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

Abstract

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°C) or near the extremes for normal development (T E = 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 (U crit ), but each T E group had reduced thermal sensitivity at its respective T E . In contrast, unexpected differences arose after long-term acclimation to 16°C, when performance in the cold was ∼20% higher in both 32°C and 22°C T E groups compared with 27°C T E 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 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°C and 32°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.environmental physiology | fish | muscle transcriptome | functional genomics | high-throughput sequencing T emperature has profound effects on the physical and chemical processes that dictate how biological systems function. Ectothermic organisms-those that cannot regulate body temperature using endogenous heat production-are particularly susceptible to changes in environmental temperature. Species and populations can typically survive and perform across a finite range of temperatures, the breadth of which is a critical determinant of their distribution and abundance (1, 2). The physiological and molecular mechanisms underlying how ectotherms perform when faced with daily and seasonal temperature variation have attracted significant attention for decades, and this 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 performance breadth (5), which may increase fitness and improve the viability of populations during warming (6-8). However, much of what we know about the integrative mechanisms for this ability comes from studies of juvenile and adult animals. There has been relatively little emphasis on how interactions between temperature and ...

Temperature during embryonic development has persistent effects on metabolic enzymes in the muscle of zebrafish

“…1, Table 3). These results were probably not caused by differences in fibre type composition of the muscle, because there are no differences between T E groups in the total transverse area of either slow oxidative (red) or fast oxidative (pink, intermediate) fibres in the axial musculature at 27°C (Scott and Johnston, 2012). However, embryonic temperature does affect the ) to body mass that are shown in Fig.…”

“…Furthermore, there were clear differences in thermal optima between the 22°C T E group (T opt of 27°C) and the 32°C T E group (T opt of 32°C). These findings provide some insight into the underlying mechanism of our previous observation that T E influences the shortterm thermal sensitivity of swimming performance (Scott and Johnston, 2012). For example, zebrafish raised at 22°C as embryos maintain higher swim speeds after transfer to 22°C than fish raised at 32°C, possibly in part because their COX enzyme was better suited to function at cooler temperatures.…”

“…Our recent work suggests that the thermal environment experienced in early life can have a profound influence on exercise performance (Scott and Johnston, 2012). We found that embryonic temperature (T E ) affected prolonged swimming performance (critical swimming speed, U crit ) in adult zebrafish in response to a short-term thermal challenge, such that fish raised at a particular T E had reduced thermal sensitivity at its respective T E .…”

“…Natural populations typically reproduce during the monsoon season, when food is readily available and temperatures range from ~23 to 31°C (Spence et al, 2008). We tested two hypotheses that could explain our previous observations on the effects of embryonic temperature on swimming performance (Scott and Johnston, 2012) based on differences in muscle enzyme function: (1) that embryonic temperature would shift the thermal optima of metabolic enzyme activity towards the T E , and (2) that development at a low embryonic temperature would blunt the warm acclimation response of metabolic enzymes. We focused our efforts on enzymes that reflect the flux capacity of oxidative phosphorylation [cytochrome c oxidase (COX)], the citric acid cycle [citrate synthase (CS)], glycolysis [pyruvate kinase (PK) and lactate dehydrogenase (LDH)] and fatty acid oxidation [hydroxyacyl-coA dehydrogenase (HOAD)].…”

Epigenetics in natural animal populations

“…As a consequence, depending on the rate and magnitude of environmental change, as well as factors such as habitat fragmentation and natural barriers, many species are experiencing conditions outside their physiological tolerances and are therefore vulnerable to decline and extinction (Hoffmann & Sgr o, 2011). One important mechanism that may reduce the detrimental effects of environmental change on organisms is phenotypic plasticity, for example, temperature acclimation (Angilletta, 2009) via the adjustment of breeding time in birds (Charmantier et al, 2008) or fibre-type composition in the swimming muscles of fish (Scott & Johnston, 2016). Although studies on the evolution of phenotypic plasticity have typically used classic quantitative genetics to partition phenotypic variance (V P ) into genetic (V G ), environmental (V E ) and genotype-by-environment variance (V G9E ), and focused on how selection acts on genetically based phenotypic plasticity (Pigliucci, 2005;, it has been suggested that there may be insufficient genetic variation to permit this kind of phenotypic response to climate change in many natural populations (e.g.…”