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Dalziel, Anne C.; Laporte, Martin; Rougeux, Clément; Guderley, Helga; Bernatchez, Louis 2016-09-20 The repeated evolution of similar phenotypes by similar mechanisms can be indicative of local adaptation, constraints or biases in the evolutionary process. Little is known about the incidence of physiological convergence in natural populations, so here we test whether energy metabolism in ‘dwarf’ and ‘normal’ Lake Whitefish evolves by similar mechanisms. Prior genomic and transcriptomic studies have found that divergence in energy metabolism is key to local adaptation in whitefish species pairs, but that distinct genetic and transcriptomic changes often underlie phenotypic evolution among lakes. Here, we predicted that traits at higher levels of biological organization, including the activities of energy metabolism enzymes (the product of enzyme concentration and turnover rate) and the relative proportions of metabolically active tissues (heart, liver, skeletal muscle), would show greater convergence than genetic and transcriptomic variation. We compared four whitefish species pairs and found convergence in organ size whereby all dwarf whitefish populations have a higher proportion of red skeletal muscle, three have relatively larger livers and two have relatively larger ventricles than normal fish. On the other hand, hepatic and muscle enzyme activities showed little convergence and were largely dependent on lake of origin. Only the most genetically divergent species pair (Cliff Lake) displayed white muscle enzyme activities matching results from laboratory-reared normal and dwarf whitefish. Overall, these data show convergence in the evolution of organ size, but not in the activities of candidate enzymes of energy metabolism, which may have evolved mainly as a consequence of demographic or ecological differences among lakes.
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Dalziel, Anne C.; Martin, Nicolas; Laporte, Martin; Guderley, Helga; Bernatchez, Louis 2015-07-09 The physiological mechanisms underlying local adaptation in natural populations of animals, and whether the same mechanisms contribute to adaptation and acclimation, are largely unknown. Therefore, we tested for evolutionary divergence in aerobic exercise physiology in laboratory bred, size-matched crosses of ancestral, benthic, normal Lake Whitefish (Coregonus clupeaformis) and derived, limnetic, more actively-swimming ‘dwarf’ ecotypes. We acclimated fish to constant swimming (emulating limnetic foraging) and control conditions (emulating normal activity levels) to simultaneously study phenotypic plasticity. We found extensive divergence between ecotypes: dwarf fish generally had constitutively higher values of traits related to oxygen transport (ventricle size) and use by skeletal muscle (percent oxidative muscle, mitochondrial content), and also evolved differential plasticity of mitochondrial function (Complex I activity and flux through Complexes I-IV and IV). The effects of swim-training were less pronounced than differences among ecotypes and the traits which had a significant training effect (ventricle protein content, ventricle MDH activity and muscle Complex V activity) did not differ among ecotypes. Only one trait, ventricle mass, varied in a similar manner with acclimation and adaptation and followed a pattern consistent with genetic accommodation. Overall, the physiological and biochemical mechanisms underlying acclimation and adaptation to swimming activity in Lake Whitefish generally differ.
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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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Vines, Timothy H.; Dalziel, Anne C.; Albert, Arianne; Veen, Thor; Schulte, Patricia Marita; Schluter, Dolph; Albert, Arianne Y. K. 2016-03-25 Strong ecological selection on a genetic locus can maintain allele frequency differences between populations in different environments, even in the face of hybridization. When alleles at divergent loci come into tight linkage disequilibrium, selection acts on them as a unit and can significantly reduce gene flow. For populations interbreeding across a hybrid zone, linkage disequilibria between loci can force clines to share the same slopes and centers. However, strong ecological selection on a locus can also pull its cline away from the others, reducing linkage disequilibrium and weakening the barrier to gene flow. We looked for this ‘cline uncoupling’ effect in a hybrid zone between stream resident and anadromous sticklebacks at two genes known to be under divergent natural selection (Eda and ATP1a1) and five morphological traits that repeatedly evolve in freshwater stickleback. These clines were all steep and located together at the top of the estuary, such that we found no evidence for cline uncoupling. However, we did not observe the stepped shape normally associated with steep concordant clines. It thus remains possible that these clines cluster together because their individual selection regimes are identical, but this would be very surprising given their diverse roles in osmoregulation, body armor and swimming performance. https://creativecommons.org/publicdomain/zero/1.0/
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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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