Physiological and molecular mechanisms of osmoregulatory plasticity in killifish after seawater transfer

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.

Section: Results and Discussion Physiological Acclimationsupporting

confidence: 89%

Section: Results and Discussion Physiological Acclimationmentioning

confidence: 46%

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

Brennan

Gálvez

Whitehead

2015

“…Surprisingly, baseline expression of the 'seawater' isoform NKA-1b of Na + ,K + -ATPase (Richards et al, 2003;Bystriansky et al, 2006) did not differ between the two salinities ( Fig.9G), but there are two other reports where this was also the case (Shrimpton et al, 2005;Kiilerich et al, 2007). The higher expression of NKCC1a in SW trout (Fig.9H) is consistent with the SW-adaptive role of this basolateral transporter in net NaCl extrusion (McCormick, 2001;Tipsmark et al, 2002;Scott et al, 2005;Scott et al, 2008;Kiilerich et al, 2007). Control NHE2 expression was also greater in SW trout (Fig.9D); there have been many studies of this apical transporter in various teleosts (reviewed by Ivanis et al, 2008), but the only previous salinity study suggested that expression of NHE2 transiently increased after transfer from brackish water to FW in the killifish (Scott et al, 2005).…”

Section: Differences In Baseline Gene Expression Between Fw and Sw Troutmentioning

confidence: 53%

A nose-to-nose comparison of the physiological and molecular responses of rainbow trout to high environmental ammonia in seawater versus freshwater

Wood

Nawata

2011

Self Cite

SUMMARY Steelhead rainbow trout acclimated to either freshwater (FW) or seawater (SW) were exposed to high environmental ammonia (HEA, 1000 μmol l–1 NH4HCO3, pH 7.8–8.0) for 24 h. SW trout restored ammonia excretion more rapidly (3–6 h versus 9–12 h in FW), despite higher production rates and lower plasma pH. Plasma total ammonia levels stabilized at comparable levels below the external HEA concentration, and blood acid–base disturbances were small at both salinities. The electrochemical gradients for NH4+ entry (FNH4+) were the same in the two salinities, but only because FW trout allowed their transepithelial potential to rise by ∼15 mV during HEA exposure. Elevation of plasma [cortisol] during HEA exposure was more prolonged in SW fish. Plasma [glucose] increased in SW, but decreased in FW trout. Plasma [urea-N] also decreased in FW, in concert with elevated urea transporter (UT) mRNA expression in the gills. Of 13 branchial transporters, baseline mRNA expression levels were higher for Rhcg1, NHE2, NKCC1a and UT, and lower for NBC1 and NKA-α1a in SW trout, whereas NKA-α1b, NHE3, CA2, H+-ATPase, Rhag, Rhbg and Rhcg2 did not differ. Of the Rh glycoprotein mRNAs responding to HEA, Rhcg2 was greatly upregulated in both FW and SW, Rhag decreased only in SW and Rhcg1 decreased only in FW. H+-ATPase mRNA increased in FW whereas NHE2 mRNA increased in SW; NHE3 did not respond, and V-type H+-ATPase activity declined in SW during HEA exposure. Branchial Na+,K+-ATPase activity was much higher in SW gills, but could not be activated by NH4+. Overall, the more effective response of SW trout was explained by differences in physical chemistry between SW and FW, which greatly reduced the plasma NH3 tension gradient for NH3 entry, as well as by the higher [Na+] in SW, which favoured Na+-coupled excretion mechanisms. At a molecular level, responses in SW trout showed subtle differences from those in FW trout, but were very different than in the SW pufferfish. Upregulation of Rhcg2 appears to play a key role in the response to HEA in both FW and SW trout, and NH4+ does not appear to move through Na+,K+-ATPase.

“…While knowledge of the basic physiology of fishes with respect to ion and water regulation has progressed greatly from the first historic investigations (Smith, 1930;Keys, 1931;Krogh, 1937), most studies have been based on constraining fish to controlled environments and in many cases subjecting them to single step changes in salinity (e.g. Katoh et al, 2008;Scott et al, 2008;Madsen et al, 2009). However, in nature, these animals are capable of movement throughout their habitats, and they may rapidly encounter a variety of salinities.…”

Section: Introductionmentioning

confidence: 99%

Diet influences salinity preference of an estuarine fish, the killifishFundulus heteroclitus

Bucking

Wood

Grosell

2012

Self Cite

SUMMARYUnderstanding the interplay among the external environment, physiology and adaptive behaviour is crucial for understanding how animals survive in their natural environments. The external environment can have wide ranging effects on the physiology of animals, while behaviour determines which environments are encountered. Here, we identified changes in the behavioural selection of external salinity in Fundulus heteroclitus, an estuarine teleost, as a consequence of digesting a meal. Fish that consumed high levels of dietary calcium exhibited a higher preferred salinity compared with unfed fish, an effect that was exaggerated by elevated dietary sodium chloride. The mean swimming speed (calculated as a proxy of activity level) was not affected by consuming a diet of any type. Constraining fish to water of 22p.p.t. salinity during the digestion of a meal did not alter the amount of calcium that was absorbed across the intestine. However, when denied the capacity to increase their surrounding salinity, the compromised ability to excrete calcium to the water resulted in significantly elevated plasma calcium levels, a potentially hazardous physiological consequence. This study is the first to show that fish behaviourally exploit their surroundings to enhance their ionoregulation during digestion, and to pinpoint the novel role of dietary calcium and sodium in shaping this behaviour. We conclude that in order to resolve physiological disturbances in ion balance created by digestion, fish actively sense and select the environment they inhabit. Ultimately, this may result in transient diet-dependent alteration of the ecological niches occupied by fishes, with broad implications for both physiology and ecology.