Differential regulation of select osmoregulatory genes and Na+/K+-ATPase paralogs may contribute to population differences in salinity tolerance in a semi-anadromous fish

The time course of molecular acclimation to seawater in a euryhaline fish

“…At 24 h post-transfer, genes related to cell adhesion began to be upregulated, and cytoskeleton and extracellular matrix organization functions showed increased expression from hours of exposure. Cell adhesion and extracellular matrix pathway upregulation was similarly reported in Sacramento splittails between one and seven days into the acclimation to elevated salinity (Jeffries et al, 2019;Mundy et al, 2020), and branchial cell cytoskeleton reorganization is largely recognized as a fundamental aspect of salinity acclimation in teleosts (T. G. Evans & Somero, 2008;Fiol & Kultz, 2007;Nguyen et al, 2016). As a consequence of tissue remodelling events, an upregulation of mitochondrial respiratory chain and metabolism related genes is also expected to support the increased energy demand, as previously found in similar experiments of euryhaline fish translocation (Chen et al, 2018;Lam et al, 2014;Whitehead et al, 2012).…”

“…Although the NKA gene is usually identified in marine acclimated teleosts, where it is part of the ion secretion machinery, in Arabian pupfish different transcripts annotated to the -1 subunit gene were upregulated in desert pond individuals, and only one transcript was upregulated in Red Sea pupfish. While this could be an indication of populationspecific NKA subunit -1 isoforms (Mundy et al, 2020), it is likely that salinity-dependent isoforms with opposite functions of ion uptake in hyposaline water and salt secretion in seawater exist in this species, as previously described for several euryhaline teleosts (Bystriansky, Richards, Schulte, & Ballantyne, 2006;McCormick, Regish, & Christensen, 2009;Richards, Semple, Bystriansky, & Schulte, 2003;Tipsmark et al, 2011;Urbina, Schulte, Bystriansky, & Glover, 2013;Velotta et al, 2017). In the climbing perch (Anabas testudines) and in salmonids, NKA -1 isoform a expression levels are highest in freshwater and decreases post-transfer to seawater, while other isoform mRNA expressions increase following exposure (Bystriansky et al, 2006;Ip et al, 2012).…”

Inter-population differences in salinity tolerance of adult wild Sacramento splittail: osmoregulatory and metabolic responses to salinity

“…Divergent responses between adult splittail populations exposed to salinity manipulations add support to previously reported evidence of local adaptation based on population genetics ( Baerwald et al . 2008 ; Mahardja et al ., 2015 ) and divergent physiological and transcriptomic responses of juvenile splittail populations to salinity manipulations ( Verhille et al ., 2016 ; Jeffries et al ., 2019 ; Mundy et al ., 2020 ). Our studies on juvenile Sacramento splittail showed greater physiological disruption ( Verhille et al ., 2016 ) and reduced transcriptome plasticity ( Jeffries et al ., 2019 ; Mundy et al ., 2020 ) in CV compared to SP splittail in response to experimental elevation of water salinity.…”

“…2008 ; Mahardja et al ., 2015 ) and divergent physiological and transcriptomic responses of juvenile splittail populations to salinity manipulations ( Verhille et al ., 2016 ; Jeffries et al ., 2019 ; Mundy et al ., 2020 ). Our studies on juvenile Sacramento splittail showed greater physiological disruption ( Verhille et al ., 2016 ) and reduced transcriptome plasticity ( Jeffries et al ., 2019 ; Mundy et al ., 2020 ) in CV compared to SP splittail in response to experimental elevation of water salinity. Combined with similar divergent physiological responses reported here for adult splittail, this series of studies suggest that SP splittail are more salinity tolerant relative to CV splittail, throughout their entire life history.…”

“…Otolith strontium signatures of wild-captured fish have shown age-0 SP splittail to experience greater water salinities than the equivalent CV life stages ( Feyrer et al ., 2005 , 2007 , 2010 ). In our previous studies, modest interpopulation variation in juvenile splittail physiological responses ( Verhille et al ., 2016 ) to salinity was reflected in divergent transcriptomic responses indicative of improved plasticity, especially for gill remodelling, in the SP population ( Jeffries et al ., 2019 ; Mundy et al ., 2020 ). This variation corresponded with previously reported strontium signature findings, suggesting local adaptation of juvenile SP splittail to its higher-salinity spawning habitat.…”