Molecular Response to Extreme Summer Temperatures Differs Between Two Genetically Differentiated Populations of a Coral Reef Fish

Abstract

Extreme thermal events are increasing in frequency and duration as the climate continues to warm, with potential detrimental effects on marine organisms. However, the effects of heatwaves may differ among geographically separated populations depending on their capacity for thermal plasticity. Here, we compared the response to simulated summer heatwave temperatures (+1.5 and +3.0 • C above average) in two populations of a coral reef damselfish with different capacities for thermal plasticity. We found that the more thermally tolerant population had greater plasticity of gene expression and had significantly more downregulated genes, which may provide more energy to repair damage associated with thermal stress and to maintain basic functions at these extreme temperatures. In contrast, the thermally sensitive population exhibited higher basal levels of heat shock proteins and had three times fewer changes in gene expression overall. The limited changes in gene regulation suggest that individuals have reduced genome plasticity to tolerate thermal fluctuations and consequently may not have enough energy to repair damage and resume cellular homeostasis at extreme temperatures. Thus, we have identified the molecular signatures of how two genetically distinct fish populations cope with an extreme thermal event, and why they differ in their capacity for thermal plasticity.

Comparative transcriptomics of spotted seatrout (Cynoscion nebulosus) populations to cold and heat stress

“…In comparative studies of populations or closely related species, a larger transcriptomic response can either indicate a general stress response or physiological adaptation (Narum & Campbell, 2015; Veilleux et al, 2018). Thus, transcriptomic studies should be viewed within an ecological and physiological context (DeBiasse & Kelly, 2016).…”

“…Next‐generation sequencing and RNA‐sequencing (RNA‐seq) have become more accessible and allowed the transcriptome (whole set of the messenger RNA molecules in a cell or tissue) of any organisms to be studied (Alvarez et al., 2015; Todd et al., 2016). Previous studies looking at gene expression differences have generally focused on sublethal temperature stress lasting from weeks to months (Narum & Campbell, 2015; Newton et al., 2013; Veilleux et al, 2018). How gene expression responds to acute temperature stress on the scale of hours to days is less well understood (Buckley, 2006; Healy et al, 2010).…”

“…Fish populations that experience contrasting temperature regimes show distinct transcriptomic responses, likely as a result of local adaptation (Newton et al., 2013; Veilleux et al, 2018). Spotted seatrout living at its northern range limit in Chesapeake Bay encounter near‐freezing water temperature yearly (McGrath & Hilton, 2017), while its southern counterparts rarely experience temperatures below 5°C.…”

Diurnal and seasonal hsp70 gene expression in a cryptic reef fish, the bluebanded goby Lythrypnus dalli (Gilbert 1890)

“…The effect of thermal variability may differ between species, and even populations, according to phenotypic tolerance and plasticity derived from acclimatization to the thermal conditions prevailing in their environment (Veilleux et al, 2018). Some organisms that inhabit environments with high thermal variability have a greater capacity to modulate the expression levels of some hsps, including hsp70 (Logan and Somero, 2011;Jesus et al, 2013).…”

“…Some organisms that inhabit environments with high thermal variability have a greater capacity to modulate the expression levels of some hsps, including hsp70 (Logan and Somero, 2011;Jesus et al, 2013). In contrast, organisms that inhabit narrower thermal ranges (tropical or polar regions) tend to lack a thermal shock response when exposed to acute thermal changes (Hofmann, 2005;Veilleux et al, 2018). Measurement of physical parameters suggest a marked seasonal variation in Punta Diablo, particularly in temperature.…”