Aquatic Sciences

, Volume 74, Issue 1, pp 171–178 | Cite as

Exposing local adaptation: synergistic stressors elicit population-specific lactate dehydrogenase-B (ldh-b) expression profiles in Australian barramundi, Lates calcarifer

  • Richard C. EdmundsEmail author
  • Carolyn Smith-Keune
  • Lynne van Herwerden
  • Christopher J. Fulton
  • Dean R. Jerry
Research Article


The molecular response of fish to independently and/or concurrently applied ecological stressors (e.g. thermal and/or aerobic stress) can be quantified at the level of transcript abundance (i.e. gene expression). In temperate fish, the expression of the metabolic candidate gene lactate dehydrogenase-B (ldh-b) responds to both aerobic swimming challenge and extended acclimation to various ecologically relevant temperatures. We examined hepatic ldh-b expression in juvenile Lates calcarifer from two geographically, genetically and thermally distinct Australian populations to determine if similar environmental stressors also influence the transcription of this locus in a tropical fish. Hepatic ldh-b expression was quantified following 28-day acclimation to ecologically relevant temperatures (20, 25, 30 and 35°C). Expression was also quantified in L. calcarifer subjected to aerobic swimming challenge at these temperatures. Fish from southern (high latitude) and northern (low latitude) populations within this species’ Australian distribution exhibited a significant increase in hepatic ldh-b expression following aerobic swimming challenge at native temperatures of 25 and 30°C, respectively (p < 0.001). Southern and northern fish also exhibited significant increase in hepatic ldh-b expression (p < 0.001 and p < 0.01, respectively) following 28-day acclimation to heat-stress (35°C). However, only southern fish exhibited significant increase in expression (p < 0.001) following 28-day acclimation to cold-stress (20°C). The novel evidence presented herein suggests that (a) transcription of hepatic ldh-b is responsive to both aerobic and thermal stress when applied independently, and (b) southern Australian L. calcarifer populations may be locally adapted to cooler seasonal water temperatures.


Thermal tolerance Thermal stress Aerobic challenge Local adaptation 



Thanks to Dianne Rowe (JCU) for laboratory assistance and Bill Foley (ANU) for storage and transportation of tissue samples. This research was funded by the Research Advancement Program in Finfish Aquaculture Grant (LvH and DRJ).


  1. Basu N, Todgham AE, Ackerman PA, Bibeau MR, Nakano K, Schulte PM, Iwama GK (2002) Heat shock protein genes and their functional significance in fish. Gene 295:173–183PubMedGoogle Scholar
  2. Beitinger TL, Bennett WA (2000) Quantification of the role of acclimation temperature in temperature tolerance of fishes. Environ Biol Fish 58:277–288Google Scholar
  3. Beitinger TL, Bennett WA, McCauley RW (2000) Temperature tolerances of North American freshwater fishes exposed to dynamic changes in temperature. Environ Biol Fish 58(2000):237–275Google Scholar
  4. Bustin SA (2000) Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J Mol Endocrinol 25:169–193PubMedGoogle Scholar
  5. Bustin SA, Nolan T (2004) Pitfalls of quantitative real-time reverse-transcription polymerase chain reaction. J Biomol Tech 15:155–166PubMedGoogle Scholar
  6. Bustin SA, Benes V, Nolan T, Pfaffl MW (2005) Quantitative real-time RT-PCR—a perspective. J Mol Endocrinol 34:597–601PubMedGoogle Scholar
  7. Chenoweth SF, Hughes JM, Keenan CP, Lavery S (1998) When oceans meet: a teleost shows secondary intergradation at an Indian-Pacific Interface. Proc R Soc Lond B Biol Sci 265(1394):415–420Google Scholar
  8. Claireaux G, Couturier C, Groison AL (2006) Effect of temperature on maximum swimming speed and cost of transport in juvenile European sea bass (Dicentrarchus labrax). J Exp Biol 209:3420–3428PubMedGoogle Scholar
  9. Crawford DL, Powers DA (1992) Evolutionary adaptation to different thermal environments via transcriptional regulation. Mol Biol Evol 9(5):806–813PubMedGoogle Scholar
  10. DiMichele L, Powers DA (1982) Physiological basis for swimming endurance differences between LDH-B genotypes of Fundulus heteroclitus. Science 216(4549):1014–1016PubMedGoogle Scholar
  11. Douglas SE (2006) Microarray studies of gene expression in fish. OMICS J Integ Biol 10(4):474–489Google Scholar
  12. Doupé RG, Horwitz P, Lymbery AJ (1999) Mitochondrial genealogy of Western Australian barramundi: applications of inbreeding coefficients and coalescent analysis for separating temporal population processes. J Fish Biol 54:1197–1209Google Scholar
  13. Edmunds RC (2009) Evidence for thermal adaptation among geographically, genetically and thermally distinct populations of the Australian barramundi, Lates calcarifer (Bloch 1790): a multi-level approach. Ph.D. Dissertation, James Cook UniversityGoogle Scholar
  14. Edmunds RC, van Herwerden L, Smith-Keune C, Jerry D (2009a) Comparative characterization of a temperature responsive gene (lactate dehydrogenase-B, ldh-b) in two congeneric tropical fish, Lates calcarifer and Lates niloticus. Int J Biol Sci 5:558–569PubMedGoogle Scholar
  15. Edmunds RC, Hillersøy G, Momigliano P, van Herwerden L (2009b) Classic approach revitalizes genomics: complete characterization of a candidate gene for thermal adaptation in two coral reef fishes. Mar Gen 2:215–222Google Scholar
  16. Edmunds RC, van Herwerden L, Fulton CJ (2010) Population-specific locomotor phenotypes are displayed by barramundi Lates calcarifer in response to thermal stress. Can J Fish Aquat Sci 67:1068–1074Google Scholar
  17. Fangue NA, Mandic M, Richards JG, Schulte PM (2008) Swimming performance and energetics as a function of temperature in killifish Fundulus heteroclitus. Physiol Biochem Zool 81(4):389–401PubMedGoogle Scholar
  18. Fulton CJ (2007) Swimming speed performance in coral reef fishes: field validations reveal distinct functional groups. Coral Reefs 26:217–228Google Scholar
  19. Fulton CJ (2010) The role of swimming in reef fish ecology. In: Domenici P, Kapoor BG (eds) Fish locomotion: an eco-ethological perspective. Science Publishers, Enfield, pp 374–406Google Scholar
  20. Gracey AY, Fraser EJ, Li W, Fang Y, Taylor RR, Rogers J, Brass A, Cossins AR (2004) Coping with cold: an integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate. Proc Nati Acad Sci USA 101(48):16970–16975Google Scholar
  21. Herbert NA, Steffensen JF (2005) The response of Atlantic cod, Gadus morhua, to progressive hypoxia: fish swimming speed and physiological stress. Mar Biol 147:1403–1412Google Scholar
  22. Jain KE, Farrell AP (2003) Influence of seasonal temperature on the repeat swimming performance of rainbow trout Oncorhynchus mykiss. J Exp Biol 206:3569–3579PubMedGoogle Scholar
  23. Jonassen TM, Imsland AK, Stefansson SO (1999) The interaction of temperature and fish size on growth of juvenile halibut. J Fish Biol 54:556–572Google Scholar
  24. Ju Z, Dunham RA, Lui Z (2002) Differential gene expression in the brain of channel catfish (Ictalurus punctatus) in response to cold acclimation. Mol Genet Genomics 268:87–95PubMedGoogle Scholar
  25. Kassahn KS, Caley MJ, Ward AC, Connolly AR, Stone G, Crozier RH (2007a) Heterologous microarray experiments used to identify the early gene response to heat stress in a coral reef fish. Mol Ecol 16:1749–1763PubMedGoogle Scholar
  26. Kassahn KS, Crozier RH, Ward AC, Stone G, Caley MJ (2007b) From transcriptome to biological function: environmental stress in an ectothermic vertebrate, the coral reef fish Pomacentrus moluccensis. BMC Genomics 8:358PubMedGoogle Scholar
  27. Katersky RS, Carter CG (2005) Growth efficiency of juvenile barramundi, Lates calcarifer, at high temperatures. Aquaculture 250:775–780Google Scholar
  28. Katersky RS, Carter CG (2007) High growth efficiency occurs over a wide temperature range for juvenile barramundi Lates calcarifer fed a balanced diet. Aquaculture 272:444–450Google Scholar
  29. Keenan CP (1994) Recent evolution of population structure in Australian barramundi, Lates calcarifer (Bloch): an example of isolation by distance in one dimension. Aust J Mar Freshw Res 45:1123–1148Google Scholar
  30. Keenan CP (2000) Should we allow human-induced migration of the Indo-West Pacific fish, barramundi Lates calcarifer (Bloch) within Australia? Aquaculture Res 31:121–131Google Scholar
  31. Korsmeyer KE, Steffensen JF, Herskin J (2002) Energetics of median and paired fin swimming, body and caudal fin swimming, and gait transition in parrotfish (Scarus schlegeli) and triggerfish (Rhinecanthus aculeatus). J Exp Biol 205:1253–1263PubMedGoogle Scholar
  32. Lucassen M, Koschnick N, Eckerle LG, Pörtner H-O (2006) Mitochondrial mechanisms of cold adaptation in cod (Gadus morhua L.) populations from different climatic zones. J Exp Biol 209:2462–2471PubMedGoogle Scholar
  33. Meeuwig MH, Dunham JB, Hayes JP, Vinyard GL (2004) Effects of constant and cyclical thermal regimes on growth and feeding of juvenile cutthroat trout of variable sizes. Ecol Freshw Fish 13:208–216Google Scholar
  34. Munday PL, Kingsford MG, O’Callaghan M, Donelson JM (2008) Elevated temperature restricts growth potential of the coral reef fish Acanthochromis polyacanthus. Coral Reefs 27:927–931Google Scholar
  35. Newton JR, Smith-Keune C, Jerry DR (2010) Thermal tolerance varies in tropical and sub-tropical populations of barramundi (Lates calcarifer) consistent with local adaptation. Aquaculture 308:S128–S132Google Scholar
  36. Picard DJ, Schulte PM (2004) Variation in gene expression in response to stress in two populations of Fundulus heteroclitus. Comp Biochem Physiol A 137(2004):205–216PubMedGoogle Scholar
  37. Place AR, Powers DA (1984a) Purification and Characterization of the Lactate Dehydrogenase (LDH-B4) allozymes of Fundulus heteroclitus. J Biol Chem 259:1299–1308PubMedGoogle Scholar
  38. Place AR, Powers DA (1984b) Kinetic characterization of the lactate dehydrogenase (LDH-B4) allozymes of Fundulus heteroclitus. J Biol Chem 259:1309–1318PubMedGoogle Scholar
  39. Plaut I (2001) Critical swimming speed: its ecological relevance. Comp Biochem Physiol A 131:41–50Google Scholar
  40. Podrabsky JE, Somero GN (2004) Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish Austrofundulus limnaeus. J Exp Biol 207:2237–2254PubMedGoogle Scholar
  41. Podrabsky JE, Javillonar C, Hand SC, Crawford DL (2000) Intraspecific variation in aerobic metabolism and glycolytic enzyme expression in heart ventricles. Am J Physiol Regul Integr Comp Physiol 279:2344–2348Google Scholar
  42. Pörtner H-O, Bock C, Knust R, Lannig G, Lucassen M, Mark FC, Sartoris FJ (2008) Cod and climate in a latitudinal cline: physiological analyses of climate effects in marine fishes. Clim Res 37:253–270Google Scholar
  43. Powers DA, Schulte PM (1998) Evolutionary adaptations of gene structure and expression in natural populations in relation to a changing environment: a multidisciplinary approach to address the million-year saga of a small fish. J Exp Zool Comp Exp Biol 282:71–94Google Scholar
  44. Rees BB, Bowman JAL, Schulte PM (2001) Structure and sequence conservation of a putative hypoxia response element in the lactate dehydrogenase-B gene of Fundulus. Biol Bull 200:247–251PubMedGoogle Scholar
  45. Russell DJ, Garrett RN (1985) Early life history of barramundi, Lates calcarifer (Bloch), in northeastern Queensland. Aust J Mar Freshwat Res 36:191–201Google Scholar
  46. Schulte PM (2001) Environmental adaptations as windows on molecular evolution. Comp Biochem Physiol B Biochem Mol Biol 128:597–611PubMedGoogle Scholar
  47. Schulte PM, Glemet HC, Fiebig AA, Powers DA (2000) Adaptive variation in lactate dehydrogenase-B gene expression: role of a stress-responsive regulatory element. Proc Nati Acad Sci USA 97(12):6597–6602Google Scholar
  48. Segal JA, Crawford DL (1994) LDH-B enzyme expression: the mechanisms of altered gene expression in acclimation and evolutionary adaptation. Am J Physiol Regul Integr Comp Physiol 267:1150–1153Google Scholar
  49. Virani NA, Rees BB (2000) Oxygen consumption, blood lactate and inter-individual variation in the gulf killifish, Fundulus grandis, during hypoxia and recovery. Comp Biochem Physiol A 126:397–405Google Scholar

Copyright information

© Springer Basel AG 2011

Authors and Affiliations

  • Richard C. Edmunds
    • 1
    • 2
    • 3
    Email author
  • Carolyn Smith-Keune
    • 1
  • Lynne van Herwerden
    • 1
  • Christopher J. Fulton
    • 2
  • Dean R. Jerry
    • 1
  1. 1.Molecular Evolution and Ecology Laboratory, School of Marine and Tropical BiologyJames Cook UniversityTownsvilleAustralia
  2. 2.Evolution, Ecology and Genetics, Research School of BiologyAustralian National UniversityCanberraAustralia
  3. 3.Environmental Conservation Division, Northwest Fisheries Science CenterNational Oceanic and Atmospheric AdministrationSeattleUSA

Personalised recommendations