Abstract
Resilience to climate change depends on a species' adaptive potential and phenotypic plasticity. The latter can enhance survival of individual organisms during short periods of extreme environmental perturbations, allowing genetic adaptation to take place over generations. Along the U.S. East Coast, estuarine‐dependent spotted seatrout (Cynoscion nebulosus) populations span a steep temperature gradient that provides an ideal opportunity to explore the molecular basis of phenotypic plasticity. Genetically distinct spotted seatrout sampled from a northern and a southern population were exposed to acute cold and heat stress (5 biological replicates in each treatment and control group), and their transcriptomic responses were compared using RNA‐sequencing (RNA‐seq). The southern population showed a larger transcriptomic response to acute cold stress, whereas the northern population showed a larger transcriptomic response to acute heat stress compared with their respective population controls. Shared transcripts showing significant differences in expression levels were predominantly enriched in pathways that included metabolism, transcriptional regulation, and immune response. In response to heat stress, only the northern population significantly upregulated genes in the apoptosis pathway, which could suggest greater vulnerability to future heat waves in this population as compared to the southern population. Genes showing population‐specific patterns of expression, including hpt, acot, hspa5, and hsc71, are candidates for future studies aiming to monitor intraspecific differences in temperature stress responses in spotted seatrout. Our findings contribute to the current understanding of phenotypic plasticity and provide a basis for predicting the response of a eurythermal fish species to future extreme temperatures.
Highlights
Temperature has direct and pervasive effects on fish physiology (Angilletta et al, 2010; Fry, 1947)
Transcriptomic studies of fish populations originating from contrasting temperature regimes have shown distinct responses to chronic thermal stress, but little is known about the effects of acute thermal stress
We conducted RNA-seq on two genetically distinct and physiologically divergent populations of spotted seatrout exposed to acute temperature stress and de novo-assembled the first liver transcriptome for this species
Summary
Temperature has direct and pervasive effects on fish physiology (Angilletta et al, 2010; Fry, 1947). Cynoscion nebulosus, is a teleostean fish distributed from coastal waters in New York to the Gulf of Mexico (Bortone, 2002) This species is uncommon north of Chesapeake Bay, most likely due to its low survival in water temperatures below 5°C (Ellis et al, 2017). Studies of spotted seatrout on the East Coast of the United States have revealed a range of physiological and life history differences such as growth rate (Smith et al, 2008), size at maturity (Brown-Peterson, 2003; Ihde, 2000), and metabolic rate (Song et al, 2019), but whether these populations respond differently to thermal stress is unknown. The purpose of this study was to compare the underlying transcriptomic response to acute temperature stress in these two genetically distinct and physiologically divergent spotted seatrout populations to better understand the observed metabolic differences. The objectives were threefold: (a) to construct a high-quality transcriptome for spotted seatrout, (b) to discover and quantify shared transcriptomic responses to cold and heat stress in both populations, and (c) to discover and quantify unique transcriptomic responses to cold and heat stress in each population
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