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Dalziel, Anne C.; Vines, Timothy H.; Schulte, Patricia M. 2011-10-14 We compared ancestral anadromous-marine and nonmigratory, stream-resident threespine stickleback (Gasterosteus aculeatus) populations to examine the outcome of relaxed selection on prolonged swimming performance. We reared marine and stream-resident fish from two locations in a common environment and found that both stream-resident populations had lower critical swimming speeds (Ucrits) than marine populations. F1 hybrids from the two locations displayed significant differences in dominance, suggesting that the genetic basis for variation in Ucrit differs between locations. To determine which traits evolved in conjunction with, and may underlie, differences in performance capacity we measured a suite of traits known to affect prolonged swimming performance in fishes. While some candidate traits did not evolve (standard metabolic rate and two body shape traits), multiple morphological (pectoral fin size, shape and four body shape measures) and physiological (maximum metabolic rate; MMR) traits evolved in the predicted direction in both stream-resident populations. However, data from F1 hybrids suggested that only one of these traits (MMR) had dominance effects similar to those of Ucrit in both locations. Overall, our data suggest that reductions in prolonged swimming performance were selected for in non-migratory populations of threespine stickleback, and that decreases in MMR may mediate these reductions in performance.
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Gibbons, Taylor C.; Rudman, Seth M.; Schulte, Patricia M. 2015-12-02 Abiotic factors can act as barriers to colonization and drive local adaptation. During colonization, organisms may cope with changes in abiotic factors using existing phenotypic plasticity, but the role of phenotypic plasticity in assisting or hindering the process of local adaptation remains unclear. To address these questions, we explore the role of winter conditions in driving divergence during freshwater colonization and the effects of plasticity on local adaptation in ancestral marine and derived freshwater ecotypes of threespine stickleback (Gasterosteus aculeatus). We found that freshwater-resident stickleback had greater tolerance of acute exposure to low temperatures than marine stickleback, but these differences were abolished after acclimation to simulated winter conditions (9L:15D photoperiod at 4°C). Plasma chloride levels differed between the ecotypes, but showed a similar degree of plasticity between ecotypes. Gene expression of the epithelial calcium channel (ECaC) differed between ecotypes, with the freshwater ecotype demonstrating substantially greater expression than the marine ecotype, but there was no plasticity in this trait under these conditions in either ecotype. In contrast, growth (assessed as final mass) and the expression of an isoform of the electroneutral Na+/H+ exchanger (NHE3) exhibited substantial change with temperature in the marine ecotype that was not observed in the freshwater ecotype under the conditions tested here, which is consistent with evolution of these traits by a process such as genetic assimilation. These data demonstrate substantial divergence in many of these traits between freshwater and marine stickleback, but also illustrate the complexity of possible relationships between plasticity and local adaptation.
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Healy, Timothy M.; Bryant, Heather J.; Schulte, Patricia M. 2016-11-29 Adjustments of aerobic metabolic processes are critical components of organismal responses to environmental change that require tight co-ordination between the nuclear and mitochondrial genomes. Intraspecific differences in mitochondrial genotype can affect gene transcription in both genomes. Thus, variation in mitochondrial genotype may be associated with differences in the plasticity of gene expression when organisms are faced with changes in environmental conditions. Cold acclimation is known to result in metabolic responses involving increases in mitochondrial amount and capacity, suggesting that low temperatures may pose a particular challenge when co-ordinating the functions of the nuclear and mitochondrial genomes. In this study, we utilized RNA-seq to assess transcriptome-wide gene expression in the muscle of Atlantic killifish (Fundulus heteroclitus) from a population that contains segregating variation in mitochondrial genotype. We examined gene expression plasticity in response to 5°C acclimation and the effects of mitochondrial genotype on this plasticity. Cold acclimation resulted in changes in gene expression consistent with up-regulation of genes involved in many cellular functions, including spliceosomal and proteasomal processes, and with down-regulation of genes involved in extracellular matrix, muscle contraction and oxidative phosphorylation functions. There were few differences in gene expression between killifish with different mitochondrial genotypes: 14 genes demonstrated significant interactions between mitochondrial genotype and acclimation temperature and 3 genes demonstrated effects of mitochondrial genotype alone. These results indicate that variation in mitochondrial genotype has modest effects on gene expression; the majority of which are revealed as differences in plasticity as a result of environmental change.
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Dalziel, Anne C.; Bittman, Jesse; Mandic, Milica; Ou, Michelle; Schulte, Patricia M. 2014-06-05 The Salmoniform whole-genome duplication is hypothesized to have facilitated the evolution of anadromy, but little is known about the contribution of paralogs from this event to the physiological performance traits required for anadromy, such as salinity tolerance. Here, we determined when two candidate salinity-responsive paralogs of the Na+, K+ ATPase α subunit (α1a and α1b) evolved and studied their evolutionary trajectories and tissue-specific expression patterns. We found that these paralogs arose during a small scale duplication event prior to the Salmoniform, but after the teleost, whole-genome duplication. The ‘freshwater paralog’ (α1a) is primarily expressed in the gills of Salmoniformes and an unduplicated freshwater sister-species (Esox lucius), and experienced positive selection in the fresh-water ancestor of Salmoniformes and Esociformes. Contrary to our predictions, the ‘saltwater paralog’ (α1b), which is more widely expressed than α1a, did not experience positive selection during the evolution of anadromy in the Coregoninae and Salmonine. To determine if parallel mutations in Na+, K+ ATPase α1 may contribute to salinity tolerance in other fishes, we studied independently evolved salinity-responsive Na+, K+ ATPase α1 paralogs in Anabas testudineus and Oreochromis mossambicus. We found that a quarter of the mutations occurring between salmonid α1a and α1b in functionally important sites also evolved in parallel in at least one of these species. Together, these data argue that paralogs contributing to salinity tolerance evolved prior to the Salmoniform whole-genome duplication and that strong selection and/or functional constraints have led to parallel evolution in salinity-responsive Na+, K+ ATPase α1 paralogs in fishes.
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Metzger, David C.H.; Schulte, Patricia M.; Metzger, David C. H. 2018-03-29 Phenotypic plasticity occurs at a variety of time-scales, but little is known about the degree to which plastic responses at different time-scales are associated with similar underlying molecular processes, which is critical for assessing the effects of plasticity on evolutionary trajectories. To address this issue, we identified differential gene expression in response to developmental temperature in the muscle transcriptome of adult threespine stickleback (Gasterosteus aculeatus) exposed to 12, 18, and 24 °C until hatch and then held at 18 °C for nine months, and compared these results to differential gene expression in response to adult thermal acclimation in stickleback developed at 18 °C and then acclimated to 5 and 25 °C as adults. Adult thermal acclimation affected the expression of 7,940 and 7,015 genes in response to cold and warm acclimation, respectively, and 4,851 of these genes responded in both treatments. In contrast, the expression of only 33 and 29 genes were affected by cold and warm development, respectively. The majority of the genes affected by developmental temperature were also affected by adult acclimation temperature. Many genes that were differentially expressed as a result of adult acclimation were associated with previously identified temperature-dependent effects on DNA methylation patterns, suggesting a role of epigenetic mechanisms in regulating gene expression plasticity during acclimation. Taken together, these results demonstrate similarities between the persistent effects of developmental plasticity on gene expression and the effects of adult thermal acclimation, emphasizing the potential for mechanistic links between plasticity acting at these different life stages.

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