scholarly journals Rapid genomic convergent evolution in experimental populations of Trinidadian guppies (Poecilia reticulata)

2021 ◽  
Author(s):  
Mijke J van der Zee ◽  
James R Whiting ◽  
Josephine R Paris ◽  
Ron D Bassar ◽  
Joseph Travis ◽  
...  

It is now accepted that phenotypic evolution can occur quickly but the genetic basis of rapid adaptation to natural environments is largely unknown in multicellular organisms. Population genomic studies of experimental populations of Trinidadian guppies (Poecilia reticulata) provide a unique opportunity to study this phenomenon. Guppy populations that were transplanted from high-predation (HP) to low-predation (LP) environments have been shown to mimic naturally-colonised LP populations phenotypically in as few as 8 generations. The new phenotypes persist in subsequent generations in lab environments, indicating their high heritability. Here, we compared whole genome variation in four populations recently introduced into LP sites along with the corresponding HP source population. We examined genome-wide patterns of genetic variation to estimate past demography, and uncovered signatures of selection with a combination of genome scans and a novel multivariate approach based on allele frequency change vectors. We were able to identify a limited number of candidate loci for convergent evolution across the genome. In particular, we found a region on chromosome 15 under strong selection in three of the four populations, with our multivariate approach revealing subtle parallel changes in allele frequency in all four populations across this region. Investigating patterns of genome-wide selection in this uniquely replicated experiment offers remarkable insight into the mechanisms underlying rapid adaptation, providing a basis for comparison with other species and populations experiencing rapidly changing environments.

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.


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.


eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Heather E Machado ◽  
Alan Bergland ◽  
Ryan W Taylor ◽  
Susanne Tilk ◽  
Emily Behrman ◽  
...  

To advance our understanding of adaptation to temporally varying selection pressures, we identified signatures of seasonal adaptation occurring in parallel among Drosophila melanogaster populations. Specifically, we estimated allele frequencies genome-wide from flies sampled early and late in the growing season from 20 widely dispersed populations. We identified parallel seasonal allele frequency shifts across North America and Europe, demonstrating that seasonal adaptation is a general phenomenon of temperate fly populations. Seasonally fluctuating polymorphisms are enriched in large chromosomal inversions and we find a broad concordance between seasonal and spatial allele frequency change. The direction of allele frequency change at seasonally variable polymorphisms can be predicted by weather conditions in the weeks prior to sampling, linking the environment and the genomic response to selection. Our results suggest that fluctuating selection is an important evolutionary force affecting patterns of genetic variation in Drosophila.


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.


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.


2017 ◽  
Vol 27 (1) ◽  
pp. 233-247 ◽  
Author(s):  
Jonathan Corbi ◽  
Eric J. Baack ◽  
Jennifer M. Dechaine ◽  
Gerald Seiler ◽  
John M. Burke

2018 ◽  
Author(s):  
Heather E. Machado ◽  
Alan O. Bergland ◽  
Ryan Taylor ◽  
Susanne Tilk ◽  
Emily Behrman ◽  
...  

AbstractTo advance our understanding of adaptation to temporally varying selection pressures, we identified signatures of seasonal adaptation occurring in parallel amongDrosophila melanogasterpopulations. To study these evolutionary dynamics, we estimated allele frequencies genome-wide from flies sampled early and late in the growing season from 20 widely dispersed populations. We identify parallel seasonal allele frequency shifts across North America and Europe, demonstrating that seasonal adaptation is a general phenomenon of temperate fly populations. The direction of allele frequency change at seasonally variable polymorphisms can be predicted by weather conditions in the weeks prior to sampling, linking the environment and the genomic response to selection. The extent of allele frequency fluctuations implies that seasonal evolution drives substantial (5-10%) allele frequency fluctuations at >1% of common polymorphisms across the genome. Our results suggest that fluctuating selection is an important evolutionary force affecting the extent and stability of linked and functional variation.


2021 ◽  
Author(s):  
Yoshinobu Uemoto ◽  
Kasumi Ichinoseki ◽  
Toshimi Matsumoto ◽  
Nozomi Oka ◽  
Hironori Takamori ◽  
...  

Abstract Background: The genetic improvement of disease resistance in pig has been well-received. Identification of a quantitative trait locus (QTL) related to a chronic respiratory disease such as Mycoplasmal pneumonia of swine (MPS) and immune-related traits is important for understanding the genomic background of disease resistance and to apply marker-assisted selection. The objective of this study was to understand the influence of genomic factors on respiratory disease and immune-related traits in MPS-selected pigs.Results: A total of 874 Landrace purebred pigs, which were selected based on MPS resistance, were genotyped using the Illumina PorcineSNP60 BeadChip, and were then used for genomic analyses. First, we performed genome-wide association studies (GWAS) to detect a novel QTL for a total of 22 performance, respiratory disease, and immune-related traits using additive and nonadditive genetic effects. Second, we evaluated the changes in allele frequency due to selection for MPS resistance and compared the putative selected regions with the detected QTL. GWAS detected a total of 11 genome-wide significant single nucleotide polymorphisms (SNPs) with an additive effect in five traits and a total of three significant SNPs with a nonadditive effect in three traits. Most of these detected QTL regions were novel regions with some candidate genes located in them. With regard to a pleiotropic region among traits, only five of these detected QTL regions overlapped among traits. Changes in allele frequencies at the many putative selected regions were spread across the whole genome and overlapped with the detected QTL. Some of these selected regions were the ones that contained the detected QTL for MPS score and other traits.Conclusion: These results suggest that a closed-line breeding population is a useful target population to refine and confirm QTL regions by integrating the results of GWAS and allele frequency changes. The study provides new insights into the genomic factors that affect respiratory disease and immune-related traits in pigs.


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