Reciprocal osmotic challenges reveal mechanisms of divergence in phenotypic plasticity in the killifish Fundulus heteroclitus

Abstract

The killifish Fundulus heteroclitus is an estuarine species with broad physiological plasticity, enabling acclimation to diverse stressors. Previous work suggests that freshwater populations expanded their physiology to accommodate low salinity environments; however, it is unknown whether this compromises their tolerance to high salinity. We used a comparative approach to investigate the mechanisms of a derived freshwater phenotype and the fate of an ancestral euryhaline phenotype after invasion of a freshwater environment. We compared physiological and transcriptomic responses to high-and low-salinity stress in fresh and brackish water populations and found an enhanced plasticity to low salinity in the freshwater population coupled with a reduced ability to acclimate to high salinity. Transcriptomic data identified genes with a conserved common response, a conserved salinity-dependent response and responses associated with population divergence. Conserved common acclimation responses revealed stress responses and alterations in cell-cycle regulation as important mechanisms in the general osmotic response. Salinityspecific responses included the regulation of genes involved in ion transport, intracellular calcium, energetic processes and cellular remodeling. Genes diverged between populations were primarily those showing salinity-specific expression and included those regulating polyamine homeostasis and the cell cycle. Additionally, when populations were matched with their native salinity, expression patterns were consistent with the concept of 'transcriptomic resilience', suggesting local adaptation. These findings provide insight into the fate of a plastic phenotype after a shift in environmental salinity and help to reveal mechanisms allowing for euryhalinity.

The utility of transcriptomics in fish conservation

“…5A) were impacted in the longfin smelt at 20°C. Associated with muscle activity is the regulation of cellular calcium and potassium levels; however, these processes can also be affected by osmoregulatory stress (Brennan et al, 2015). Longfin smelt showed differential expression of several genes involved in ion channels and ion homeostasis due to the temperature treatment (e.g.…”

Understanding the molecular basis of adaptation to freshwater environments by prawns in the genus Macrobrachium

“…To date, osmoregulatory capacity is considered to be the principal mechanism for crustacean adaptation to freshwater (Faria et al, 2011;Brennan et al, 2015;Velotta et al, 2017). However, osmoregulation cannot be the sole mechanism for freshwater adaptation.…”

“…Tighter cell junctions are required for osmoregulation in freshwater compared with raised salinity conditions (Tipsmark et al, 2002;Brennan et al, 2015;Velotta et al, 2017). The intensity of selection pressure acts differently under different environmental conditions that in turn, can result in sequence divergence in the coding regions in a number of candidate genes controlling a specific phenotype while maintaining the sequences conserved in other genes (Ellegren, 2014;Berdan et al, 2015;Bailey and Bataillon, 2016 In a diverse array of crustacean species, regulation of internal body fluid content via haemolymph production is considered to be one of the principal mechanisms for maintaining an iso-osmotic body fluid concentration relative to the surrounding aquatic medium (McNamara et al, 2015;Mitterboeck et al, 2016).…”

“…To date however, little work has been directed at identifying and characterizing genes and pathways that facilitated crustacean adaptation to freshwater environments. A number of studies of fish have concluded that changes to expression of osmoregulatory genes have played the principal roles in driving this process (DeFaveri et al, 2011;DeFaveri and Merila, 2014;Brennan et al, 2015;Velotta et al, 2015;Velotta et al, 2017). Crustaceans unlike most vertebrates often possess complex life cycles that involve many developmental stages in different habitats.…”

“…Adaptive responses to environmental stressors can depend on the type of organism, its current physiological state as well as the natural environment in which it evolved (Nadal et al, 2011;Wray, 2013). Multicellular organisms have evolved an array of sophisticated mechanisms to deal efficiently with different environmental stressors including: sensing stress and signal transduction; activating signaling pathways; and modifying expression of underlying genes that allow individuals to control most aspects of physiology (Nadal et al, 2011;Stern, 2013;Brennan et al, 2015). So, multicellular organisms are often able to minimize any potential negative physiological changes by maintaining their internal homeostasis and by buffering extracellular changes efficiently via regulation of gene expression (Velotta et al, 2015).…”