Temporal Changes In Allele Frequencies Research Articles

Temporal allele frequency changes in large-effect loci reveal potential fishing impacts on salmon life-history diversity.

Fishing has the potential to influence the life-history traits of exploited populations. However, our understanding of how fisheries can induce evolutionary genetic changes remains incomplete. The discovery of large-effect loci linked with ecologically important life-history traits, such as age at maturity in Atlantic salmon (Salmo salar), provides an opportunity to study the impacts of temporally varying fishing pressures on these traits. A 93-year archive of fish scales from wild Atlantic salmon catches from the northern Baltic Sea region allowed us to monitor variation in adaptive genetic diversity linked with age at maturity of wild Atlantic salmon populations. The dataset consisted of samples from both commercial and recreational fisheries that target salmon on their spawning migration. Using a genotyping-by-sequencing approach (GT-seq), we discovered strong within-season allele frequency changes at the vgll3 locus linked with Atlantic salmon age at maturity: fishing in the early season preferentially targeted the vgll3 variant linked with older maturation. We also found within-season temporal variation in catch proportions of different wild Atlantic salmon subpopulations. Therefore, selective pressures of harvesting may vary depending on the seasonal timing of fishing, which has the potential to cause evolutionary changes in key life-history traits and their diversity. This knowledge can be used to guide fisheries management to reduce the effects of fishing practices on salmon life-history diversity. Thus, this study provides a tangible example of using genomic approaches to infer, monitor and help mitigate human impacts on adaptively important genetic variation in nature.

Estimating Temporally Variable Selection Intensity from Ancient DNA Data.

Novel technologies for recovering DNA information from archaeological and historical specimens have made available an ever-increasing amount of temporally spaced genetic samples from natural populations. These genetic time series permit the direct assessment of patterns of temporal changes in allele frequencies and hold the promise of improving power for the inference of selection. Increased time resolution can further facilitate testing hypotheses regarding the drivers of past selection events such as the incidence of plant and animal domestication. However, studying past selection processes through ancient DNA (aDNA) still involves considerable obstacles such as postmortem damage, high fragmentation, low coverage, and small samples. To circumvent these challenges, we introduce a novel Bayesian framework for the inference of temporally variable selection based on genotype likelihoods instead of allele frequencies, thereby enabling us to model sample uncertainties resulting from the damage and fragmentation of aDNA molecules. Also, our approach permits the reconstruction of the underlying allele frequency trajectories of the population through time, which allows for a better understanding of the drivers of selection. We evaluate its performance through extensive simulations and demonstrate its utility with an application to the ancient horse samples genotyped at the loci for coat coloration. Our results reveal that incorporating sample uncertainties can further improve the inference of selection.

MLNe: Simulating and estimating effective size and migration rate from temporal changes in allele frequencies.

In studies of molecular ecology, conservation biology, and evolutionary biology, the current or recent effective size (Ne) of a population is frequently estimated from the marker genotype data of two or more temporally spaced samples of individuals taken from the population. Despite the developments of numerous Bayesian, likelihood, and moment estimators, only a couple of them can use both temporally and spatially spaced samples of individuals to estimate jointly the effective size (Ne) of and the migration rate (m) into a population. In this note, I describe new implementations of these joint estimators of Ne and m in software MLNe which runs on multiple platforms (Windows, Mac, Linux) with or without a graphical user interface (GUI), and has an integrated simulation module to simulate genotype data for investigating the impacts of various factors (such as sample size and sampling interval) on estimation precision and accuracy, exploits both message passing interface (MPI) and openMP for parallel computations using multiple cores and nodes to speed up analysis. The program does not require data pre-processing and accepts multiple formats of a file of original genotype data and a file of parameters as input. The GUI facilitates data and parameter inputs and produces publication-quality output graphs, while the non-GUI version of software is convenient for batch analysis of multiple datasets as in simulations. MLNe will help advance the analysis of temporal genetic marker data for estimating Ne of and m between populations, which are important parameters that will help biologists for the conservation management of natural and managed populations. MLNe can be downloaded free from the website http://www.zsl.org/science/research/software/.

Genomic inference of contemporary effective population size in a large island population of collared flycatchers (Ficedula albicollis).

Due to its central importance to many aspects of evolutionary biology and population genetics, the long-term effective population size (Ne ) has been estimated for numerous species and populations. However, estimating contemporary Ne is difficult and in practice this parameter is often unknown. In principle, contemporary Ne can be estimated using either analyses of temporal changes in allele frequencies, or the extent of linkage disequilibrium (LD) between unlinked markers. We applied these approaches to estimate contemporary Ne of a relatively recently founded island population of collared flycatchers (Ficedula albicollis). We sequenced the genomes of 85 birds sampled in 1993 and 2015, and applied several temporal methods to estimate Ne at a few thousand (4000-7000). The approach based on LD provided higher estimates of Ne (20,000-32,000) and was associated with high variance, often resulting in infinite Ne . We conclude that whole-genome sequencing data offers new possibilities to estimate high (>1000) contemporary Ne , but also note that such estimates remain challenging, in particular for LD-based methods for contemporary Ne estimation.

Estimating the genome-wide contribution of selection to temporal allele frequency change

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.

Genes acting in synapses and neuron projections are early targets of selection during urban colonization.

When a species colonizes an urban habitat, differences in the environment can create novel selection pressures. Successful colonization will further lead to demographic perturbations and genetic drift, which can interfere with selection. Here, we test for consistent urban selection signals in multiple populations of the burrowing owl (Athene cunicularia), a species that colonized South American cities just a few decades ago. We sequenced 213 owls from three urban-rural population pairs and performed a genome-wide comparison of urban against rural birds. We further studied genome-wide associations with flight initiation distance, a measure of harm avoidance in which urban and rural birds are known to differ. Based on four samples taken over nine years from one of the urban populations, we investigated temporal allele frequency changes. The genomic data were also used to identify urban-specific signatures of selective sweeps. Single genomic sites did not reach genome-wide significance for any association. However, a gene-set analysis on the strongest signals from these four selection scans suggests a significant enrichment of genes with known functions related to synapses and neuron projections. We identified 98 genes predominantly expressed in the brain, of which many may play a role in the modulation of brain connectivity and consequently in cognitive function and motivational behaviour during urbanization. Furthermore, polymorphisms in the promoter region of the synaptic SERT gene - one of the two candidates known to correlate with urban colonization in birds - associated with the habitat in which individuals lived (urban vs. rural).

Adaptive dynamics of cuticular hydrocarbons in Drosophila.

Cuticular hydrocarbons (CHCs) are hydrophobic compounds deposited on the arthropod cuticle that are of functional significance with respect to stress tolerance, social interactions and mating dynamics. We characterized CHC profiles in natural populations of Drosophila melanogaster at five levels: across a latitudinal transect in the eastern United States, as a function of developmental temperature during culture, across seasonal time in replicate years, and as a function of rapid evolution in experimental mesocosms in the field. Furthermore, we also characterized spatial and temporal changes in allele frequencies for SNPs in genes that are associated with the production and chemical profile of CHCs. Our data demonstrate a striking degree of parallelism for clinal and seasonal variation in CHCs in this taxon; CHC profiles also demonstrate significant plasticity in response to rearing temperature, and the observed patterns of plasticity parallel the spatiotemporal patterns observed in nature. We find that these congruent shifts in CHC profiles across time and space are also mirrored by predictable shifts in allele frequencies at SNPs associated with CHC chain length. Finally, we observed rapid and predictable evolution of CHC profiles in experimental mesocosms in the field. Together, these data strongly suggest that CHC profiles respond rapidly and adaptively to environmental parameters that covary with latitude and season, and that this response reflects the process of local adaptation in natural populations of D.melanogaster.

Temporal changes in allele frequencies in a small marble trout Salmo marmoratus population threatened by extreme flood events.

The effect of extreme floods on the genetic composition of marble trout Salmo marmoratus living in Lipovscek, a tributary of the Soca River in Slovenia, which has been affected by multiple destructive flood events for centuries was investigated. By monitoring genetic variability during the period 2004-2011, apparent signatures of genetic erosion including a decline in observed and expected heterozygosities and allelic richness were observed. Contemporary effective population size was estimated between 11 and 55 individuals, which is congruent with census data. The data suggest asymmetric gene flow between the two sections of the river. The existence of substantial downstream migration (15-19%) was confirmed by paternity analysis. A small (1-3%) upstream migration was also suggested, which was confirmed by tagging data. Overall, low genetic diversity has not prevented the survival of the Lipovscek population, which might be a common feature of salmonid freshwater populations.

Temporal genetic dynamics among mosquitofish (Gambusia holbrooki) populations in invaded watersheds

The temporal components of genetic diversity and geographical structure of invasive mosquitofish populations are poorly known. Through the genetic monitoring of four consecutive cohorts of Gambusia holbrooki from three different river basins we aimed to determine temporal patterns of regional genetic variation and dispersal rates within invasive populations. Despite showing evidence of strong population size fluctuations, genetic diversity levels were maintained among local cohorts. We only detected temporal allele frequency changes associated with seasonal flooding that did not modify major trends on population structure among cohorts. Downstream gene flow coupled with increased connectivity at lowland locations to increase genetic diversity levels in these areas. A large proportion of local fish (up to 50 %) were dispersers, often originated from locations within the same river basin. High dispersal capability, ecological tolerance, and reproductive traits likely promote river colonization. Finally, our results also confirmed that human-assisted translocations promote within and among basin gene flow and maintained levels of genetic diversity, particularly in upstream locations.

Samples from subdivided populations yield biased estimates of effective size that overestimate the rate of loss of genetic variation.

Many empirical studies estimating effective population size apply the temporal method that provides an estimate of the variance effective size through the amount of temporal allele frequency change under the assumption that the study population is completely isolated. This assumption is frequently violated, and the magnitude of the resulting bias is generally unknown. We studied how gene flow affects estimates of effective size obtained by the temporal method when sampling from a population system and provide analytical expressions for the expected estimate under an island model of migration. We show that the temporal method tends to systematically underestimate both local and global effective size when populations are connected by gene flow, and the bias is sometimes dramatic. The problem is particularly likely to occur when sampling from a subdivided population where high levels of gene flow obscure identification of subpopulation boundaries. In such situations, sampling in a manner that prevents biased estimates can be difficult. This phenomenon might partially explain the frequently reported unexpectedly low effective population sizes of marine populations that have raised concern regarding the genetic vulnerability of even exceptionally large populations.

Short-Term Genetic Changes: Evaluating Effective Population Size Estimates in a Comprehensively Described Brown Trout (Salmo trutta) Population

The effective population size (N(e)) is notoriously difficult to accurately estimate in wild populations as it is influenced by a number of parameters that are difficult to delineate in natural systems. The different methods that are used to estimate N(e) are affected variously by different processes at the population level, such as the life-history characteristics of the organism, gene flow, and population substructure, as well as by the frequency patterns of genetic markers used and the sampling design. Here, we compare N(e) estimates obtained by different genetic methods and from demographic data and elucidate how the estimates are affected by various factors in an exhaustively sampled and comprehensively described natural brown trout (Salmo trutta) system. In general, the methods yielded rather congruent estimates, and we ascribe that to the adequate genotyping and exhaustive sampling. Effects of violating the assumptions of the different methods were nevertheless apparent. In accordance with theoretical studies, skewed allele frequencies would underestimate temporal allele frequency changes and thereby upwardly bias N(e) if not accounted for. Overlapping generations and iteroparity would also upwardly bias N(e) when applied to temporal samples taken over short time spans. Gene flow from a genetically not very dissimilar source population decreases temporal allele frequency changes and thereby acts to increase estimates of N(e). Our study reiterates the importance of adequate sampling, quantification of life-history parameters and gene flow, and incorporating these data into the N(e) estimation.

Testing metapopulation dynamics using genetic, demographic and ecological data

The metapopulation concept is a cornerstone in the recent history of ecology and evolution. However, determining whether a natural system fits a metapopulation model is a complex issue. Extinction-colonization dynamics are indeed often difficult to quantify because species detectability is not always 100%, resulting in an imperfect record of extinctions. Here, we explore whether combining population genetics with demographic and ecological surveys can yield more realistic estimates of metapopulation dynamics. We apply this approach to the freshwater snail Drepanotrema depressissimum in a fragmented landscape of tropical ponds. In addition to studying correlations between genetic diversity and demographical or ecological characteristics, we undertake, for the first time, a detailed search for genetic signatures of extinction-recolonization events using temporal changes in allele frequencies within sites. Surprisingly, genetic data indicate that extinction is much rarer than suggested by demographic surveys. Consequently, this system is better described as a set of populations with different sizes and immigration rates than as a true metapopulation. We identify several cases of apparent extinction owing to nondetection of low-density populations, and of aestivating individuals in desiccated ponds. More generally, we observed a frequent mismatch between genetic and demographical/ecological information at small spatial and temporal scales. We discuss the causes of these discrepancies and show how these two types of data provide complementary information on population dynamics and history, especially when temporal genetic samples are available.

USING ISOLATION BY DISTANCE AND EFFECTIVE DENSITY TO ESTIMATE DISPERSAL SCALES IN ANEMONEFISH

Robust estimates of dispersal are critical for understanding population dynamics and local adaptation, as well as for successful spatial management. Genetic isolation by distance patterns hold clues to dispersal, but understanding these patterns quantitatively has been complicated by uncertainty in effective density. In this study, we genotyped populations of a coral reef fish (Amphiprion clarkii) at 13 microsatellite loci to uncover fine-scale isolation by distance patterns in two replicate transects. Temporal changes in allele frequencies between generations suggested that effective densities in these populations are 4-21 adults/km. A separate estimate from census densities suggested that effective densities may be as high as 82-178 adults/km. Applying these effective densities with isolation by distance theory suggested that larval dispersal kernels in A. clarkii had a spread near 11 km (4-27 km). These kernels predicted low fractions of self-recruitment in continuous habitats, but the same kernels were consistent with previously reported, high self-recruitment fractions (40-60%) when realistic levels of habitat patchiness were considered. Our results suggested that ecologically relevant larval dispersal can be estimated with widely available genetic methods when effective density is measured carefully through cohort sampling and ecological censuses, and that self-recruitment studies should be interpreted in light of habitat patchiness.

Testing temporal changes in allele frequencies: a simulation approach

Analysis of the temporal variation in allele frequencies is useful for studying microevolutionary processes. However, many statistical methods routinely used to test temporal changes in allele frequencies fail to establish a proper hypothesis or have theoretical or practical limitations. Here, a Bayesian statistical test is proposed in which the distribution of the distances among sampling frequencies is approached with computer simulations, and hypergeometric sampling is considered instead of binomial sampling. To validate the test and compare its performance with other tests, agent-based model simulations were run for a variety of scenarios, and two real molecular databases were analysed. The results showed that the simulation test (ST) maintained the significance value used (α=0·05) for a vast combination of parameter values, whereas other tests were sensitive to the effect of genetic drift or binomial sampling. The differences between binomial and hypergeometric sampling were more complex than expected, and a novel effect was described. This study suggests that the ST is especially useful for studies with small populations and many alleles, as in microsatellite or sequencing molecular data.

Survival of the endangered butterfly Lycaena helle in a fragmented environment: Genetic analyses over 15 years

Temporal changes in allele frequencies are often assumed in studies addressing the history of populations affected by different anthropogenic and natural impacts at different time scales. Yet, few studies directly compare the genetic composition of populations over time spans of more than 10 years. Therefore, to test the genetic effects of 15 years of population isolation in the butterfly Lycaena helle, we analysed 472 individuals from 27 samples, of which nine were collected in 1991 and 18 in 2006. Sampling was performed in five mountain regions (Pyrenees, Massif Central, Jura, Vosges and Ardennes). Genetic analyses were performed using five polymorphic microsatellites. Old and new samples of identical or neighbouring populations revealed similar genetic differentiations among these five mountain regions. A comparatively strong genetic differentiation among populations combined with a high amount of private alleles for each mountain area was detected, but mountain-specific alleles were in most cases identical in 1991 and 2006. Nevertheless, the obtained data also indicate moderate changes between 1991 and 2006 in the species genetic structure – genetic differentiation among local populations increased marginally and allele frequencies showed corresponding modifications. A significant decline in genetic diversity was not detectable, and nine private alleles exclusive to a single mountain region were only detected in samples from the year 1991, whereas eleven were only observed in the individuals collected in 2006. These observations might indicate the results of genetic drift within isolated populations.

MHC class II DQA gene variation across cohorts of brown hares ( Lepus europaeus) from eastern Austria: Testing for different selection hypotheses

We have studied the temporal variation (1999–2007) in the MHC class II DQA gene and 8 microsatellites across 8 cohorts in a population of brown hare ( Lepus europaeus) from eastern Austria. Our results show no significant temporal changes in allele frequencies both in microsatellites and the DQA gene. Although positive selection on a larger evolutionary time scale has occurred in DQA, we have not observed evidence of contemporary balancing selection in this gene. Our results are not compatible with the negative frequency-dependent selection or the variable selection in time hypotheses within a timeframe of 8 consecutive generations. However, selection heterogeneity in space occurs. The studied cohorts have probably not been exposed to strong effects of parasites and pathogens during the period of this study, as indicated by our endoparasite counts and infection data. Furthermore, the most common DQA allele ( Leeu-DQA*06) was found to be in a stable frequency equilibrium which is consistent with the occurrence of stabilizing selection. This could indicate that major selective agents have been rather constant in their frequency across our temporal samples.

Genetic effective size, Ne, tracks density in a small freshwater cyprinid, Pecos bluntnose shiner (Notropis simus pecosensis)

Genetic monitoring tracks changes in measures of diversity including allelic richness, heterozygosity and genetic effective size over time, and has emerged as an important tool for understanding evolutionary consequences of population management. One proposed application of genetic monitoring has been to estimate abundance and its trajectory through time. Here, genetic monitoring was conducted across five consecutive year for the Pecos bluntnose shiner, a federally threatened minnow. Temporal changes in allele frequencies at seven microsatellite DNA loci were used to estimate variance effective size (N(eV)) across adjacent years in the time series. Likewise, effective size was computed using the linkage disequilibrium method (N(eD)) for each sample. Estimates of N(e) were then compared to estimates of adult fish density obtained from traditional demographic monitoring. For Pecos bluntnose shiner, density (catch-per-unit-effort), N(eV) and N(eD) were positively associated across this time series. Results for Pecos bluntnose shiner were compared to a related and ecologically similar species, the Rio Grande silvery minnow. In this species, density and N(eV) were negatively associated, which suggested decoupling of abundance and effective size trajectories. Conversely, density and N(eD) were positively associated. For Rio Grande silvery minnow, discrepancies among estimates of N(e) and their relationships with adult fish density could be related to effects of high variance in reproductive success in the wild and/or effects of supplementation of the wild population with captive-bred and reared fish. The efficacy of N(e) as a predictor of density and abundance may depend on intrinsic population dynamics of the species and how these dynamics are influenced by the landscape features, management protocols and other factors.

Widespread selective sweeps affecting microsatellites in Drosophila populations adapting to captivity: Implications for captive breeding programs

Many threatened species are being maintained in captivity to save them from extinction, often with the eventual aim of reintroduction. The objective of genetic management in captivity is to ‘freeze’ evolution i.e. to avoid genetic adaptation to captivity and to retain genetic diversity. Most current genetic management of threatened species addresses the latter, but does not explicitly address the former. The theory underlying current genetic management and its practical implementation assumes neutrality of loci. However, genetic adaptation in captive populations may cause non-neutral behavior at neutral loci due to selective sweeps (hitchhiking) caused by rapid allele frequency changes at linked fitness loci. We compared changes in microsatellite genetic diversity at eight non-coding loci with neutral predictions in 23 pedigreed captive populations of Drosophila melanogaster maintained with effective sizes of 25 (eight replicates), 50 (6), 100 (4), 250 (3) and 500 (2) for 48 generations. Loss of microsatellite heterozygosity was significantly faster (by 12%) than predicted by neutral theory, as assessed by regressing proportion of heterozygosity retained on pedigree inbreeding coefficients. Further, greater than neutral changes were observed for both variances in allele frequencies across replicates (by 25%), and for temporal changes in allele frequencies (by 33%). All eight microsatellite loci showed signals of selectively-driven changes. Rather than having their evolution ‘frozen’, captive populations are undergoing major genome-wide selective sweeps that affect not only fitness loci but linked neutral loci. Captive genetic management for threatened species destined for reintroduction requires modification to explicitly minimize genetic adaptation to captivity.

How Ebola Impacts Genetics of Western Lowland Gorilla Populations

BackgroundEmerging infectious diseases in wildlife are major threats for both human health and biodiversity conservation. Infectious diseases can have serious consequences for the genetic diversity of populations, which could enhance the species' extinction probability. The Ebola epizootic in western and central Africa induced more than 90% mortality in Western lowland gorilla population. Although mortality rates are very high, the impacts of Ebola on genetic diversity of Western lowland gorilla have never been assessed.Methodology/Principal FindingsWe carried out long term studies of three populations of Western lowland gorilla in the Republic of the Congo (Odzala-Kokoua National Park, Lossi gorilla sanctuary both affected by Ebola and Lossi's periphery not affected). Using 17 microsatellite loci, we compared genetic diversity and structure of the populations and estimate their effective size before and after Ebola outbreaks. Despite the effective size decline in both populations, we did not detect loss in genetic diversity after the epizootic. We revealed temporal changes in allele frequencies in the smallest population.Conclusions/SignificanceImmigration and short time elapsed since outbreaks could explain the conservation of genetic diversity after the demographic crash. Temporal changes in allele frequencies could not be explained by genetic drift or random sampling. Immigration from genetically differentiated populations and a non random mortality induced by Ebola, i.e., selective pressure and cost of sociality, are alternative hypotheses. Understanding the influence of Ebola on gorilla genetic dynamics is of paramount importance for human health, primate evolution and conservation biology.

Temporally stable genetic structure of heavily exploited Atlantic herring (Clupea harengus) in Swedish waters

Information on the temporal stability of genetic structures is important to permit detection of changes that can constitute threats to biological resources. Large-scale harvesting operations are known to potentially alter the composition and reduce the variability of populations, and Atlantic herring (Clupea harengus) has a long history of heavy exploitation. In the Baltic Sea and Skagerrak waters, the census population sizes have declined by 35-50% over the last three decades. We compared the genetic structure of Atlantic herring in these waters sampled at least two different times between 1979 and 2003 by assaying 11 allozyme and nine microsatellite loci. We cannot detect any changes in the amount of genetic variation or spatial structure, and differentiation is weak with overall F(ST)=0.003 among localities for the older samples and F(ST)=0.002 for the newer ones. There are indications of temporal allele frequency changes, particularly in one of five sampling localities that is reflected in a relatively small local N(e) estimate of c. 400. The previously identified influence of selection at the microsatellite locus Cpa112 remains stable over the 24-year period studied here. Despite little genetic differentiation, migration among localities appears small enough to permit demographic independence between populations.