scholarly journals Predicting evolutionary change at the DNA level in a natural Mimulus population

2020 ◽  
Author(s):  
Patrick J. Monnahan ◽  
Jack Colicchio ◽  
Lila Fishman ◽  
Stuart J. Macdonald ◽  
John K. Kelly
Keyword(s):  
Natural Selection ◽  
Reproductive Success ◽  
Allele Frequency ◽  
Population Genetic ◽  
Evolutionary Change ◽  
Genetic Models ◽  
Next Generation ◽  
Fitness Components ◽  
Trade Offs ◽  
Frequency Changes

AbstractEvolution by natural selection occurs when the frequencies of genetic variants change because individuals differ in Darwinian fitness components such as survival or reproductive success. Differential fitness has been demonstrated in field studies of many organisms, but our ability to quantitatively predict allele frequency changes from fitness measurements remains unclear. Here, we characterize natural selection on millions of Single Nucleotide Polymorphisms (SNPs) across the genome of the annual plant Mimulus guttatus. We use fitness estimates to calibrate population genetic models that effectively predict observed allele frequency changes into the next generation. Hundreds of SNPs experienced “male selection” in 2013 with one allele at each SNP elevated in frequency among successful male gametes relative to the entire population of adults. In the following generation, allele frequencies at these SNPs consistently shifted in the predicted direction. A second year of study revealed that SNPs had effects on both viability and reproductive success with pervasive trade-offs between fitness components. SNPs favored by male selection were, on average, detrimental to survival. These trade-offs (antagonistic pleiotropy and temporal fluctuations in fitness) may be essential to the long-term maintenance of alleles undergoing substantial changes from generation to generation. Despite the challenges of measuring selection in the wild, the strong correlation between predicted and observed allele frequency changes suggests that population genetic models have a much greater role to play in forward-time prediction of evolutionary change.Author summaryFor the last 100 years, population geneticists have been deriving equations for Δp, the change in allele frequency owing to mutation, selection, migration, and genetic drift. Seldom are these equations used directly, to match a prediction for Δp to an observation of Δp. Here, we apply genomic sequencing technologies to samples from natural populations, obtaining millions of observations of Δp. We estimate natural selection on SNPs in a natural population of yellow monkeyflowers and find extensive evidence for selection through differential male success. We use the SNP-specific fitness estimates to calibrate a population genetic model that predicts observed Δp into the next generation. We find that when male selection favored one nucleotide at a SNP, that nucleotide increased in frequency in the next generation. Since neither observed nor predicted Δp are generally large in magnitude, we developed a novel method called “haplotype matching” to improve prediction accuracy. The method leverages intensive whole genome sequencing of a reference panel (187 individuals) to infer sequence-specific selection in thousands of field individuals sequenced at much lower coverage. This method proved essential to accurately predicting Δp in this experiment and further development may facilitate population genetic prediction more generally.

scholarly journals Predicting evolutionary change at the DNA level in a natural Mimulus population

PLoS Genetics ◽  
2021 ◽  
Vol 17 (1) ◽  
pp. e1008945
Author(s):  
Patrick J. Monnahan ◽  
Jack Colicchio ◽  
Lila Fishman ◽  
Stuart J. Macdonald ◽  
John K. Kelly
Keyword(s):  
Natural Selection ◽  
Reproductive Success ◽  
Allele Frequency ◽  
Population Genetic ◽  
Evolutionary Change ◽  
Genetic Models ◽  
Fitness Components ◽  
Male Gametes ◽  
Trade Offs ◽  
Frequency Changes

Evolution by natural selection occurs when the frequencies of genetic variants change because individuals differ in Darwinian fitness components such as survival or reproductive success. Differential fitness has been demonstrated in field studies of many organisms, but it remains unclear how well we can quantitatively predict allele frequency changes from fitness measurements. Here, we characterize natural selection on millions of Single Nucleotide Polymorphisms (SNPs) across the genome of the annual plant Mimulus guttatus. We use fitness estimates to calibrate population genetic models that effectively predict allele frequency changes into the next generation. Hundreds of SNPs experienced “male selection” in 2013 with one allele at each SNP elevated in frequency among successful male gametes relative to the entire population of adults. In the following generation, allele frequencies at these SNPs consistently shifted in the predicted direction. A second year of study revealed that SNPs had effects on both viability and reproductive success with pervasive trade-offs between fitness components. SNPs favored by male selection were, on average, detrimental to survival. These trade-offs (antagonistic pleiotropy and temporal fluctuations in fitness) may be essential to the long-term maintenance of alleles. Despite the challenges of measuring selection in the wild, the strong correlation between predicted and observed allele frequency changes suggests that population genetic models have a much greater role to play in forward-time prediction of evolutionary change.

scholarly journals Population genetic models of genomic imprinting.

Genetics ◽  
1992 ◽  
Vol 130 (4) ◽  
pp. 899-907 ◽  
Author(s):  
G P Pearce ◽  
H G Spencer
Keyword(s):  
Allele Frequency ◽  
Genomic Imprinting ◽  
Population Genetic ◽  
Sex Chromosome ◽  
Genetic Models ◽  
Chromosome Inactivation ◽  
Heterozygote Advantage ◽  
Males And Females ◽  
Frequency Changes ◽  
Parameter Values

Abstract The phenomenon of genomic imprinting has recently excited much interest among experimental biologists. The population genetic consequences of imprinting, however, have remained largely unexplored. Several population genetic models are presented and the following conclusions drawn: (i) systems with genomic imprinting need not behave similarly to otherwise identical systems without imprinting; (ii) nevertheless, many of the models investigated can be shown to be formally equivalent to models without imprinting; (iii) consequently, imprinting often cannot be discovered by following allele frequency changes or examining equilibrium values; (iv) the formal equivalences fail to preserve some well known properties. For example, for populations incorporating genomic imprinting, parameter values exist that cause these populations to behave like populations without imprinting, but with heterozygote advantage, even though no such advantage is present in these imprinting populations. We call this last phenomenon "pseudoheterosis." The imprinting systems that fail to be formally equivalent to nonimprinting systems are those in which males and females are not equivalent, i.e., two-sex viability systems and sex-chromosome inactivation.

scholarly journals Using seasonal genomic changes to understand historical adaptation: parallel selection on stickleback in highly-variable estuaries

2020 ◽  
Author(s):  
Alan Garcia-Elfring ◽  
Antoine Paccard ◽  
Timothy J. Thurman ◽  
Ben A. Wasserman ◽  
Eric P. Palkovacs ◽  
...  
Keyword(s):  
Natural Selection ◽  
Allele Frequency ◽  
Calcium Binding ◽  
Gasterosteus Aculeatus ◽  
Environmental Changes ◽  
Threespine Stickleback ◽  
Functional Enrichment ◽  
Genomic Changes ◽  
Parallel Selection ◽  
Frequency Changes

AbstractParallel evolution is considered strong evidence for natural selection. However, few studies have investigated the process of parallel selection as it plays out in real time. The common approach is to study historical signatures of selection in populations already well adapted to different environments. Here, to document selection in action under natural conditions, we study six populations of threespine stickleback (Gasterosteus aculeatus) inhabiting bar-built estuaries that undergo seasonal cycles of environmental changes. Estuaries are periodically isolated from the ocean due to sandbar formation during dry summer months, with concurrent environmental shifts that resemble the long-term changes associated with postglacial colonization of freshwater habitats by marine populations. We used pooled whole-genome sequencing (Pool-WGS) to track seasonal allele frequency changes in these populations and search for signatures of natural selection. We found consistent changes in allele frequency across estuaries, suggesting a potential role for parallel selection. Functional enrichment among candidate genes included transmembrane ion transport and calcium binding, which are important for osmoregulation and ion balance. The genomic changes that occur in threespine stickleback from bar-built estuaries could provide a glimpse into the early stages of adaptation that have occurred in many historical marine to freshwater transitions.

scholarly journals Allele frequency dynamics in a pedigreed natural population

2018 ◽  
Vol 116 (6) ◽  
pp. 2158-2164 ◽  
Author(s):  
Nancy Chen ◽  
Ivan Juric ◽  
Elissa J. Cosgrove ◽  
Reed Bowman ◽  
John W. Fitzpatrick ◽  
...  
Keyword(s):  
Gene Flow ◽  
Reproductive Success ◽  
Allele Frequency ◽  
Natural Population ◽  
Allele Frequencies ◽  
Frequency Change ◽  
Short Term ◽  
Individual Survival ◽  
Frequency Changes ◽  
Genetic Contributions

A central goal of population genetics is to understand how genetic drift, natural selection, and gene flow shape allele frequencies through time. However, the actual processes underlying these changes—variation in individual survival, reproductive success, and movement—are often difficult to quantify. Fully understanding these processes requires the population pedigree, the set of relationships among all individuals in the population through time. Here, we use extensive pedigree and genomic information from a long-studied natural population of Florida Scrub-Jays (Aphelocoma coerulescens) to directly characterize the relative roles of different evolutionary processes in shaping patterns of genetic variation through time. We performed gene dropping simulations to estimate individual genetic contributions to the population and model drift on the known pedigree. We found that observed allele frequency changes are generally well predicted by accounting for the different genetic contributions of founders. Our results show that the genetic contribution of recent immigrants is substantial, with some large allele frequency shifts that otherwise may have been attributed to selection actually due to gene flow. We identified a few SNPs under directional short-term selection after appropriately accounting for gene flow. Using models that account for changes in population size, we partitioned the proportion of variance in allele frequency change through time. Observed allele frequency changes are primarily due to variation in survival and reproductive success, with gene flow making a smaller contribution. This study provides one of the most complete descriptions of short-term evolutionary change in allele frequencies in a natural population to date.

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 Within-Generation Polygenic Selection Shapes Fitness-Related Traits across Environments in Juvenile Sea Bream

Genes ◽  
2020 ◽  
Vol 11 (4) ◽  
pp. 398 ◽  
Author(s):  
Carine Rey ◽  
Audrey Darnaude ◽  
Franck Ferraton ◽  
Bruno Guinand ◽  
François Bonhomme ◽  
...  
Keyword(s):  
Allele Frequency ◽  
Evolutionary Biology ◽  
Larval Settlement ◽  
Habitat Type ◽  
Sea Bream ◽  
Relative Role ◽  
Growth Strategies ◽  
Trade Offs ◽  
Local Selection ◽  
Frequency Changes

Understanding the genetic underpinnings of fitness trade-offs across spatially variable environments remains a major challenge in evolutionary biology. In Mediterranean gilthead sea bream, first-year juveniles use various marine and brackish lagoon nursery habitats characterized by a trade-off between food availability and environmental disturbance. Phenotypic differences among juveniles foraging in different habitats rapidly appear after larval settlement, but the relative role of local selection and plasticity in phenotypic variation remains unclear. Here, we combine phenotypic and genetic data to address this question. We first report correlations of opposite signs between growth and condition depending on juvenile habitat type. Then, we use single nucleotide polymorphism (SNP) data obtained by Restriction Associated DNA (RAD) sequencing to search for allele frequency changes caused by a single generation of spatially varying selection between habitats. We found evidence for moderate selection operating at multiple loci showing subtle allele frequency shifts between groups of marine and brackish juveniles. We identified subsets of candidate outlier SNPs that, in interaction with habitat type, additively explain up to 3.8% of the variance in juvenile growth and 8.7% in juvenile condition; these SNPs also explained significant fraction of growth rate in an independent larval sample. Our results indicate that selective mortality across environments during early-life stages involves complex trade-offs between alternative growth strategies.

scholarly journals Allele frequency dynamics in a pedigreed natural population

2018 ◽  
Author(s):  
Nancy Chen ◽  
Ivan Juric ◽  
Elissa J. Cosgrove ◽  
Reed Bowman ◽  
John W. Fitzpatrick ◽  
...  
Keyword(s):  
Gene Flow ◽  
Reproductive Success ◽  
Allele Frequency ◽  
Natural Population ◽  
Allele Frequencies ◽  
Frequency Change ◽  
Short Term ◽  
Individual Survival ◽  
Frequency Changes ◽  
Genetic Contributions

ABSTRACTA central goal of population genetics is to understand how genetic drift, natural selection, and gene flow shape allele frequencies through time. However, the actual processes underlying these changes - variation in individual survival, reproductive success, and movement - are often difficult to quantify. Fully understanding these processes requires the population pedigree, the set of relationships among all individuals in the population through time. Here, we use extensive pedigree and genomic information from a long-studied natural population of Florida Scrub-Jays (Aphelocoma coerulescens) to directly characterize the relative roles of different evolutionary processes in shaping patterns of genetic variation through time. We performed gene dropping simulations to estimate individual genetic contributions to the population and model drift on the known pedigree. We found that observed allele frequency changes are generally well predicted by accounting for the different genetic contributions of founders. Our results show that the genetic contribution of recent immigrants is substantial, with some large allele frequency shifts that otherwise may have been attributed to selection actually due to gene flow. We identified a few SNPs under directional short-term selection after appropriately accounting for gene flow. Using models that account for changes in population size, we partitioned the proportion of variance in allele frequency change through time. Observed allele frequency changes are primarily due to variation in survival and reproductive success, with gene flow making a smaller contribution. This study provides one of the most complete descriptions of short-term evolutionary change in allele frequencies in a natural population to date.

Sign in / Sign up

Export Citation Format

Share Document