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

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 temperatures (TE: 27°C) or near the extremes for normal development (TE: 22°C or 32°C), and were then raised to adulthood under common conditions at 27°C. Short-term temperature challenge affected aerobic exercise performance (Ucrit), but each TE group had reduced thermal sensitivity at their respective TE. This contrasted the unexpected differences after long-term acclimation to 16°C, when performance in the cold was ~20% higher in both 32°C and 22°C TE groups compared to 27°C TE controls. Differences in performance after acclimation to cold or warm (34°C) temperatures were partially explained by variation in fiber type composition in the swimming muscle. Cold acclimation changed the abundance of 3452 out of 19712 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°C and 32°C TE groups. This was associated with differences in expression for genes involved in energy metabolism, angiogenesis, cell stress, muscle contraction and remodelling, 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.