scholarly journals Unique Genomic and Phenotypic Responses to Extreme and Variable pH Conditions in Purple Urchin Larvae

2020 ◽  
Vol 60 (2) ◽  
pp. 318-331
Author(s):  
April D Garrett ◽  
Reid S Brennan ◽  
Anya L Steinhart ◽  
Aubrey M Pelletier ◽  
Melissa H Pespeni
Keyword(s):  
Genetic Variation ◽  
Allele Frequency ◽  
Sea Urchin ◽  
Genetic Basis ◽  
Adaptive Genetic Variation ◽  
Protein Coding ◽  
Purple Sea Urchin ◽  
Ph Conditions ◽  
Frequency Changes ◽  
Genetic Responses

Synopsis Environmental variation experienced by a species across space and time can promote the maintenance of genetic diversity that may be adaptive in future global change conditions. Selection experiments have shown that purple sea urchin, Strongylocentrotus purpuratus, populations have adaptive genetic variation for surviving pH conditions at the “edge” (pH 7.5) of conditions experienced in nature. However, little is known about whether populations have genetic variation for surviving low-pH events beyond those currently experienced in nature or how variation in pH conditions affects organismal and genetic responses. Here, we quantified survival, growth, and allele frequency shifts in experimentally selected developing purple sea urchin larvae in static and variable conditions at three pH levels: pH 8.1 (control), pH 7.5 (edge-of-range), and pH 7.0 (extreme). Variable treatments recovered body size relative to static treatments, but resulted in higher mortality, suggesting a potential tradeoff between survival and growth under pH stress. However, within each pH level, allele frequency changes were overlapping between static and variable conditions, suggesting a shared genetic basis underlying survival to mean pH regardless of variability. In contrast, genetic responses to pH 7.5 (edge) versus pH 7.0 (extreme) conditions were distinct, indicating a unique genetic basis of survival. In addition, loci under selection were more likely to be in exonic regions than regulatory, indicating that selection targeted protein-coding variation. Loci under selection in variable pH 7.5 conditions, more similar to conditions periodically experienced in nature, performed functions related to lipid biosynthesis and metabolism, while loci under selection in static pH 7.0 conditions performed functions related to transmembrane and mitochondrial processes. While these results are promising in that purple sea urchin populations possess genetic variation for surviving extreme pH conditions not currently experienced in nature, they caution that increased acidification does not result in a linear response but elicits unique physiological stresses and survival mechanisms.

scholarly journals The Linked Selection Signature of Rapid Adaptation in Temporal Genomic Data

2019 ◽  
Author(s):  
Vince Buffalo ◽  
Graham Coop
Keyword(s):  
Genetic Variation ◽  
Allele Frequency ◽  
Genomic Data ◽  
Frequency Change ◽  
Rapid Adaptation ◽  
Effective Population ◽  
Additive Genetic Variation ◽  
Analytic Expressions ◽  
Frequency Changes ◽  
Linked Selection

AbstractPopulations can adapt over short, ecological timescales via standing genetic variation. Genomic data collected over tens of generations in both natural and lab populations is increasingly used to find selected loci underpinning such rapid adaptation. Although selection on large effect loci may be detectable in such data, often the fitness differences between individuals have a polygenic architecture, such that selection at any one locus leads to allele frequency changes that are too subtle to distinguish from genetic drift. However, one promising signal comes from the fact that selection on polygenic traits leads to heritable fitness backgrounds that neutral alleles can become stochastically associated with. These associations perturb neutral allele frequency trajectories, creating autocovariance across generations that can be directly measured from temporal genomic data. We develop theory that predicts the magnitude of these temporal autocovariances, showing that it is determined by the level of additive genetic variation, recombination, and linkage disequilibria in a region. Furthermore, by using analytic expressions for the temporal variances and autocovariances in allele frequency, we demonstrate one can estimate the additive genetic variation for fitness and the drift-effective population size from temporal genomic data. Finally, we also show how the proportion of total variation in allele frequency change due to linked selection can be estimated from temporal data. Temporal genomic data offers strong opportunities to identify the role linked selection has on genome-wide diversity over short timescales, and can help bridge population genetic and quantitative genetic studies of adaptation.

scholarly journals Rapid polygenic selection generates fine spatial structure among ecological niches in a well-mixed population

2020 ◽  
Author(s):  
Moritz A. Ehrlich ◽  
Dominique N. Wagner ◽  
Marjorie F. Oleksiak ◽  
Douglas L. Crawford
Keyword(s):  
Genetic Variation ◽  
Natural Selection ◽  
Allele Frequency ◽  
Local Adaptation ◽  
Genetic Variants ◽  
Mixed Population ◽  
Single Generation ◽  
Coastal Basins ◽  
Frequency Changes ◽  
Polygenic Selection

AbstractEvolution by natural selection may be effective enough to allow for recurrent, rapid adaptation to distinct niche environments within a well-mixed population. For this to occur, selection must act on standing genetic variation such that mortality i.e. genetic load, is minimized while polymorphism is maintained. Selection on multiple, redundant loci of small effect provides a potentially inexpensive solution. Yet, demonstrating adaptation via redundant, polygenic selection in the wild remains extremely challenging because low per-locus effect sizes and high genetic redundancy severely reduce statistical power. One approach to facilitate identification of loci underlying polygenic selection is to harness natural replicate populations experiencing similar selection pressures that harbor high within-, yet negligible among-population genetic variation. Such populations can be found among the teleost Fundulus heteroclitus. F. heteroclitus inhabits salt marsh estuaries that are characterized by high environmental heterogeneity e.g. tidal ponds, creeks, coastal basins. Here, we sample four of these heterogeneous niches (one coastal basin and three replicate tidal ponds) at two time points from among a single, panmictic F. heteroclitus population. We identify 10,861 single nucleotide polymorphisms using a genotyping-by-sequencing approach and quantify temporal allele frequency change within, as well as spatial divergence among subpopulations residing in these niches. We find a significantly elevated number of concordant allele frequency changes among all subpopulations, suggesting ecosystem-wide adaptation to a common selection pressure. Remarkably, we also find an unexpected number of temporal allele frequency changes that generate fine-scale divergence among subpopulations, suggestive of local adaptation to distinct niche environments. Both patterns are characterized by a lack of large-effect loci yet an elevated total number of significant loci. Adaptation via redundant, polygenic selection offers a likely explanation for these patterns as well as a potential mechanism for polymorphism maintenance in the F. heteroclitus system.Author SummaryEvolution by adaptation to local environmental conditions may occur more rapidly than previously thought. Recent studies show that natural selection is extremely effective when acting on, not one, but multiple genetic variants that are already present in a population. Here, we show that polygenic selection can lead to adaptation within a single generation by studying a wild, well-mixed population of mud minnows inhabiting environmentally distinct locations or niches (i.e. tidal ponds and coastal basins). We monitor allele proportions at over 10,000 genetic variants over time within a single generation and find a significant number to be changing substantially in every niche, suggestive of natural selection. We further demonstrate this genetic change to be non-random, generating mild, yet significant divergence between residents inhabiting distinct niches, indicative of local adaptation. We corroborate a previous study which discovered similar genetic divergence among niches during a different year, suggesting that local adaptation via natural selection occurs every generation. We show polygenic selection on standing genetic variation to be an effective and evolutionarily inexpensive mechanism, allowing organisms to rapidly adapt to their environments even at extremely short time scales. Our study provides valuable insights into the rate of evolution and the ability of organisms to respond to environmental change.

scholarly journals Rare genetic variation and balanced polymorphisms are important for survival in global change conditions

2018 ◽  
Author(s):  
Reid S. Brennan ◽  
April D. Garrett ◽  
Kaitlin E. Huber ◽  
Heidi Hargarten ◽  
Melissa H. Pespeni
Keyword(s):  
Genetic Variation ◽  
Global Change ◽  
Rare Variants ◽  
Balancing Selection ◽  
Large Population ◽  
Allele Frequencies ◽  
Adaptive Genetic Variation ◽  
Ph Tolerance ◽  
Rare Genetic Variation ◽  
Ph Conditions

AbstractStanding genetic variation is important for population persistence in extreme environmental conditions. While some species may have the capacity to adapt to predicted average future global change conditions, the ability to survive extreme events is largely unknown. We used single generation selection experiments on hundreds of thousands of Strongylocentrotus purpuratus sea urchin larvae generated from wild-caught adults to identify adaptive genetic variation responsive to moderate (pH 8.0) and extreme (pH 7.5) low pH conditions. Sequencing genomic DNA from pools of larvae, we identified consistent changes in allele frequencies across replicate cultures of both conditions and observed increased linkage disequilibrium around selected loci, revealing selection on recombined standing genetic variation. We found that loci responding uniquely to either selection regime were at low starting allele frequencies while variants that responded to both pH conditions (11.6% of selected variants) started at high frequencies. Loci under selection performed functions related to energetics, pH tolerance, cell growth, and actin/cytoskeleton dynamics. These results highlight that persistence in future conditions will require two classes of genetic variation: common, pH-responsive variants maintained by balancing selection in a heterogeneous environment, and rare variants, particularly for extreme conditions, that must be maintained by large population sizes.

scholarly journals A Population Genomic Assessment of Three Decades of Evolution in a Natural Drosophila Population

2021 ◽  
Author(s):  
Jeremy D Lange ◽  
Heloise Bastide ◽  
Justin B Lack ◽  
John E Pool
Keyword(s):  
Genetic Variation ◽  
Population Size ◽  
Effective Population Size ◽  
Allele Frequency ◽  
Effective Population ◽  
Pyrethroid Insecticides ◽  
Time Points ◽  
Multiple Sampling ◽  
A Genome ◽  
Frequency Changes

Population genetics seeks to illuminate the forces shaping genetic variation, often based on a single snapshot of genomic variation. However, utilizing multiple sampling times to study changes in allele frequencies can help clarify the relative roles of neutral and non-neutral forces on short time scales. This study compares whole-genome sequence variation of recently collected natural population samples of Drosophila melanogaster against a collection made approximately 35 years prior from the same locality - encompassing roughly 500 generations of evolution. The allele frequency changes between these time points would suggest a relatively small local effective population size on the order of 10,000, significantly smaller than the global effective population size of the species. Some loci display stronger allele frequency changes than would be expected anywhere in the genome under neutrality - most notably the tandem paralogs Cyp6a17 and Cyp6a23, which are impacted by structural variation associated with resistance to pyrethroid insecticides. We find a genome-wide excess of outliers for high genetic differentiation between old and new samples, but a larger number of adaptation targets may have affected SNP-level differentiation versus window differentiation. We also find evidence for strengthening latitudinal allele frequency clines: northern-associated alleles have increased in frequency by an average of nearly 2.5% at SNPs previously identified as clinal outliers, but no such pattern is observed at random SNPs. This project underscores the scientific potential of using multiple sampling time points to investigate how evolution operates in natural populations, by quantifying how genetic variation has changed over ecologically relevant timescales.

scholarly journals Rare genetic variation and balanced polymorphisms are important for survival in global change conditions

2019 ◽  
Vol 286 (1904) ◽  
pp. 20190943 ◽  
Author(s):  
Reid S. Brennan ◽  
April D. Garrett ◽  
Kaitlin E. Huber ◽  
Heidi Hargarten ◽  
Melissa H. Pespeni
Keyword(s):  
Genetic Variation ◽  
Global Change ◽  
Rare Variants ◽  
Balancing Selection ◽  
Large Population ◽  
Allele Frequencies ◽  
Adaptive Genetic Variation ◽  
Ph Tolerance ◽  
Rare Genetic Variation ◽  
Ph Conditions

Standing genetic variation is important for population persistence in extreme environmental conditions. While some species may have the capacity to adapt to predicted average future global change conditions, the ability to survive extreme events is largely unknown. We used single-generation selection experiments on hundreds of thousands of Strongylocentrotus purpuratus sea urchin larvae generated from wild-caught adults to identify adaptive genetic variation responsive to moderate (pH 8.0) and extreme (pH 7.5) low-pH conditions. Sequencing genomic DNA from pools of larvae, we identified consistent changes in allele frequencies across replicate cultures for each pH condition and observed increased linkage disequilibrium around selected loci, revealing selection on recombined standing genetic variation. We found that loci responding uniquely to either selection regime were at low starting allele frequencies while variants that responded to both pH conditions (11.6% of selected variants) started at high frequencies. Loci under selection performed functions related to energetics, pH tolerance, cell growth and actin/cytoskeleton dynamics. These results highlight that persistence in future conditions will require two classes of genetic variation: common, pH-responsive variants maintained by balancing selection in a heterogeneous environment, and rare variants, particularly for extreme conditions, that must be maintained by large population sizes.

scholarly journals Polygenic selection within a single generation leads to subtle divergence among ecological niches

2020 ◽  
Author(s):  
Moritz A Ehrlich ◽  
Dominique N Wagner ◽  
Marjorie F Oleksiak ◽  
Douglas L Crawford
Keyword(s):  
Genetic Variation ◽  
Allele Frequency ◽  
Local Adaptation ◽  
Ecological Niches ◽  
Frequency Change ◽  
Heterogeneous Environments ◽  
Nucleotide Polymorphisms ◽  
Single Generation ◽  
Frequency Changes ◽  
Polygenic Selection

Abstract Selection on standing genetic variation may be effective enough to allow for adaptation to distinct niche environments within a single generation. Minor allele frequency changes at multiple, redundant loci of small effect can produce remarkable phenotypic shifts. Yet, demonstrating rapid adaptation via polygenic selection in the wild remains challenging. Here we harness natural replicate populations that experience similar selection pressures and harbor high within-, yet negligible among-population genetic variation. Such populations can be found among the teleost Fundulus heteroclitus which inhabits marine estuaries characterized by high environmental heterogeneity. We identify 10,861 single nucleotide polymorphisms in F. heteroclitus that belong to a single, panmictic population yet reside in environmentally distinct niches (one coastal basin and three replicate tidal ponds). By sampling at two time-points within a single generation we quantify both allele frequency change within as well as spatial divergence among niche subpopulations. We observe few individually significant allele frequency changes yet find that the number of moderate changes exceeds the neutral expectation by 10-100%. We find allele frequency changes to be significantly concordant in both direction and magnitude among all niche subpopulations, suggestive of parallel selection. In addition, within-generation allele frequency changes generate subtle but significant divergence among niches, indicative of local adaptation. Although we cannot distinguish between selection and genotype-dependent migration as drivers of within-generation allele frequency changes, the trait/s determining fitness and/or migration likelihood appear to be polygenic. In heterogeneous environments, polygenic selection and polygenic, genotype-dependent migration offer conceivable mechanisms for within-generation, local adaptation to distinct niches.

Sign in / Sign up

Export Citation Format

Share Document