Acid stress mediated adaptive divergence in ion channel function during embryogenesis in Rana arvalis

Abstract

Ion channels and pumps are responsible for ion flux in cells, and are key mechanisms mediating cellular function. Many environmental stressors, such as salinity and acidification, are known to severely disrupt ionic balance of organisms thereby challenging fitness of natural populations. Although ion channels can have several vital functions during early life-stages (e.g. embryogenesis), it is currently not known i) how developing embryos maintain proper intracellular conditions when exposed to environmental stress and ii) to what extent environmental stress can drive intra-specific divergence in ion channels. Here we studied the moor frog, Rana arvalis, from three divergent populations to investigate the role of different ion channels and pumps for embryonic survival under acid stress (pH 4 vs 7.5) and whether populations adapted to contrasting acidities differ in the relative role of different ion channel/pumps. We found that ion channels that mediate Ca2+ influx are essential for embryonic survival under acidic pH, and, intriguingly, that populations differ in calcium channel function. Our results suggest that adaptive divergence in embryonic acid stress tolerance of amphibians may in part be mediated by Ca2+ balance. We suggest that ion flux may mediate adaptive divergence of natural populations at early life-stages in the face of environmental stress.

Molecular phenotyping of maternally mediated parallel adaptive divergence withinRana arvalisandRana temporaria

“…First, in several taxa, jelly components have been shown to influence sperm-egg interactions, to harbour intraspecific variation in their effects on sperm motility (Simmons et al 2009) and, hence, to affect fertilization (reviewed in Wong & Wessel 2006;Shu et al 2015a). The effects of jelly on gamete recognition have recently been suggested to have facilitated incipient speciation in a sea star (Hart et al 2014).…”

“…; Shu et al . ,c; reviewed in Räsänen & Green ). In amphibians, a key mechanism for negative fitness effects is the so‐called curling defect, in which embryos exposed to acidic conditions may develop normally but become curled within the egg coats and, finally, fail to hatch (Gosner & Black ; Dunson & Connell ; Pierce ).…”

“…Jelly coats can have major impacts on reproductive fitness by influencing fertilization, by providing a floating or adhesive medium for the embryo and by providing protection against various biotic and abiotic environmental hazards (reviewed in Shu et al 2015a). Jelly coats are typically highly variable in structure and composition among species (reviewed in Wong & Wessel 2006;Menkhorst & Selwood 2008;Shu et al 2015a) and there is some evidence for intraspecific variation in relation to sperm-egg interactions (Levitan & Irvine 2001;Podolsky 2001;Simmons et al 2009). However, intraspecific variability in jelly coats in relation to diversifying natural selection has largely been overlooked (Shu et al 2015a).…”

Peer Review #1 of "De novo oviduct transcriptome of the moor frog Rana arvalis: a quest for maternal effect candidate genes (v0.1)"

“…In the moor frog Rana arvalis, jelly coat mediated maternal effects have driven adaptive divergence in embryonic acid stress tolerance (Hangartner et al 2011;Persson et al 2007;Räsänen et al 2003b;Shu et al 2015a;Shu et al 2016;Shu et al 2015c). This divergence is primarily due to glycoproteins of the jelly coats, which influence water balance and, subsequently, embryonic survival in acidic conditions (Shu et al 2015a).…”

“…In the moor frog Rana arvalis, jelly coat mediated maternal effects have driven adaptive divergence in embryonic acid stress tolerance (Hangartner et al 2011;Persson et al 2007;Räsänen et al 2003b;Shu et al 2015a;Shu et al 2016;Shu et al 2015c). This divergence is primarily due to glycoproteins of the jelly coats, which influence water balance and, subsequently, embryonic survival in acidic conditions (Shu et al 2015a). Egg jelly glycoproteins are complex glycan structures attached to a protein backbone (Hedrick & Nishihara 1991) and are highly species specific (Coppin et al 1999;Delplace et al 2002;Strecker et al 2003).…”