, Mahapatro NM, Jena BS (1994) Ageing in fishes. Gerontology 40:113–132CrossRefGoogle Scholar
  52. Podrabsky JE, Hrbek T, Hand SC (1998) Physical and chemical characteristics of ephemeral pond habitats in the Maracaibo basin and Llanos region of Venezuela. Hydrobiologia 362:67–78CrossRefGoogle Scholar
  53. Poleksic V, Mitrovic-Tutundzic V (1994) Fish gills as a monitor of sublethal and chronic effects of pollution. In: Müller R, Lloyd R (eds) Sublethal and chronic effects of pollutants on freshwater fish. Fishing News Books, Oxford, pp 339–352Google Scholar
  54. Reichard M (2016) Evolutionary ecology of aging: time to reconcile field and laboratory research. Ecol Evol 6:2988–3000CrossRefGoogle Scholar
  55. Reichard M, Polacik M, Sedlacek O (2009) Distribution, colour polymorphism and habitat use of the African killifish Nothobranchius furzeri, the vertebrate with the shortest life span. J Fish Biol 74:198–212CrossRefGoogle Scholar
  56. Reichard M, Polacik M, Blazek R, Vrtilek M (2014) Female bias in the adult sex ratio of African annual fishes: interspecific differences, seasonal trends and environmental predictors. Evol Ecol 28:1105–1120CrossRefGoogle Scholar
  57. Reichard M, Lanés LE, Polačik M, Blažek R, Vrtílek M, Godoy RS, Maltchik L (2018) Avian predation mediates size-specific survival in a Neotropical annual fish: a field experiment. Biol J Linnean Soc 124:56–66CrossRefGoogle Scholar
  58. Rudolph KL, Chang S, Lee HW, Blasco M, Gottlieb GJ, Gleider C, Depinho RA (1999) Longevity, stress response, and cancer in aging telomerase-deficient mice. Cell 96:701–712CrossRefGoogle Scholar
  59. Silva GG, Weber V, Green AJ, Hoffmann P, Silva VS, Volcan M, Lanés LEK, Stenert C, Reichard M, Maltchik L (2019) Killifish eggs can disperse via gut passage through waterfowl. Ecology.  https://doi.org/10.1002/ecy.2774 Google Scholar
  60. Stegeman JJ, Lech JJ (1991) Cytochrom p- 450 monoocygenase systems in aquatic species: carcinogen metabolism and biomarkers for carcinogen and pollutant exposure. Environ Health Persp 90:93–100Google Scholar
  61. Stenert C, Bacca RC, Mostardeiro CC, Maltchik L (2008) Environmental predictors of macroinvertebrate communities in coastal wetlands of southern Brazil. Mar Freshwater Res 59:540–548CrossRefGoogle Scholar
  62. Systat (2007) Systat Software. Richmond, CaliforniaGoogle Scholar
  63. Tagliani PRA (1995) Estratégia de planificação ambiental para o sistema ecológico da Restinga da Lagoa dos Patos-Planicie Costeira do Rio Grande do Sul. Dissertation, Universidade de São CarlosGoogle Scholar
  64. Tozzini TE, Valenzano DR, Benedetti M, Roncagli 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
  65. Valenzano DR, Terzibasi E, Genade T, Cattaneo A, Domenici L, Cellerino A (2006) Resveratrol prolongs lifespan and retards the onset of age-related markers in a short-lived vertebrate. Curr Biol 16:296–300CrossRefGoogle Scholar
  66. Volcan MV, Gonçalves ÂC, Guadagnin DL (2018) Body size and population dynamics of annual fishes from temporary wetlands in Southern Brazil. Hydrobiologia 827:367–378CrossRefGoogle Scholar
  67. Vrtílek M, Reichard M (2015) Highly plastic resource allocation to growth and reproduction in females of an African annual fish. Ecol Freshw Fish 24:616–628CrossRefGoogle Scholar
  68. Vrtílek M, Žák J, Polačik M, Blažek R, Reichard M (2018) Longitudinal demographic study of wild populations of African annual killifish. Sci Rep 8:4774CrossRefGoogle Scholar
  69. Walford RL, Liu RK, Troup G, Hsiu J (1969) Alterations in soluble/insoluble collagen ratios in the annual fish, Cynolebias bellottii, in relation to age and environmental temperature. Exp Gerontol 4:103–109CrossRefGoogle Scholar
  70. Woodhead AD (1998) Aging, the fishy side: an appreciation of Alex Comfort’s studies. Exp Gerontol 33:39–51CrossRefGoogle Scholar
  71. Wootton RJ, Smith C (2014) Reproductive biology of teleost fishes. Wiley, OxfordCrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Laboratory of Ecology and Conservation of Aquatic EcosystemsUNISINOS UniversitySão Leopoldo, Rio Grande Do SulBrazil
  2. 2.Laboratório de Fisiologia da ConservaçãoPontifícia Universidade Católica do Rio Grande do Sul (PUCRS)Porto AlegreBrazil

Personalised recommendations