Mitochondrial volume density and evidence for its role in adaptive divergence in response to thermal tolerance in threespine stickleback.

Phenotypic plasticity is predicted to permit persistence in new environments, and may subsequently evolve to enhance fitness. Colonizing environments with lower winter temperatures can lead to the evolution of lower critical thermal minima; the corresponding physiological traits associated with temperature tolerance are predicted to involve mitochondrial function. Threespine stickleback (Gasterosteus aculeatus) have colonized freshwater lakes along the Pacific Northwest. These freshwater populations are known to exhibit cold-induced increases in mitochondrial volume density in pectoral muscle, but whether such plasticity evolved before or after colonization is uncertain. Here, we measure critical thermal minima (CTmin) in one marine and one freshwater population of threespine stickleback, and mitochondrial volume density in pectoral and cardiac tissue of both populations acclimated to different temperature treatments (6.2, 14.5 and 20.6 â„ƒ). Mitochondrial volume density increased with cold acclimation in pectoral muscle; cardiac muscle was non-plastic but had elevated mitochondrial volume densities compared to pectoral muscle across all temperature treatments. There were no differences in the levels of plasticity between marine and freshwater stickleback, but neither were there differences in CTmin. Importantly, marine stickleback exhibited plasticity under low-salinity conditions, suggesting that marine stickleback had at least one necessary phenotype for persistence in freshwater environments before colonization occurred.

The power and limitations of gene expression pathway analyses toward predicting population response to environmental stressors.

Rapid environmental changes impact the global distribution and abundance of species, highlighting the urgency to understand and predict how populations will respond. The analysis of differentially expressed genes has elucidated areas of the genome involved in adaptive divergence to past and present environmental change. Such studies however have been hampered by large numbers of differentially expressed genes and limited knowledge of how these genes work in conjunction with each other. Recent methods (broadly termed "pathway analyses") have emerged that aim to group genes that behave in a coordinated fashion to a factor of interest. These methods aid in functional annotation and uncovering biological pathways, thereby collapsing complex datasets into more manageable units, providing more nuanced understandings of both the organism-level effects of modified gene expression, and the targets of adaptive divergence. Here, we reanalyze a dataset that investigated temperature-induced changes in gene expression in marine-adapted and freshwater-adapted threespine stickleback (Gasterosteus aculeatus), using Weighted Gene Co-expression Network Analysis (WGCNA) with PANTHER Gene Ontology (GO)-Slim overrepresentation and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis. Six modules exhibited a conserved response and six a divergent response between marine and freshwater stickleback when acclimated to 7°C or 22°C. One divergent module showed freshwater-specific response to temperature, and the remaining divergent modules showed differences in height of reaction norms. PPARAa, a transcription factor that regulates fatty acid metabolism and has been implicated in adaptive divergence, was located in a module that had higher expression at 7°C and in freshwater stickleback. This updated methodology revealed patterns that were not found in the original publication. Although such methods hold promise toward predicting population response to environmental stressors, many limitations remain, particularly with regard to module expression representation, database resources, and cross-database integration.

Heterozygosity and asymmetry: Ectodysplasin as a form of genetic stress in marine threespine stickleback.

Genome-wide heterozygosity has long been hypothesized to play a role in buffering organisms against developmental perturbations, potentially resulting in increased symmetry. If true, this could in part explain the maintenance of standing genetic variation in wild populations. Marine threespine sticklebacks (Gasterosteus aculeatus) were sampled across their eastern Pacific coastal distribution from Alaska to California and variations in asymmetry for both structural and nonstructural armor traits (lateral plates) were assessed. Structural plates consistently showed less asymmetry than nonstructural plates, but standardized measures of heterozygosity were not correlated with the extent of asymmetry expressed by a fish. Fish that were heterozygous for the major-effect gene controlling lateral plate variation (Ectodysplasin) had higher occurrences of asymmetry, even when the individuals were phenotypically fully plated. Collectively, this suggests that heterozygosity at a major-effect locus can have a greater impact on asymmetry than heterozygosity sampled across the genome.

Contemporary ancestor? Adaptive divergence from standing genetic variation in Pacific marine threespine stickleback.

BACKGROUND: Populations that have repeatedly colonized novel environments are useful for studying the role of ecology in adaptive divergence - particularly if some individuals persist in the ancestral habitat. Such "contemporary ancestors" can be used to demonstrate the effects of selection by comparing phenotypic and genetic divergence between the derived population and their extant ancestors. However, evolution and demography in these "contemporary ancestors" can complicate inferences about the source (standing genetic variation, de novo mutation) and pace of adaptive divergence. Marine threespine stickleback (Gasterosteus aculeatus) have colonized freshwater environments along the Pacific coast of North America, but have also persisted in the marine environment. To what extent are marine stickleback good proxies of the ancestral condition? RESULTS: We sequenced > 5800 variant loci in over 250 marine stickleback from eight locations extending from Alaska to California, and phenotyped them for platedness and body shape. Pairwise FST varied from 0.02 to 0.18. Stickleback were divided into five genetic clusters, with a single cluster comprising stickleback from Washington to Alaska. Plate number, Eda, body shape, and candidate loci showed evidence of being under selection in the marine environment. Comparisons to a freshwater population demonstrated that candidate loci for freshwater adaptation varied depending on the choice of marine populations. CONCLUSIONS: Marine stickleback are structured into phenotypically and genetically distinct populations that have been evolving as freshwater stickleback evolved. This variation complicates their usefulness as proxies of the ancestors of freshwater populations. Lessons from stickleback may be applied to other "contemporary ancestor"-derived population studies.

Plasticity-mediated persistence in new and changing environments.

Baldwin's synthesis of the Organicist position, first published in 1896 and elaborated in 1902, sought to rescue environmentally induced phenotypes from disrepute by showing their Darwinian significance. Of particular interest to Baldwin was plasticity's mediating role during environmental change or colonization-plastic individuals were more likely to successfully survive and reproduce in new environments than were nonplastic individuals. Once a population of plastic individuals had become established, plasticity could further mediate the future course of evolution. The evidence for plasticity-mediated persistence (PMP) is reviewed here with a particular focus on evolutionary rescue experiments, studies on invasive success, and the role of learning in survival. Many PMP studies are methodologically limited, showing that preexistent plasticity has utility in new environments (soft PMP) rather than directly demonstrating that plasticity is responsible for persistence (hard PMP). An ideal PMP study would be able to demonstrate that (1) plasticity preexisted environmental change, (2) plasticity was fortuitously beneficial in the new environment, (3) plasticity was responsible for individual persistence in the new environment, and (4) plasticity was responsible for population persistence in succeeding generations. Although PMP is not ubiquitous, Baldwin's hypotheses have been largely vindicated in theoretical and empirical studies, but much work remains.

Gene expression plasticity evolves in response to colonization of freshwater lakes in threespine stickleback.

Phenotypic plasticity is predicted to facilitate individual survival and/or evolve in response to novel environments. Plasticity that facilitates survival should both permit colonization and act as a buffer against further evolution, with contemporary and derived forms predicted to be similarly plastic for a suite of traits. On the other hand, given the importance of plasticity in maintaining internal homeostasis, derived populations that encounter greater environmental heterogeneity should evolve greater plasticity. We tested the evolutionary significance of phenotypic plasticity in coastal British Columbian postglacial populations of threespine stickleback (Gasterosteus aculeatus) that evolved under greater seasonal extremes in temperature after invading freshwater lakes from the sea. Two ancestral (contemporary marine) and two derived (contemporary freshwater) populations of stickleback were raised near their thermal tolerance extremes, 7 and 22 °C. Gene expression plasticity was estimated for more than 14,000 genes. Over five thousand genes were similarly plastic in marine and freshwater stickleback, but freshwater populations exhibited significantly more genes with plastic expression than marine populations. Furthermore, several of the loci shown to exhibit gene expression plasticity have been previously implicated in the adaptive evolution of freshwater populations, including a gene involved in mitochondrial regulation (PPARAa). Collectively, these data provide molecular evidence that highlights the importance of plasticity in colonization and adaptation to new environments.

Hybridization effects on phenotypic plasticity: experimental compensatory growth in farmed-wild Atlantic salmon.

Compensatory growth (CG) is a means by which organisms can increase their growth rate above their routine growth rate after a period of environmentally induced growth depression. Despite a focus on the implications of CG for aquaculture, little research has evaluated the effect of domesticated-wild hybridization on CG. Any deviation in the mean compensatory ability of hybrids relative to their wild progenitors, or any notable costs to compensation in terms of body morphology, could affect the ability of hybrids to persist in changing environments. We compared CG of farmed, wild and hybrid (F1, F2, wild backcross) juvenile Atlantic salmon (Salmo salar). Wild salmon experienced both lower routine and CG rates relative to farmed salmon, while hybrids were intermediate. However, the compensatory responses (slopes of the reaction norms) for each cross were parallel, indicating that hybridization did not affect the CG response itself. Morphological costs to compensation were not detected. In addition to contributing to risk assessments of the consequences of interbreeding between wild and escaped domesticated organisms, we conclude that plasticity studies on domesticated-wild hybrids and their progenitors are useful for testing basic predictions about the evolution of phenotypic plasticity, as well as understanding the evolutionary significance of hybrids.