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

2019 ◽  
Author(s):  
Vince Buffalo ◽  
Graham Coop

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.

2019 ◽  
Author(s):  
Vince Buffalo ◽  
Graham Coop

AbstractRapid phenotypic adaptation is often observed in natural populations and selection experiments. However, detecting the genome-wide impact of this selection is difficult, since adaptation often proceeds from standing variation and selection on polygenic traits, both of which may leave faint genomic signals indistinguishable from a noisy background of genetic drift. One promising signal comes from the genome-wide covariance between allele frequency changes observable from temporal genomic data, e.g. evolve-and-resequence studies. These temporal covariances reflect how heritable fitness variation in the population leads changes in allele frequencies at one timepoint to be predictive of the changes at later timepoints, as alleles are indirectly selected due to remaining associations with selected alleles. Since genetic drift does not lead to temporal covariance, we can use these covariances to estimate what fraction of the variation in allele frequency change through time is driven by linked selection. Here, we reanalyze three selection experiments to quantify the effects of linked selection over short timescales using covariance among time-points and across replicates. We estimate that at least 17% to 37% of allele frequency change is driven by selection in these experiments. Against this background of positive genome-wide temporal covariances we also identify signals of negative temporal covariance corresponding to reversals in the direction of selection for a reasonable proportion of loci over the time course of a selection experiment. Overall, we find that in the three studies we analyzed, linked selection has a large impact on short-term allele frequency dynamics that is readily distinguishable from genetic drift.Significance StatementA long-standing problem in evolutionary biology is to understand the processes that shape the genetic composition of populations. In a population without migration, the two processes that change allele frequencies are selection, which increases beneficial alleles and removes deleterious ones, and genetic drift which randomly changes frequencies as some parents contribute more or less alleles to the next generation. Previous efforts to disentangle these processes have used genomic samples from a single timepoint and models of how selection affects neighboring sites (linked selection). Here, we use genomic data taken through time to quantify the contributions of selection and drift to genome-wide frequency changes. We show selection acts over short timescales in three evolve-and-resequence studies and has a sizable genome-wide impact.


2021 ◽  
Author(s):  
Rose M.H. Driscoll ◽  
Felix E.G. Beaudry ◽  
Elissa J Cosgrove ◽  
Reed Bowman ◽  
John W Fitzpatrick ◽  
...  

Sex-biased demography, including sex-biased survival or migration, can impact allele frequency changes across the genome. In particular, we can expect different patterns of genetic variation on autosomes and sex chromosomes due to sex-specific differences in life histories, as well as differences in effective population size, transmission modes, and the strength and mode of selection. Here, we demonstrate the role that sex differences in life history played in shaping short-term evolutionary dynamics across the genome. We used a 25-year pedigree and genomic dataset from a long-studied population of Florida Scrub-Jays (Aphelocoma coerulescens) to directly characterize the relative roles of sex-biased demography and inheritance in shaping genome-wide allele frequency trajectories. We used gene dropping simulations to estimate individual genetic contributions to future generations and to model drift and immigration on the known pedigree. We quantified differential expected genetic contributions of males and females over time, showing the impact of sex-biased dispersal in a monogamous system. Due to female-biased dispersal, more autosomal variation is introduced by female immigrants. However, due to male-biased transmission, more Z variation is introduced by male immigrants. Finally, we partitioned the proportion of variance in allele frequency change through time due to male and female contributions. Overall, most allele frequency change is due to variance in survival and births. Males and females have similar contributions to autosomal allele frequency change, but males have higher contributions to allele frequency change on the Z chromosome. Our work shows the importance of understanding sex-specific demographic processes in accounting for genome-wide allele frequency change in wild populations.


2020 ◽  
Vol 117 (34) ◽  
pp. 20672-20680
Author(s):  
Vince Buffalo ◽  
Graham Coop

Rapid phenotypic adaptation is often observed in natural populations and selection experiments. However, detecting the genome-wide impact of this selection is difficult since adaptation often proceeds from standing variation and selection on polygenic traits, both of which may leave faint genomic signals indistinguishable from a noisy background of genetic drift. One promising signal comes from the genome-wide covariance between allele frequency changes observable from temporal genomic data (e.g., evolve-and-resequence studies). These temporal covariances reflect how heritable fitness variation in the population leads changes in allele frequencies at one time point to be predictive of the changes at later time points, as alleles are indirectly selected due to remaining associations with selected alleles. Since genetic drift does not lead to temporal covariance, we can use these covariances to estimate what fraction of the variation in allele frequency change through time is driven by linked selection. Here, we reanalyze three selection experiments to quantify the effects of linked selection over short timescales using covariance among time points and across replicates. We estimate that at least 17 to 37% of allele frequency change is driven by selection in these experiments. Against this background of positive genome-wide temporal covariances, we also identify signals of negative temporal covariance corresponding to reversals in the direction of selection for a reasonable proportion of loci over the time course of a selection experiment. Overall, we find that in the three studies we analyzed, linked selection has a large impact on short-term allele frequency dynamics that is readily distinguishable from genetic drift.


2021 ◽  
Author(s):  
Jeremy D Lange ◽  
Heloise Bastide ◽  
Justin B Lack ◽  
John E Pool

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.


Genetics ◽  
1995 ◽  
Vol 139 (2) ◽  
pp. 1077-1090 ◽  
Author(s):  
P E Jorde ◽  
N Ryman

Abstract In this paper we study the process of allele frequency change in finite populations with overlapping generations with the purpose of evaluating the possibility of estimating the effective size from observations of temporal frequency shifts of selectively neutral alleles. Focusing on allele frequency changes between successive cohorts (individuals born in particular years), we show that such changes are not determined by the effective population size alone, as they are when generations are discrete. Rather, in populations with overlapping generations, the amount of temporal allele frequency change is dependent on the age-specific survival and birth rates. Taking this phenomenon into account, we present an estimator for effective size that can be applied to populations with overlapping generations.


Author(s):  
Moritz A Ehrlich ◽  
Dominique N Wagner ◽  
Marjorie F Oleksiak ◽  
Douglas L Crawford

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.


2020 ◽  
Vol 60 (2) ◽  
pp. 318-331
Author(s):  
April D Garrett ◽  
Reid S Brennan ◽  
Anya L Steinhart ◽  
Aubrey M Pelletier ◽  
Melissa H Pespeni

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.


Genes ◽  
2020 ◽  
Vol 11 (4) ◽  
pp. 400 ◽  
Author(s):  
Alexandre Rêgo ◽  
Samridhi Chaturvedi ◽  
Amy Springer ◽  
Alexandra M. Lish ◽  
Caroline L. Barton ◽  
...  

Genes that affect adaptive traits have been identified, but our knowledge of the genetic basis of adaptation in a more general sense (across multiple traits) remains limited. We combined population-genomic analyses of evolve-and-resequence experiments, genome-wide association mapping of performance traits, and analyses of gene expression to fill this knowledge gap and shed light on the genomics of adaptation to a marginal host (lentil) by the seed beetle Callosobruchus maculatus. Using population-genomic approaches, we detected modest parallelism in allele frequency change across replicate lines during adaptation to lentil. Mapping populations derived from each lentil-adapted line revealed a polygenic basis for two host-specific performance traits (weight and development time), which had low to modest heritabilities. We found less evidence of parallelism in genotype-phenotype associations across these lines than in allele frequency changes during the experiments. Differential gene expression caused by differences in recent evolutionary history exceeded that caused by immediate rearing host. Together, the three genomic datasets suggest that genes affecting traits other than weight and development time are likely to be the main causes of parallel evolution and that detoxification genes (especially cytochrome P450s and beta-glucosidase) could be especially important for colonization of lentil by C. maculatus.


2021 ◽  
Vol 288 (1961) ◽  
Author(s):  
John K. Kelly

Selection component analyses (SCA) relate individual genotype to fitness components such as viability, fecundity and mating success. SCA are based on population genetic models and yield selection estimates directly in terms of predicted allele frequency change. This paper explores the statistical properties of gSCA: experiments that apply SCA to genome-wide scoring of SNPs in field sampled individuals. Computer simulations indicate that gSCA involving a few thousand genotyped samples can detect allele frequency changes of the magnitude that has been documented in field experiments on diverse taxa. To detect selection, imprecise genotyping from low-level sequencing of large samples of individuals provides much greater power than precise genotyping of smaller samples. The simulations also demonstrate the efficacy of ‘haplotype matching’, a method to combine information from a limited collection of whole genome sequence (the reference panel) with the much larger sample of field individuals that are measured for fitness. Pooled sequencing is demonstrated as another way to increase statistical power. Finally, I discuss the interpretation of selection estimates in relation to the Beavis effect, the overestimation of selection intensities at significant loci.


Genetics ◽  
1983 ◽  
Vol 104 (3) ◽  
pp. 531-548
Author(s):  
Edward Pollak

ABSTRACT A new procedure is proposed for estimating the effective population size, given that information is available on changes in frequencies of the alleles at one or more independently segregating loci and the population is observed at two or more separate times. Approximate expressions are obtained for the variances of the new statistic, as well as others, also based on allele frequency changes, that have been discussed in the literature. This analysis indicates that the new statistic will generally have a smaller variance than the others. Estimates of effective population sizes and of the standard errors of the estimates are computed for data on two fly populations that have been discussed in earlier papers. In both cases, there is evidence that the effective population size is very much smaller than the minimum census size of the population.


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