
Temperature during embryonic development has persistent effects on thermal acclimation capacity in zebrafish Graham R. Scotta,b,1 and Ian A. Johnstonb aDepartment of Biology, McMaster University, Hamilton, ON L8S 4K1, Canada; and bScottish Oceans Institute, School of Biology, University of St Andrews, St Andrews, Fife KY16 8LB, United Kingdom Edited by George N. Somero, Stanford University, Pacific Grove, CA, and approved July 19, 2012 (received for review March 27, 2012) Global warming is intensifying interest in the mechanisms enabling swimming performance in subsequent life stages. In the wild, ectothermic animals to adjust physiological performance and cope zebrafish experience daily temperature fluctuations of ∼5 °C and with temperature change. Here we show that embryonic tempera- wide seasonal variation in temperature, from as low as 6 °C in ture can have dramatic and persistent effects on thermal acclima- winter to ∼38 °C in summer, across their native range (Ganges tion capacity at multiple levels of biological organization. Zebrafish and Brahmaputra river basins in southern Asia) (11). Natural populations typically reproduce during the monsoon season, when embryos were incubated until hatching at control temperature ∼ (T = 27 °C) or near the extremes for normal development (T = food is readily available and temperatures range from 23 °C to E E 31 °C (12). We used fish derived from a wild-caught strain and 22 °C or 32 °C) and were then raised to adulthood under common a large number of families to approximate the natural genetic conditions at 27 °C. Short-term temperature challenge affected aer- variation found in wild populations. We reared zebrafish em- obic exercise performance (Ucrit), but each TE group had reduced T bryos at three temperatures (22 °C, 27 °C, and 32 °C) spanning thermal sensitivity at its respective E. In contrast, unexpected dif- the range for normal reproduction and development (Fig. 1). ferences arose after long-term acclimation to 16 °C, when perfor- Embryonic temperature had striking and often unpredictable ∼ T mance in the cold was 20% higher in both 32 °C and 22 °C E effects on thermal acclimation that persisted to adulthood, even T groups compared with 27 °C E controls. Differences in performance after fish were raised from hatching at a common temperature PHYSIOLOGY after acclimation to cold or warm (34 °C) temperatures were par- (27 °C). These effects could be explained by differences in how tially explained by variation in fiber type composition in the swim- thermal acclimation affected the abundance and proportion of ming muscle. Cold acclimation changed the abundance of 3,452 of fiber types in the swimming muscle and in the expression of a 19,712 unique and unambiguously identified transcripts detected in subset of transcripts across the transcriptome. the fast muscle using RNA-Seq. Principal components analysis dif- ferentiated the general transcriptional responses to cold of the Results and Discussion 27 °C and 32 °C TE groups. Differences in expression were observed Embryonic Temperature Affects Thermal Sensitivity and Acclimation for individual genes involved in energy metabolism, angiogenesis, of Swimming Performance in Adult Zebrafish. We first assessed how cell stress, muscle contraction and remodeling, and apoptosis. swimming performance (“critical swimming speed”) in adult fish Therefore, thermal acclimation capacity is not fixed and can be from each embryonic temperature (TE) group was affected by modified by temperature during early development. Developmen- temperature after (i) short-term (1 d) transfer to 22 °C, 27 °C “ ” tal plasticity may thus help some ectothermic organisms cope with (control), or 32 °C ( thermal sensitivity ) and (ii) long-term ac- – the more variable temperatures that are expected under future climation (28 30 d) to 16 °C or 34 °C (Fig. 1). We used a strong climate-change scenarios. inference approach to distinguish between multiple competing hypotheses for how TE influences the temperature dependence of swimming performance (13). Two-factor ANOVA with orthog- environmental physiology | fish | muscle transcriptome | onal polynomial contrasts of T was used to determine the level functional genomics | high-throughput sequencing E of statistical support for various hypotheses: “beneficial de- velopmental plasticity” (significant interactions of TE and swim emperature has profound effects on the physical and chem- temperature, TS), “hotter is better” or “colder is better” (signif- Tical processes that dictate how biological systems function. icant linear effects of TE with a positive or a negative contrast Ectothermic organisms—those that cannot regulate body tem- coefficient, respectively), “optimal intermediate temperature” perature using endogenous heat production—are particularly (significant quadratic effect of TE with downward concavity), and susceptible to changes in environmental temperature. Species “developmental buffering” (no effect of TE), which would reflect and populations can typically survive and perform across a finite canalization of embryonic development. range of temperatures, the breadth of which is a critical de- TE affected the short-term thermal sensitivity of swimming terminant of their distribution and abundance (1, 2). The phys- performance (Fig. 2A and Table S1). Performance was generally iological and molecular mechanisms underlying how ectotherms improved at the temperature zebrafish were raised as embryos, perform when faced with daily and seasonal temperature varia- consistent with the hypothesis that developmental plasticity is tion have attracted significant attention for decades, and this beneficial. This result was supported by statistically significant interest has intensified in an attempt to understand the potential ecological impacts of global climate change (3, 4). It is clear that temperature acclimatization can shift thermal optima and per- Author contributions: G.R.S. and I.A.J. designed research; G.R.S. performed research; G.R.S. formance breadth (5), which may increase fitness and improve analyzed data; and G.R.S. and I.A.J. wrote the paper. the viability of populations during warming (6–8). However, The authors declare no conflict of interest. much of what we know about the integrative mechanisms for this This article is a PNAS Direct Submission. ability comes from studies of juvenile and adult animals. There Data deposition: The sequence data reported in this paper has been deposited in the has been relatively little emphasis on how interactions between Array Express Archive (European Bioinformatics Institute; EBI) database, www.ebi.ac.uk/ar- temperature and the developmental program might affect phe- rayexpress (accession no. E-MTAB-1155). notypic plasticity in later life (9, 10). 1To whom correspondence should be addressed. E-mail: [email protected]. fi fl Here we use zebra sh as a model to investigate the in uence This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. of temperature change during embryonic development on 1073/pnas.1205012109/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1205012109 PNAS | August 28, 2012 | vol. 109 | no. 35 | 14247–14252 Downloaded by guest on September 27, 2021 interactions for total muscle area and the total transverse area of fast fibers (P = 0.006 and P = 0.040) and by the cold-induced increases in total muscle, slow fiber, and fast fiber transverse areas in only the 22 °C and 32 °C TE groups. It is unclear whether these differences are related to variation in the num- ber of axial myotomes, because TE affects the rate of somite Fig. 1. Fish were raised at one of three embryonic temperature (TE) treat- ments and then at a common postembryonic temperature until adulthood, after which they underwent one of five adult temperature treatments. Swimming performance was measured in each TE group after each adult temperature treatment. Muscle phenotype was determined in fish accli- mated to 27 °C, 16 °C, and 34 °C (*). Transcriptome-wide analysis of gene expression was conducted for the 27 °C and 32 °C TE groups acclimated to † 27 °C and 16 °C ( ). Each individual was subject to one distinct path from left to right. TE groups are offset for clarity. TS × TE interactions in two-factor ANOVA with orthogonal polynomial contrasts (P = 0.049 overall and P = 0.036 for linear contrast) (Table S2). Compared with swim trials at 27 °C, only the 22 °C TE group sustained performance at 22 °C and only the 32 °C TE group increased performance at 32 °C. Differences between TE groups were not caused by differences in body mass or length (Table S3). TE also affected thermal acclimation capacity, but the effects were not always of predictable benefit (Fig. 2B and Table S1). Some results suggested that development at a specific TE might optimize performance at that temperature, such as the significant TS × TE interactions (P < 0.001 overall and for both contrasts) (Table S2) and the lower performance of the 22 °C TE group at 34 °C. However, there also appeared to be an overall benefitof developing at 32 °C on thermal acclimation across all temper- atures. The 32 °C TE group performed better than the 27 °C TE group in the cold and the main effect for the linear contrast of TE was significant (P < 0.001) (Table S2). The former difference was specifically due to TE-induced variation in thermal acclimation capacity, rather than to persistent effects on short-term thermal sensitivity, because critical swimming speed after 1 d at 16 °C was similar in 32 °C and 27 °C TE groups (9.89 ± 0.15 and 9.05 ± 0.32 standard body lengths/s, n = 4) (Table S1). We next sought to determine whether the differences in acclimation capacity be- tween TE groups were due to differences in muscle plasticity. We therefore examined swimming muscle phenotype using standard histological methods (Fig. 3 A–D) in the caudal region of the trunk (0.7 of standard body length) for the same fish as were swum at acclimation temperatures (TA) of 16 °C, 27 °C, and 34 °C (Fig.
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