Gene expression plasticity in response to salinity acclimation in threespine stickleback ecotypes from different salinity habitats

Abstract

Phenotypic plasticity is thought to facilitate the colonization of novel environments and shape the direction of evolution in colonizing populations. However, the relative prevalence of various predicted patterns of changes in phenotypic plasticity following colonization remains unclear. Here, we use a whole-transcriptome approach to characterize patterns of gene expression plasticity in the gills of a freshwater-adapted and a saltwater-adapted ecotype of threespine stickleback (Gasterosteus aculeatus) exposed to a range of salinities. The response of the gill transcriptome to environmental salinity had a large shared component common to both ecotypes (2159 genes) with significant enrichment of genes involved in transmembrane ion transport and the restructuring of the gill epithelium. This transcriptional response to freshwater acclimation is induced at salinities below two parts per thousand. There was also differentiation in gene expression patterns between ecotypes (2515 genes), particularly in processes important for changes in the gill structure and permeability. Only 508 genes that differed between ecotypes also responded to salinity and no specific processes were enriched among this gene set, and an even smaller number (87 genes) showed evidence of changes in the extent of the response to salinity acclimation between ecotypes. No pattern of relative expression dominated among these genes, suggesting that neither gains nor losses of plasticity dominated the changes in expression patterns between the ecotypes. These data demonstrate that multiple patterns of changes in gene expression plasticity can occur following colonization of novel habitats.

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

“…Consequently, prominent gaps remain in our understanding of the evolutionary process in nature; by 2017, scientists had only managed to confirm ~20 convincing cases of natural selection in the wild (Stapley et al, 2010;McCormack et al, 2013;Blank et al, 2014;Gibbons et al, 2017). We are now able to identify genes and mutations associated with evolutionarily significant traits, and it is also possible to target extinct populations/ species in the same way.…”

“…Colonization of freshwater from a marine ancestral state represents a major evolutionary transition, in which phenotypic plasticity plasticity (ability of a single genotype to produce variable phenotypes in different environments) which is widespread in nature, is likely to have played a vital role, following which plasticity itself may be subject to adaptive processes (Orr, 2005;Gibbons et al, 2017;Schneider and Meyer, 2017). A variety of changes potentially occur in plastic responses following freshwater colonization.…”

“…For example, the Baldwin effect-occurs initially when plastic traits contribute to better survival rates that allow organisms to persist in novel environments long enough for selection to act on other traits (DeBiasse and Kelly, 2016;Hendry, 2016;Gibbon et al, 2017). This can result in an increase in general trait plasticity or a shift in other traits in the same direction as plastic ones that result in accumulation of phenotypic differences between populations or species that contribute to rapid convergence toward a new optimal phenotype (Brennan et al, 2015;Gibbons et al, 2017). Plastic responses however, can also be deleterious if they shift phenotypes from the optimum range so that organisms are unable to buffer against perturbations imposed by the newly colonized environment (Scheiner, 1993;Huang and Agarwal, 2016).…”

“…Phenotypic trait plasticity is considered to have facilitated colonization of many novel environments and can also shape the direction of evolution experienced by colonizing populations (Hendry, 2016;Gibbons et al, 2017). In parallel, changes may occur in many other organismal attributes including food habits, energy budgets, stress tolerance, and metabolic and behavioral processes directed at coping with newly invaded environments (Velotta et al, 2015).…”

“…Comparative studies of gene expression patterns can reveal molecular signatures of adaptation to a wide diversity of environmental conditions (Romero et al, 2012). A number of recent studies have been conducted on aquatic species to identify and characterize genes with roles in freshwater adaptation and salinity tolerance (DeFaveri et al, 2011;Havird et al, 2014;Brennan et al, 2015;Gibbons et al, 2017;Moshtaghi et al, 2017;Velotta et al, 2017), primarily concerned with osmoregulatory capacity. Comparing gene expression patterns among closely related species (preferably with a common ancestry) under common experimental conditions can allow a comprehensive understanding to be developed about the functional roles that specific genes may have on adaptive response.…”