Reduced swimming performance repeatedly evolves on loss of migration in landlocked populations of alewife

Author Posting. © University of Chicago, 2018. This article is posted here by permission of University of Chicago Press for personal use, not for redistribution. The definitive version was published in Physiological and Biochemical Zoology 91 (2018):814–825, doi:10.1086/696877.Whole-organism performance tasks are accomplished by the integration of morphological traits and physiological functions. Understanding how evolutionary change in morphology and physiology influences whole-organism performance will yield insight into the factors that shape its own evolution. We demonstrate that nonmigratory populations of alewife (Alosa pseudoharengus) have evolved reduced swimming performance in parallel, compared with their migratory ancestor. In contrast to theoretically and empirically based predictions, poor swimming among nonmigratory populations is unrelated to the evolution of osmoregulation and occurs despite the fact that nonmigratory alewives have a more fusiform (torpedo-like) body shape than their ancestor. Our results suggest that elimination of long-distance migration from the life cycle has shaped performance more than changes in body shape and physiological regulatory capacity.Funding was provided by the University of Connecticut’s Department of Ecology and Evolutionary Biology and El Muy Viejo.2019-01-3

Reduced swimming performance repeatedly evolves on loss of migration in landlocked populations of alewife

Author Posting. © University of Chicago, 2018. This article is posted here by permission of University of Chicago Press for personal use, not for redistribution. The definitive version was published in Physiological and Biochemical Zoology 91 (2018):814–825, doi:10.1086/696877.Whole-organism performance tasks are accomplished by the integration of morphological traits and physiological functions. Understanding how evolutionary change in morphology and physiology influences whole-organism performance will yield insight into the factors that shape its own evolution. We demonstrate that nonmigratory populations of alewife (Alosa pseudoharengus) have evolved reduced swimming performance in parallel, compared with their migratory ancestor. In contrast to theoretically and empirically based predictions, poor swimming among nonmigratory populations is unrelated to the evolution of osmoregulation and occurs despite the fact that nonmigratory alewives have a more fusiform (torpedo-like) body shape than their ancestor. Our results suggest that elimination of long-distance migration from the life cycle has shaped performance more than changes in body shape and physiological regulatory capacity.Funding was provided by the University of Connecticut’s Department of Ecology and Evolutionary Biology and El Muy Viejo.2019-01-3

Freshwater Transitions and the Evolution of Osmoregulation in the Alewife

The transition from seawater to freshwater is deeply rooted in the evolutionary history of animals, initiating the radiation and speciation of many taxa. However, crossing the boundary into freshwater from the sea represents a considerable physiological challenge for animals that maintain a near constant internal ion concentration. Because seawater and freshwater differ strongly in solute concentration, the transition into freshwater must involve the evolution of ion and water balance; yet, we have a limited understanding of the physiological modifications that facilitate this transition. Here, I investigate the evolution of the osmoregulatory system upon transition to freshwater using populations of an ancestrally anadromous fish, the Alewife (Alosa pseudoharengus), which has become landlocked on multiple, independent occasions. I take an integrative approach, exploring the molecular, physiological, and whole-organism level consequences of the freshwater transition. Overall, my dissertation demonstrates that the transition to freshwater in the Alewife leads to evolutionary shifts in osmoregulatory capacity, which may be driven by changes in the mechanisms of ion exchange at the gill. In chapter 2, I show that landlocking leads to the partial loss of seawater tolerance and hypoosmoregulatory performance, which may be mediated through reductions in expression and activity of genes for gill ion secretion. Chapter 3 demonstrates that several independently derived landlocked populations vary in the degree of seawater tolerance loss, and that this variation is negatively correlated with freshwater tolerance. This suggests that trade-offs in osmoregulation follow local adaptation to freshwater. In chapter 4, I use next generation sequencing to show that thousands of genes have differentiated in expression between Alewife life history forms. Comparison of gill transcriptomes of anadromous and landlocked Alewives reveals that changes in the regulation of transcription of genes in gill ion exchange pathways may underlie evolutionary changes in osmoregulation. In chapter 5, I demonstrate that landlocked Alewives are poor swimmers compared to anadromous Alewives, and that differences in swimming ability are not explained by differences in osmoregulatory performance or body shape. These results suggest that reductions in swimming performance among landlocked Alewives may be a function of relaxed selection on migration capacity

Physiological and genomic evidence that selection on the transcription factor Epas1 has altered cardiovascular function in highaltitude deer mice

Evolutionary adaptation to extreme environments often requires coordinated changes in multiple intersecting physiological pathways, but how such multi-trait adaptation occurs remains unresolved. Transcription factors, which regulate the expression of many genes and can simultaneously alter multiple phenotypes, may be common targets of selection if the benefits of induced changes outweigh the costs of negative pleiotropic effects. We combined complimentary population genetic analyses and physiological experiments in North American deer mice (Peromyscus maniculatus) to examine links between genetic variation in transcription factors that coordinate physiological responses to hypoxia (hypoxia-inducible factors, HIFs) and multiple physiological traits that potentially contribute to high-altitude adaptation. First, we sequenced the exomes of 100 mice sampled from different elevations and discovered that several SNPs in the gene Epas1, which encodes the oxygen sensitive subunit of HIF-2α, exhibited extreme allele frequency differences between highland and lowland populations. Broader geographic sampling confirmed that Epas1 genotype varied predictably with altitude throughout the western US. We then discovered that Epas1 genotype influences heart rate in hypoxia, and the transcriptomic responses to hypoxia (including HIF targets and genes involved in catecholamine signaling) in the heart and adrenal gland. Finally, we used a demographically-informed selection scan to show that Epas1 variants have experienced a history of spatially varying selection, suggesting that differences in cardiovascular function and gene regulation contribute to high-altitude adaptation. Our results suggest a mechanism by which Epas1 may aid long-term survival of high-altitude deer mice and provide general insights into the role that highly pleiotropic transcription factors may play in the process of environmental adaptation

Paralog switching facilitates diadromy: Ontogenetic, microevolutionary and macroevolutionary evidence

Euryhalinity is present in diverse aquatic taxa and requires flexible osmoregulation to field the challenges posed by differing salinities. Na+, K+-ATPase (NKA) is a ubiquitous ion pump in the gills of fishes and, for some species, paralogs of the catalytic -subunit (NKA 1a and NKA 1b) exhibit reciprocal expression between fresh- and seawater, termed paralog-switching. We investigated the expression and evolution of NKA paralogs in Alewife (Alosa pseudoharengus), a euryhaline and migratory fish. Comparisons between landlocked and diadromous life history forms and migrant and pre-migrant ontogenetic stages were used to study shifts in NKA paralog expression related to freshwater or seawater specialization. We exposed juvenile diadromous and landlocked alewives to freshwater (0 ppt) and seawater (30 ppt) for 2, 5, and 15 days. Additionally, we sampled migrant and pre-migrant alewives from the natal freshwater environment or after 24 hours in seawater. Diadromous Alewife exhibited salinity- dependent paralog switching, and the freshwater-specialized landlocked life history form showed greater upregulation of NKA 1b in seawater. Migrant Alewife showed a loss of freshwater readiness traded for seawater specialization through greater reliance (via upregulation) on NKA 1a in freshwater. Molecular phylogenies show Alewife NKA paralogs originated independently of paralogs in salmonids and other members of Euteleosteomorpha. This study demonstrated that NKA paralog switching is tied to halohabitat profile and that duplications of the ancestral NKA gene provided the substrate for multiple, independent molecular solutions for supporting a diadromous life history

Repeated Targets of Natural Selection during Ecological Transitions of Fish Across Salinity Boundaries

Ecological transitions across salinity boundaries have led to some of the most important diversification events in the animal kingdom, especially among fishes. Adaptations accompanying such transitions include changes in morphology, diet, whole-organism performance, and osmoregulatory function, which may be particularly prominent since divergent salinity regimes make opposing demands on systems that maintain ion and water balance. Research in the last decade has focused on the genetic targets underlying such adaptations, most notably by comparing populations of species that are distributed across salinity boundaries. Here, we synthesize research on the targets of natural selection using whole-genome approaches, with a particular emphasis on the osmoregulatory system. Given the complex, integrated and polygenic nature of this system, we expected that signatures of natural selection would span numerous genes across functional levels of osmoregulation, especially salinity sensing, hormonal control, and cellular ion exchange mechanisms. We find support for this prediction: genes coding for V-type, Ca2+, and Na+/K+-ATPases, which are key cellular ion exchange enzymes, are especially common targets of selection in species from six orders of fishes. This indicates that while polygenic selection contributes to adaptation across salinity boundaries, changes in ATPase enzymes may be of particular importance in supporting such transitions

Data from: Transcriptomic imprints of adaptation to fresh water: parallel evolution of osmoregulatory gene expression in the Alewife

Comparative approaches in physiological genomics offer an opportunity to understand the functional importance of genes involved in niche exploitation. We used populations of Alewife (Alosa pseudoharengus) to explore the transcriptional mechanisms that underlie adaptation to fresh water. Ancestrally anadromous Alewives have recently formed multiple, independently derived, landlocked populations, which exhibit reduced tolerance of saltwater and enhanced tolerance of fresh water. Using RNA-seq, we compared transcriptional responses of an anadromous Alewife population to two landlocked populations after acclimation to fresh (0 ppt) and saltwater (35 ppt). Our results suggest that the gill transcriptome has evolved in primarily discordant ways between independent landlocked populations and their anadromous ancestor. By contrast, evolved shifts in the transcription of a small suite of well-characterized osmoregulatory genes exhibited a strong degree of parallelism. In particular, transcription of genes that regulate gill ion exchange has diverged in accordance with functional predictions: freshwater ion-uptake genes (most notably, the ‘freshwater paralog’ of Na+/K+-ATPase α-subunit) were more highly expressed in landlocked forms, whereas genes that regulate saltwater ion secretion (e.g. the ‘saltwater paralog’ of NKAα) exhibited a blunted response to saltwater. Parallel divergence of ion transport gene expression is associated with shifts in salinity tolerance limits among landlocked forms, suggesting that changes to the gill's transcriptional response to salinity facilitate freshwater adaptation

Physiological and genomic evidence that selection on the transcription factor Epas1 has altered cardiovascular function in highaltitude deer mice

Evolutionary adaptation to extreme environments often requires coordinated changes in multiple intersecting physiological pathways, but how such multi-trait adaptation occurs remains unresolved. Transcription factors, which regulate the expression of many genes and can simultaneously alter multiple phenotypes, may be common targets of selection if the benefits of induced changes outweigh the costs of negative pleiotropic effects. We combined complimentary population genetic analyses and physiological experiments in North American deer mice (Peromyscus maniculatus) to examine links between genetic variation in transcription factors that coordinate physiological responses to hypoxia (hypoxia-inducible factors, HIFs) and multiple physiological traits that potentially contribute to high-altitude adaptation. First, we sequenced the exomes of 100 mice sampled from different elevations and discovered that several SNPs in the gene Epas1, which encodes the oxygen sensitive subunit of HIF-2α, exhibited extreme allele frequency differences between highland and lowland populations. Broader geographic sampling confirmed that Epas1 genotype varied predictably with altitude throughout the western US. We then discovered that Epas1 genotype influences heart rate in hypoxia, and the transcriptomic responses to hypoxia (including HIF targets and genes involved in catecholamine signaling) in the heart and adrenal gland. Finally, we used a demographically-informed selection scan to show that Epas1 variants have experienced a history of spatially varying selection, suggesting that differences in cardiovascular function and gene regulation contribute to high-altitude adaptation. Our results suggest a mechanism by which Epas1 may aid long-term survival of high-altitude deer mice and provide general insights into the role that highly pleiotropic transcription factors may play in the process of environmental adaptation

CombinedAnnotation_alewife_nr

Alewife gill transcriptome annotation