4.8 Article

Temperature during embryonic development has persistent effects on thermal acclimation capacity in zebrafish

Publisher

NATL ACAD SCIENCES
DOI: 10.1073/pnas.1205012109

Keywords

environmental physiology; fish; muscle transcriptome; functional genomics; high-throughput sequencing

Funding

  1. European Union
  2. Marine Alliance for Science and Technology for Scotland (a pooling initiative from the Scottish Funding Council)
  3. Natural Sciences and Engineering Research Council
  4. BBSRC [BBS/E/D/20310000] Funding Source: UKRI
  5. MRC [G0900740] Funding Source: UKRI
  6. Medical Research Council [G0900740] Funding Source: researchfish

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Global warming is intensifying interest in the mechanisms enabling ectothermic animals to adjust physiological performance and cope with temperature change. Here we show that embryonic temperature can have dramatic and persistent effects on thermal acclimation capacity at multiple levels of biological organization. Zebrafish embryos were incubated until hatching at control temperature (T-E = 27 degrees C) or near the extremes for normal development (T-E = 22 degrees C or 32 degrees C) and were then raised to adulthood under common conditions at 27 degrees C. Short-term temperature challenge affected aerobic exercise performance (U-crit), but each T-E group had reduced thermal sensitivity at its respective TE. In contrast, unexpected differences arose after long-term acclimation to 16 degrees C, when performance in the cold was similar to 20% higher in both 32 degrees C and 22 degrees C TE groups compared with 27 degrees C T-E controls. Differences in performance after acclimation to cold or warm (34 degrees C) temperatures were partially explained by variation in fiber type composition in the swimming muscle. Cold acclimation changed the abundance of 3,452 of 19,712 unique and unambiguously identified transcripts detected in the fast muscle using RNA-Seq. Principal components analysis differentiated the general transcriptional responses to cold of the 27 degrees C and 32 degrees C T-E groups. Differences in expression were observed for individual genes involved in energy metabolism, angiogenesis, cell stress, muscle contraction and remodeling, and apoptosis. Therefore, thermal acclimation capacity is not fixed and can be modified by temperature during early development. Developmental plasticity may thus help some ectothermic organisms cope with the more variable temperatures that are expected under future climate-change scenarios.

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