The genome-wide signature of short-term temporal selection.

Despite evolutionary biology's obsession with natural selection, few studies have evaluated multigenerational series of patterns of selection on a genome-wide scale in natural populations. Here, we report on a 10-y population-genomic survey of the microcrustacean Daphnia pulex. The genome sequences of [Formula: see text]800 isolates provide insights into patterns of selection that cannot be obtained from long-term molecular-evolution studies, including the following: the pervasiveness of near quasi-neutrality across the genome (mean net selection coefficients near zero, but with significant temporal variance about the mean, and little evidence of positive covariance of selection across time intervals); the preponderance of weak positive selection operating on minor alleles; and a genome-wide distribution of numerous small linkage islands of observable selection influencing levels of nucleotide diversity. These results suggest that interannual fluctuating selection is a major determinant of standing levels of variation in natural populations, challenge the conventional paradigm for interpreting patterns of nucleotide diversity and divergence, and motivate the need for the further development of theoretical expressions for the interpretation of population-genomic data.

Fluctuating selection and the determinants of genetic variation.

Recent studies of cosmopolitan Drosophila populations have found hundreds to thousands of genetic loci with seasonally fluctuating allele frequencies, bringing temporally fluctuating selection to the forefront of the historical debate surrounding the maintenance of genetic variation in natural populations. Numerous mechanisms have been explored in this longstanding area of research, but these exciting empirical findings have prompted several recent theoretical and experimental studies that seek to better understand the drivers, dynamics, and genome-wide influence of fluctuating selection. In this review, we evaluate the latest evidence for multilocus fluctuating selection in Drosophila and other taxa, highlighting the role of potential genetic and ecological mechanisms in maintaining these loci and their impacts on neutral genetic variation.

Fluctuating selection maintains distinct species phenotypes in an ecological community in the wild.

Species' phenotypic characteristics often remain unchanged over long stretches of geological time. Stabilizing selection-in which fitness is highest for intermediate phenotypes and lowest for the extremes-has been widely invoked as responsible for this pattern. At the community level, such stabilizing selection acting individually on co-occurring species is expected to produce a rugged fitness landscape on which different species occupy distinct fitness peaks. However, even with an explosion of microevolutionary field studies over the past four decades, evidence for persistent stabilizing selection driving long-term stasis is lacking. Nonetheless, biologists continue to invoke stabilizing selection as a major factor explaining macroevolutionary patterns. Here, by directly measuring natural selection in the wild, we identified a complex community-wide fitness surface in which four Anolis lizard species each occupy a distinct fitness peak close to their mean phenotype. The presence of local fitness optima within species, and fitness valleys between species, presents a barrier to adaptive evolutionary change and acts to maintain species differences through time. However, instead of continuously operating stabilizing selection, we found that species were maintained on these peaks by the combination of many independent periods among which selection fluctuated in form, strength, direction, or existence and in which stabilizing selection rarely occurred. Our results suggest that lack of substantial phenotypic evolutionary change through time may be the result of selection, but not persistent stabilizing selection as classically envisioned.

Evolutionary Insights from a Large-Scale Survey of Population-Genomic Variation.

The field of genomics has ushered in new methods for studying molecular-genetic variation in natural populations. However, most population-genomic studies still rely on small sample sizes (typically, <100 individuals) from single time points, leaving considerable uncertainties with respect to the behavior of relatively young (and rare) alleles and, owing to the large sampling variance of measures of variation, to the specific gene targets of unusually strong selection. Genomic sequences of ∼1,700 haplotypes distributed over a 10-year period from a natural population of the microcrustacean Daphnia pulex reveal evolutionary-genomic features at a refined scale, including previously hidden information on the behavior of rare alleles predicted by recent theory. Background selection, resulting from the recurrent introduction of deleterious alleles, appears to strongly influence the dynamics of neutral alleles, inducing indirect negative selection on rare variants and positive selection on common variants. Temporally fluctuating selection increases the persistence of nonsynonymous alleles with intermediate frequencies, while reducing standing levels of variation at linked silent sites. Combined with the results from an equally large metapopulation survey of the study species, classes of genes that are under strong positive selection can now be confidently identified in this key model organism. Most notable among rapidly evolving Daphnia genes are those associated with ribosomes, mitochondrial functions, sensory systems, and lifespan determination.

Effect of the Seed Bank on Evolutionary Rescue in Small Populations: Univariate and Multivariate Demogenetic Dynamics.

AbstractUnder global change, the impact of seed banks on evolutionary rescue is uncertain. They buffer plant populations from demographic and genetic stochasticity but extend generation time and can become a reservoir of maladapted alleles. We built analytical and individual-based models to predict the effect of seed banks on the persistence of small annual plant populations facing an abrupt or sustained directional change in uni- or multivariate trait optima. Demogenetic dynamics predict that under most scenarios seed banks increase the lag yet enhance persistence to 200-250 years by absorbing demographic losses. Simulations indicate that the seed bank has a minimal impact on the genetic skew, although we suggest that this result could depend on the fitness component under selection. Our multivariate model reveals that by enlarging and reshaping the G matrix, seed banks can diminish the impact of mutational correlation and even accelerate adaptation under antagonistic pleiotropy relative to populations without a bank. We illustrate how the magnitude of optimum fluctuations, type and degree of optimum change, selection strength, and vital rates are weights that tip the scales determining persistence. Finally, our work highlights that migration from the past is not maladaptative when optimum fluctuations are large enough to create stepping stones to the new optimum.

High parasite diversity maintained after an alga-virus coevolutionary arms race.

Arms race dynamics are a common outcome of host-parasite coevolution. While they can theoretically be maintained indefinitely, realistic arms races are expected to be finite. Once an arms race has ended, for example due to the evolution of a generalist-resistant host, the system may transition into coevolutionary dynamics that favour long-term diversity. In microbial experiments, host-parasite arms races often transition into a stable coexistence of generalist-resistant hosts, (semi-)susceptible hosts, and parasites. While long-term host diversity is implicit in these cases, parasite diversity is usually overlooked. In this study, we examined parasite diversity after the end of an experimental arms race between a unicellular alga (Chlorella variabilis) and its lytic virus (PBCV-1). First, we isolated virus genotypes from multiple time points from two replicate microcosms. A time-shift experiment confirmed that the virus isolates had escalating host ranges, i.e., that arms races had occurred. We then examined the phenotypic and genetic diversity of virus isolates from the post-arms race phase. Post-arms race virus isolates had diverse host ranges, survival probabilities, and growth rates; they also clustered into distinct genetic groups. Importantly, host range diversity was maintained throughout the post-arms race phase, and the frequency of host range phenotypes fluctuated over time. We hypothesize that this dynamic polymorphism was maintained by a combination of fluctuating selection and demographic stochasticity. Together with previous work in prokaryotic systems, our results link experimental observations of arms races to natural observations of long-term host and parasite diversity.

Early-life variation in migration is subject to strong fluctuating survival selection in a partially migratory bird.

Population dynamic and eco-evolutionary responses to environmental variation and change fundamentally depend on combinations of within- and among-cohort variation in the phenotypic expression of key life-history traits, and on corresponding variation in selection on those traits. Specifically, in partially migratory populations, spatio-seasonal dynamics depend on the degree of adaptive phenotypic expression of seasonal migration versus residence, where more individuals migrate when selection favours migration. Opportunity for adaptive (or, conversely, maladaptive) expression could be particularly substantial in early life, through the initial development of migration versus residence. However, within- and among-cohort dynamics of early-life migration, and of associated survival selection, have not been quantified in any system, preventing any inference on adaptive early-life expression. Such analyses have been precluded because data on seasonal movements and survival of sufficient young individuals, across multiple cohorts, have not been collected. We undertook extensive year-round field resightings of 9359 colour-ringed juvenile European shags Gulosus aristotelis from 11 successive cohorts in a partially migratory population. We fitted Bayesian multi-state capture-mark-recapture models to quantify early-life variation in migration versus residence and associated survival across short temporal occasions through each cohort's first year from fledging, thereby quantifying the degree of adaptive phenotypic expression of migration within and across years. All cohorts were substantially partially migratory, but the degree and timing of migration varied considerably within and among cohorts. Episodes of strong survival selection on migration versus residence occurred both on short timeframes within years, and cumulatively across entire first years, generating instances of instantaneous and cumulative net selection that would be obscured at coarser temporal resolutions. Further, the magnitude and direction of selection varied among years, generating strong fluctuating survival selection on early-life migration across cohorts, as rarely evidenced in nature. Yet, the degree of migration did not strongly covary with the direction of selection, indicating limited early-life adaptive phenotypic expression. These results reveal how dynamic early-life expression of and selection on a key life-history trait, seasonal migration, can emerge across seasonal, annual, and multi-year timeframes, yet be substantially decoupled. This restricts the potential for adaptive phenotypic, microevolutionary, and population dynamic responses to changing seasonal environments.

Heterogeneous selection on exploration behavior within and among West European populations of a passerine bird.

Heterogeneous selection is often proposed as a key mechanism maintaining repeatable behavioral variation ("animal personality") in wild populations. Previous studies largely focused on temporal variation in selection within single populations. The relative importance of spatial versus temporal variation remains unexplored, despite these processes having distinct effects on local adaptation. Using data from >3,500 great tits (Parus major) and 35 nest box plots situated within five West-European populations monitored over 4 to 18 y, we show that selection on exploration behavior varies primarily spatially, across populations, and study plots within populations. Exploration was, simultaneously, selectively neutral in the average population and year. These findings imply that spatial variation in selection may represent a primary mechanism maintaining animal personalities, likely promoting the evolution of local adaptation, phenotype-dependent dispersal, and nonrandom settlement. Selection also varied within populations among years, which may counteract local adaptation. Our study underlines the importance of combining multiple spatiotemporal scales in the study of behavioral adaptation.

Partial protection from fluctuating selection leads to evolution towards wider population size fluctuation and a novel mechanism of balancing selection.

When a population is partially protected from fluctuating selection, as when a seed bank is present, variance in fitness will be reduced and reproductive success of the population will be promoted. This study further investigates the effect of such a 'refuge' from fluctuating selection using a mathematical model that couples demographic and evolutionary dynamics. While alleles that cause smaller fluctuations in population density should be positively selected according to classical theoretic predictions, this study finds the opposite: alleles that increase the amplitude of population size fluctuation are positively selected if population density is weakly regulated. Under strong density regulation with a constant carrying capacity, long-term maintenance of polymorphism caused by the storage effect emerges. However, if the carrying capacity of the population is oscillating, mutant alleles whose fitness fluctuates in the same direction as population size are positively selected, eventually reaching fixation or intermediate frequencies that oscillate over time. This oscillatory polymorphism, which requires fitness fluctuations that can arise with simple trade-offs in life-history traits, is a novel form of balancing selection. These results highlight the importance of allowing joint demographic and population genetic changes in models, the failure of which prevents the discovery of novel eco-evolutionary dynamics.

Selective effects of a short transient environmental fluctuation on a natural population.

Natural populations experience continuous and often transient changes of environmental conditions. These in turn may result in fluctuating selection pressures leading to variable demographic and evolutionary population responses. Rapid adaptation as short-term response to a sudden environmental change has in several cases been attributed to polygenic traits, but the underlying genomic dynamics and architecture are poorly understood. In this study, we took advantage of a natural experiment in an insect population of the non-biting midge Chironomus riparius by monitoring genome-wide allele frequencies before and after a cold snap event. Whole genome pooled sequencing of time series samples revealed 10 selected haplotypes carrying ancient polymorphisms, partially with signatures of balancing selection. By constantly cold exposing genetically variable individuals in the laboratory, we could demonstrate with whole genome resequencing (i) that among the survivors, the same alleles rose in frequency as in the wild, and (ii) that the identified variants additively predicted fitness (survival time) of its bearers. Finally, by simultaneously sequencing the genome and the transcriptome of cold exposed individuals we could tentatively link some of the selected SNPs to the cis- and trans-regulation of genes and pathways known to be involved in cold response of insects, such as cytochrome P450 and fatty acid metabolism. Altogether, our results shed light on the strength and speed of selection in natural populations and the genomic architecture of its underlying polygenic trait. Population genomic time series data thus appear as promising tool for measuring the selective tracking of fluctuating selection in natural populations.

Fluctuating Environments Maintain Genetic Diversity through Neutral Fitness Effects and Balancing Selection.

Genetic variation is the raw material upon which selection acts. The majority of environmental conditions change over time and therefore may result in variable selective effects. How temporally fluctuating environments impact the distribution of fitness effects and in turn population diversity is an unresolved question in evolutionary biology. Here, we employed continuous culturing using chemostats to establish environments that switch periodically between different nutrient limitations and compared the dynamics of selection to static conditions. We used the pooled Saccharomyces cerevisiae haploid gene deletion collection as a synthetic model for populations comprising thousands of unique genotypes. Using barcode sequencing, we find that static environments are uniquely characterized by a small number of high-fitness genotypes that rapidly dominate the population leading to dramatic decreases in genetic diversity. By contrast, fluctuating environments are enriched in genotypes with neutral fitness effects and an absence of extreme fitness genotypes contributing to the maintenance of genetic diversity. We also identified a unique class of genotypes whose frequencies oscillate sinusoidally with a period matching the environmental fluctuation. Oscillatory behavior corresponds to large differences in short-term fitness that are not observed across long timescales pointing to the importance of balancing selection in maintaining genetic diversity in fluctuating environments. Our results are consistent with a high degree of environmental specificity in the distribution of fitness effects and the combined effects of reduced and balancing selection in maintaining genetic diversity in the presence of variable selection.

Increasing temporal variance leads to stable species range limits.

What prevents populations of a species from adapting to the novel environments outside the species' geographic distribution? Previous models highlighted how gene flow across spatial environmental gradients determines species expansion versus extinction and the location of species range limits. However, space is only one of two axes of environmental variation-environments also vary in time, and we know temporal environmental variation has important consequences for population demography and evolution. We used analytical and individual-based evolutionary models to explore how temporal variation in environmental conditions influences the spread of populations across a spatial environmental gradient. We find that temporal variation greatly alters our predictions for range dynamics compared to temporally static environments. When temporal variance is equal across the landscape, the fate of species (expansion versus extinction) is determined by the interaction between the degree of temporal autocorrelation in environmental fluctuations and the steepness of the spatial environmental gradient. When the magnitude of temporal variance changes across the landscape, stable range limits form where this variance increases maladaptation sufficiently to prevent local persistence. These results illustrate the pivotal influence of temporal variation on the likelihood of populations colonizing novel habitats and the location of species range limits.

Magnitude and Predictability of pH Fluctuations Shape Plastic Responses to Ocean Acidification.

AbstractPhenotypic plasticity is expected to facilitate the persistence of natural populations as global change progresses. The attributes of fluctuating environments that favor the evolution of plasticity have received extensive theoretical investigation, yet empirical validation of these findings is still in its infancy. Here, we combine high-resolution environmental data with a laboratory-based experiment to explore the influence of habitat pH fluctuation dynamics on the plasticity of gene expression in two populations of the Mediterranean mussel, Mytilus galloprovincialis. We linked differences in the magnitude and predictability of pH fluctuations in two habitats to population-specific gene expression profiles in ambient and stressful pH treatments. Our results demonstrate population-based differentiation in gene expression plasticity, whereby mussels native to a habitat exhibiting a large magnitude of pH fluctuations with low predictability display reduced phenotypic plasticity between experimentally imposed pH treatments. This work validates recent theoretical findings on evolution in fluctuating environments, suggesting that the predictability of fluctuating selection pressures may play a predominant role in shaping the phenotypic variation observed across natural populations.

Models for Eco-Evolutionary Extinction Vortices under Balancing Selection.

AbstractThe smaller a population is, the faster it loses genetic diversity as a result of genetic drift. Loss of genetic diversity can reduce population growth rate, making populations even smaller and more vulnerable to loss of genetic diversity. Ultimately, the population can be driven to extinction by this "eco-evolutionary extinction vortex." While there are already quantitative models for extinction vortices resulting from inbreeding depression and mutation accumulation, to date extinction vortices resulting from loss of genetic diversity at loci under various forms of balancing selection have been mainly described verbally. To understand better when such extinction vortices arise and to develop methods for detecting them, we propose quantitative eco-evolutionary models, both stochastic individual-based simulations and deterministic approximations, linking loss of genetic diversity and population decline. Using mathematical analysis and simulations, we identify parameter combinations that exhibit strong interactions between population size and genetic diversity and match our definition of an eco-evolutionary vortex (i.e., per capita population decline rates and per-locus fixation rates increase with decreasing population size and number of polymorphic loci). We further highlight cues that may be exhibited by such populations but find that classical early-warning signals are of limited use in detecting populations undergoing an eco-evolutionary extinction vortex.

Environmental fluctuations dampen the effects of clonal reproduction on evolutionary rescue.

Evolutionary rescue occurs when genetic change allows a population to persist in response to an environmental change that would otherwise have led to extinction. Most studies of evolutionary rescue assume that species have either fully clonal or fully sexual reproduction; however, many species have partially clonal reproductive strategies in which they reproduce both clonally and sexually. Furthermore, the few evolutionary rescue studies that have evaluated partially clonal reproduction did not consider fluctuations in the environment, which are nearly ubiquitous in nature. Here, we use individual-based simulations to investigate how environmental fluctuations (either uncorrelated or positively autocorrelated) influence the effect of clonality on evolutionary rescue. We show that, for moderate magnitudes of environmental fluctuations, as was found in the absence of fluctuations, increasing the degree of clonality increases the probability of population persistence in response to an abrupt environmental change, but decreases persistence in response to a continuous, directional environmental change. However, with large magnitudes of fluctuations, both the benefits of clonality following a step change and the detrimental effects of clonality following a continuous, directional change are generally reduced; in fact, in the latter scenario, increasing clonality can even become beneficial if environmental fluctuations are autocorrelated. We also show that increased generational overlap dampens the effects of environmental fluctuations. Overall, we demonstrate that understanding the evolutionary rescue of partially clonal organisms requires not only knowledge of the species life history and the type of environmental change, but also an understanding of the magnitude and autocorrelation of environmental fluctuations.

Inter-annual and spatial climatic variability have led to a balance between local fluctuating selection and wide-range directional selection in a perennial grass species.

BACKGROUND AND AIMS: The persistence of a plant population under a specific local climatic regime requires phenotypic adaptation with underlying particular combinations of alleles at adaptive loci. The level of allele diversity at adaptive loci within a natural plant population conditions its potential to evolve, notably towards adaptation to a change in climate. Investigating the environmental factors that contribute to the maintenance of adaptive diversity in populations is thus worthwhile. Within-population allele diversity at adaptive loci can be partly driven by the mean climate at the population site but also by its temporal variability. METHODS: The effects of climate temporal mean and variability on within-population allele diversity at putatively adaptive quantitative trait loci (QTLs) were evaluated using 385 natural populations of Lolium perenne (perennial ryegrass) collected right across Europe. For seven adaptive traits related to reproductive phenology and vegetative potential growth seasonality, the average within-population allele diversity at major QTLs (HeA) was computed. KEY RESULTS: Significant relationships were found between HeA of these traits and the temporal mean and variability of the local climate. These relationships were consistent with functional ecology theory. CONCLUSIONS: Results indicated that temporal variability of local climate has likely led to fluctuating directional selection, which has contributed to the maintenance of allele diversity at adaptive loci and thus potential for further adaptation.

MHC Reflects Fine-Scale Habitat Structure in White-Tailed Eagles, Haliaeetus albicilla.

The major histocompatibility complex (MHC) genes code for key immune receptors responsible for recognition of intra- and extracellular pathogens (MHC class I and class II, respectively). It was hypothesized that MHC polymorphism can be maintained via fluctuating selection resulting from between-habitat variation in pathogen regimes. We examined associations between MHC class I and class II genes and habitat structure in an apex avian predator, the white-tailed eagle, Haliaeetus albicilla. We genotyped MHC class I and class II genes in ca. 150 white-tailed eagle chicks from nearly 100 nesting territories distributed across 3 distinct populations in Poland. Habitat structure was quantified at the level of foraging territories and directly at the nest sites. We found strong support for associations of habitat traits with diversity and allelic composition at the MHC class II. Forest area within territory and forest productivity were identified as the major habitat predictors of MHC class II polymorphism, whereas other habitat traits (distance to nearest open water, grassland, and water area within territory or understory presence) showed fewer associations with class II alleles. In contrast, there was little support for associations between MHC class I genes and habitat structure. All significant associations were apparent at the within-population level rather than between populations. Our results suggest that extracellular (rather than intracellular) pathogens may exert much stronger selective pressure on the white-tailed eagle. Associations of habitat structure with MHC class II may reflect fluctuating (balancing) selection, which maintains MHC diversity within populations.

Fluctuating selection on migrant adaptive sodium transporter alleles in coastal Arabidopsis thaliana.

Stressors such as soil salinity and dehydration are major constraints on plant growth, causing worldwide crop losses. Compounding these insults, increasing climate volatility requires adaptation to fluctuating conditions. Salinity stress responses are relatively well understood in Arabidopsis thaliana, making this system suited for the rapid molecular dissection of evolutionary mechanisms. In a large-scale genomic analysis of Catalonian A. thaliana, we resequenced 77 individuals from multiple salinity gradients along the coast and integrated these data with 1,135 worldwide A. thaliana genomes for a detailed understanding of the demographic and evolutionary dynamics of naturally evolved salinity tolerance. This revealed that Catalonian varieties adapted to highly fluctuating soil salinity are not Iberian relicts but instead have immigrated to this region more recently. De novo genome assembly of three allelic variants of the high-affinity K+ transporter (HKT1;1) locus resolved structural variation between functionally distinct alleles undergoing fluctuating selection in response to seasonal changes in soil salinity. Plants harboring alleles responsible for low root expression of HKT1;1 and consequently high leaf sodium (HKT1;1HLS ) were migrants that have moved specifically into areas where soil sodium levels fluctuate widely due to geography and rainfall variation. We demonstrate that the proportion of plants harboring HKT1;1HLS alleles correlates with soil sodium level over time, HKT1;1HLS -harboring plants are better adapted to intermediate levels of salinity, and the HKT1;1HLS allele clusters with high-sodium accumulator accessions worldwide. Together, our evidence suggests that HKT1;1 is under fluctuating selection in response to climate volatility and is a worldwide determinant in adaptation to saline conditions.

Fierce Selection and Interference in B-Cell Repertoire Response to Chronic HIV-1.

During chronic infection, HIV-1 engages in a rapid coevolutionary arms race with the host's adaptive immune system. While it is clear that HIV exerts strong selection on the adaptive immune system, the characteristics of the somatic evolution that shape the immune response are still unknown. Traditional population genetics methods fail to distinguish chronic immune response from healthy repertoire evolution. Here, we infer the evolutionary modes of B-cell repertoires and identify complex dynamics with a constant production of better B-cell receptor (BCR) mutants that compete, maintaining large clonal diversity and potentially slowing down adaptation. A substantial fraction of mutations that rise to high frequencies in pathogen-engaging CDRs of BCRs are beneficial, in contrast to many such changes in structurally relevant frameworks that are deleterious and circulate by hitchhiking. We identify a pattern where BCRs in patients who experience larger viral expansions undergo stronger selection with a rapid turnover of beneficial mutations due to clonal interference in their CDR3 regions. Using population genetics modeling, we show that the extinction of these beneficial mutations can be attributed to the rise of competing beneficial alleles and clonal interference. The picture is of a dynamic repertoire, where better clones may be outcompeted by new mutants before they fix.

Among-individual and within-individual variation in seasonal migration covaries with subsequent reproductive success in a partially migratory bird.

Within-individual and among-individual variation in expression of key environmentally sensitive traits, and associated variation in fitness components occurring within and between years, determine the extents of phenotypic plasticity and selection and shape population responses to changing environments. Reversible seasonal migration is one key trait that directly mediates spatial escape from seasonally deteriorating environments, causing spatio-seasonal population dynamics. Yet, within-individual and among-individual variation in seasonal migration versus residence, and dynamic associations with subsequent reproductive success, have not been fully quantified. We used novel capture-mark-recapture mixture models to assign individual European shags (Phalacrocorax aristotelis) to 'resident', 'early migrant', or 'late migrant' strategies in two consecutive years, using year-round local resightings. We demonstrate substantial among-individual variation in strategy within years, and directional within-individual change between years. Furthermore, subsequent reproductive success varied substantially among strategies, and relationships differed between years; residents and late migrants had highest success in the 2 years, respectively, matching the years in which these strategies were most frequently expressed. These results imply that migratory strategies can experience fluctuating reproductive selection, and that flexible expression of migration can be partially aligned with reproductive outcomes. Plastic seasonal migration could then potentially contribute to adaptive population responses to currently changing forms of environmental seasonality.