Evolution In Natural Populations Research Articles

Manipulating a host-native microbial strain compensates for low microbial diversity by increasing weight gain in a wild bird population

Empirical studies from laboratory systems and humans show that the gut microbiota is linked to host health. Similar evidence for effects on traits linked to fitness in nature is rare, not least because experimentally manipulating the gut microbiota is challenging. We isolated, characterized, and cultured a bacterial strain, Lactobacillus kimchicus APC4233, directly from a wild bird (the great tit Parus major) and provided it as a self-administered dietary supplement. We assessed the impact of the treatment on the host microbiota community, on weight, and tested whether the treatment affected a previous result linking microbiota alpha diversity to weight in nestlings. The treatment dramatically increased L. kimchicus abundance in the gut microbiota and increased alpha diversity. This effect was strongest in the youngest birds, validating earlier findings pointing to a brief developmental window when the gut microbiota are most sensitive. In time-lagged models, nestling weight was higher in the treatment birds suggesting L. kimchicus may have probiotic potential. There was also a positive time-lagged relationship between diversity and weight in control birds but not in the treatment birds, suggesting L. kimchicus helped birds compensate for low alpha diversity. We discuss why ecological context is likely key when predicting impacts of the microbiome. The manipulation of the gut microbiota with a host native strain in this wild population provides direct evidence for the role of the microbiota in the ecology and evolution of natural populations.

Pollution offsets the rapid evolution of increased heat tolerance in a natural population

Despite the increasing evidence for rapid thermal evolution in natural populations, evolutionary rescue under global warming may be constrained by the presence of other stressors. Highly relevant in our polluted planet, is the largely ignored evolutionary trade-off between heat tolerance and tolerance to pollutants. By using two subpopulations (separated 40 years in time) from a resurrected natural population of the water flea Daphnia magna that experienced a threefold increase in heat wave frequency during this period, we tested whether rapid evolution of heat tolerance resulted in reduced tolerance to the widespread metal zinc and whether this would affect heat tolerance upon exposure to the pollutant. Our results revealed rapid evolution of increased heat tolerance in the recent subpopulation. Notably, the sensitivity to the metal tended to be stronger (reduction in net energy budget) or was only present (reductions in heat tolerance and in sugar content) in the recent subpopulation. As a result, the rapidly evolved higher heat tolerance of the recent subpopulation was fully offset when exposed to zinc. Our results highlight that the many reports of evolutionary rescue to global change stressors may give a too optimistic view as our warming planet is polluted by metals and other pollutants.

Evolution of loss of heterozygosity patterns in hybrid genomes of Candida yeast pathogens

BackgroundHybrids are chimeric organisms with highly plastic heterozygous genomes that may confer unique traits enabling the adaptation to new environments. However, most evolutionary theory frameworks predict that the high levels of genetic heterozygosity present in hybrids from divergent parents are likely to result in numerous deleterious epistatic interactions. Under this scenario, selection is expected to favor recombination events resulting in loss of heterozygosity (LOH) affecting genes involved in such negative interactions. Nevertheless, it is so far unknown whether this phenomenon actually drives genomic evolution in natural populations of hybrids. To determine the balance between selection and drift in the evolution of LOH patterns in natural yeast hybrids, we analyzed the genomic sequences from fifty-five hybrid strains of the pathogenic yeasts Candida orthopsilosis and Candida metapsilosis, which derived from at least six distinct natural hybridization events.ResultsWe found that, although LOH patterns in independent hybrid clades share some level of convergence that would not be expected from random occurrence, there is an apparent lack of strong functional selection. Moreover, while mitosis is associated with a limited number of inter-homeologous chromosome recombinations in these genomes, induced DNA breaks seem to increase the LOH rate. We also found that LOH does not accumulate linearly with time in these hybrids. Furthermore, some C. orthopsilosis hybrids present LOH patterns compatible with footprints of meiotic recombination. These meiotic-like patterns are at odds with a lack of evidence of sexual recombination and with our inability to experimentally induce sporulation in these hybrids.ConclusionsOur results suggest that genetic drift is the prevailing force shaping LOH patterns in these hybrid genomes. Moreover, the observed LOH patterns suggest that these are likely not the result of continuous accumulation of sporadic events—as expected by mitotic repair of rare chromosomal breaks—but rather of acute episodes involving many LOH events in a short period of time.

The Post-Antibiotic Era: A New Dawn for Bacteriophages.

Phages are the most biologically diverse entities in the biosphere, infecting specific bacteria. Lytic phages quickly kill bacteria, while lysogenic phages integrate their genomes into bacteria and reproduce within the bacteria, participating in the evolution of natural populations. Thus, lytic phages are used to treat bacterial infections. However, due to the huge virus invasion, bacteria have also evolved a special immune mechanism (CRISPR-Cas systems, discovered in 1987). Therefore, it is necessary to develop phage cocktails and synthetic biology methods to infect bacteria, especially against multidrug-resistant bacteria infections, which are a major global threat. This review outlines the discovery and classification of phages and the associated achievements in the past century. The main applications of phages, including synthetic biology and PT, are also discussed, in addition to the effects of PT on immunity, intestinal microbes, and potential safety concerns. In the future, combining bioinformatics, synthetic biology, and classic phage research will be the way to deepen our understanding of phages. Overall, whether phages are an important element of the ecosystem or a carrier that mediates synthetic biology, they will greatly promote the progress of human society.

Host-specific plasmid evolution explains the variable spread of clinical antibiotic-resistance plasmids

Antibiotic resistance encoded on plasmids is a pressing global health problem. Predicting which plasmids spread in the long term remains very challenging, even though some key parameters influencing plasmid stability have been identified, such as plasmid growth costs and horizontal transfer rates. Here, we show these parameters evolve in a strain-specific way among clinical plasmids and bacteria, and this occurs rapidly enough to alter the relative likelihoods of different bacterium-plasmid combinations spreading. We used experiments with Escherichia coli and antibiotic-resistance plasmids isolated from patients, paired with a mathematical model, to track long-term plasmid stability (beyond antibiotic exposure). Explaining variable stability across six bacterium-plasmid combinations required accounting for evolutionary changes in plasmid stability traits, whereas initial variation of these parameters was a relatively poor predictor of long-term outcomes. Evolutionary trajectories were specific to particular bacterium-plasmid combinations, as evidenced by genome sequencing and genetic manipulation. This revealed epistatic (here, strain-dependent) effects of key genetic changes affecting horizontal plasmid transfer. Several genetic changes involved mobile elements and pathogenicity islands. Rapid strain-specific evolution can thus outweigh ancestral phenotypes as a predictor of plasmid stability. Accounting for strain-specific plasmid evolution in natural populations could improve our ability to anticipate and manage successful bacterium-plasmid combinations.

The Dynamics of Adaptation to Stress from Standing Genetic Variation and de novo Mutations.

Adaptation from standing genetic variation is an important process underlying evolution in natural populations, but we rarely get the opportunity to observe the dynamics of fitness and genomic changes in real time. Here, we used experimental evolution and Pool-Seq to track the phenotypic and genomic changes of genetically diverse asexual populations of the yeast Saccharomyces cerevisiae in four environments with different fitness costs. We found that populations rapidly and in parallel increased in fitness in stressful environments. In contrast, allele frequencies showed a range of trajectories, with some populations fixing all their ancestral variation in <30 generations and others maintaining diversity across hundreds of generations. We detected parallelism at the genomic level (involving genes, pathways, and aneuploidies) within and between environments, with idiosyncratic changes recurring in the environments with higher stress. In particular, we observed a tendency of becoming haploid-like in one environment, whereas the populations of another environment showed low overall parallelism driven by standing genetic variation despite high selective pressure. This work highlights the interplay between standing genetic variation and the influx of de novo mutations in populations adapting to a range of selective pressures with different underlying trait architectures, advancing our understanding of the constraints and drivers of adaptation.

Shared and unique responses in the microbiome of allopatric lizards reared in a standardized environment.

The gut microbiome can influence host fitness and, consequently, the ecology and evolution of natural populations. Microbiome composition can be driven by environmental exposure but also by the host's genetic background and phenotype. To contrast environmental and genetic effects on the microbiome we leverage preserved specimens of eastern fence lizards from allopatric lineages east and west of the Mississippi River but reared in standardized conditions. Bacterial composition was indistinguishable between lineages but responded significantly to host age-a proxy for environmental exposure. This was accompanied by a continuous decrease in bacterial diversity in both lineages, partially driven by decreasing evenness seen only in western lizards. These findings indicate that longer exposure to a homogeneous habitat may have a depreciating effect on microbiome diversity in eastern fence lizards, a response shared by both lineages. We highlight the importance of such effects when extrapolating patterns from laboratory experiments to the natural world.

Natural selection favours drought escape and an acquisitive resource‐use strategy in semi‐arid Mediterranean shrubs

AbstractNatural selection is the major force driving adaptive evolution in natural populations, varying in strength, direction, and form through space and time, especially in highly variable environments such as Mediterranean ecosystems. Although a conservative resource‐use strategy has been hypothesized to be adaptive in Mediterranean taxa, patterns of selection at the intraspecific level, that is, the suite of traits determining individual fitness, are largely unknown.Using a phenotypic selection experiment in natural semi‐arid conditions, we measured direct and indirect selection acting through two different fitness components (survival and reproduction), to assess the adaptive value of 20 ecophysiological traits on individuals of two gypsum endemic species,Centaurea hyssopifoliaandHelianthemum squamatum, dwelling in environments with contrasting abiotic conditions (south‐ and north‐facing slopes) during two climatically contrasting years (dry and mesic). This allowed quantifying the magnitude and direction of natural selection at different spatiotemporal scales.Our results revealed that different abiotic conditions did not alter selection patterns, being the magnitude of selection more strongly affected by temporal environmental variation. Selection through reproduction indicated consistent selection for early phenology, low water use efficiency, high specific leaf area, low leaf dry matter content, and high leaf N across slopes and years in both species. In contrast, phenotypic trait variation was not linked to survival in either species. Furthermore, while individual reproductive output was higher or similar in environments with higher abiotic stress in both species and years, survival was similar across environmental conditions, and it was neither affected by plant size nor reproductive output.Contrary to our expectations, natural selection via reproductive fitness consistently favoured a drought‐escape, acquisitive resource‐use strategy in Mediterranean semi‐arid plants, rather than a conservative resource‐use strategy, even under conditions of higher abiotic stress (i.e. south slopes and dry year). Such acquisitive strategy could allow rapid development by maximizing resource assimilation and reproduction before the most limiting climatic conditions of mid‐late summer. Our results shed light on adaptive functional strategies of Mediterranean taxa at the intraspecific level, providing insight on future responses to environmental change, and highlight remarkable differences in selection acting through different fitness components.Read the freePlain Language Summaryfor this article on the Journal blog.

Evidence for continent-wide convergent evolution and stasis throughout 150 y of a biological invasion

The extent to which evolution can rescue a species from extinction, or facilitate range expansion, depends critically on the rate, duration, and geographical extent of the evolutionary response to natural selection. Adaptive evolution can occur quickly, but the duration and geographical extent of contemporary evolution in natural systems remain poorly studied. This is particularly true for species with large geographical ranges and for timescales that lie between “long-term” field experiments and the fossil record. Here, we introduce the Virtual Common Garden (VCG) to investigate phenotypic evolution in natural history collections while controlling for phenotypic plasticity in response to local growing conditions. Reconstructing 150 y of evolution in Lythrum salicaria (purple loosestrife) as it invaded North America, we analyze phenology measurements of 3,429 herbarium records, reconstruct growing conditions from more than 12 million local temperature records, and validate predictions across three common gardens spanning 10° of latitude. We find that phenological clines have evolved repeatedly throughout the range, during the first century of evolution. Thereafter, the rate of microevolution stalls, recapitulating macroevolutionary stasis observed in the fossil record. Our study demonstrates that preserved specimens are a critical resource for investigating limits to evolution in natural populations. Our results show how natural selection and trade-offs measured in field studies predict adaptive divergence observable in herbarium specimens over 15 decades at a continental scale.

Dynamic Behaviors of a Stochastic Eco-Epidemiological Model for Viral Infection in the Toxin-Producing Phytoplankton and Zooplankton System

It is well known that the evolution of natural populations is almost inevitably disturbed by various environmental factors. Various experiments have shown that the growth of phytoplankton might be affected by nutrient availability, water temperature, and light, while the development of zooplankton is more disturbed by the pH value of the seawater, water temperature, and water movement. However, it is not clear how these environmental fluctuations affect the dynamical behavior of the phytoplankton and zooplankton system. In this paper, a stochastic eco-epidemiological model for viral infection in the toxin-producing phytoplankton and zooplankton system is proposed. Firstly, the existence and uniqueness of globally positive solutions for this model is shown. Secondly, the stochastic boundedness of solutions for the model is proved. Moreover, sufficient conditions for the extinction and persistence in the mean for the phytoplankton and zooplankton are obtained by constructing appropriate stochastic Lyapunov functions and using analytical techniques. Numerical simulations are carried out to demonstrate different dynamical behaviors including coexistence, extinction of the whole plankton system, partial persistence and extinction, and their corresponding probability density curves.

Convergent consequences of parthenogenesis on stick insect genomes.

The shift from sexual reproduction to parthenogenesis has occurred repeatedly in animals, but how the loss of sex affects genome evolution remains poorly understood. We generated reference genomes for five independently evolved parthenogenetic species in the stick insect genus Timema and their closest sexual relatives. Using these references and population genomic data, we show that parthenogenesis results in an extreme reduction of heterozygosity and often leads to genetically uniform populations. We also find evidence for less effective positive selection in parthenogenetic species, suggesting that sex is ubiquitous in natural populations because it facilitates fast rates of adaptation. Parthenogenetic species did not show increased transposable element (TE) accumulation, likely because there is little TE activity in the genus. By using replicated sexual-parthenogenetic comparisons, our study reveals how the absence of sex affects genome evolution in natural populations, providing empirical support for the negative consequences of parthenogenesis as predicted by theory.

The evolution of larger size in high-altitude Drosophila melanogaster has a variable genetic architecture.

Important uncertainties persist regarding the genetic architecture of adaptive trait evolution in natural populations, including the number of genetic variants involved, whether they are drawn from standing genetic variation, and whether directional selection drives them to complete fixation. Here, we take advantage of a unique natural population of Drosophila melanogaster from the Ethiopian highlands, which has evolved larger body size than any other known population of this species. We apply a bulk segregant quantitative trait locus mapping approach to 4 unique crosses between highland Ethiopian and lowland Zambian populations for both thorax length and wing length. Results indicated a persistently variable genetic basis for these evolved traits (with largely distinct sets of quantitative trait loci for each cross), and at least a moderately polygenic architecture with relatively strong effects present. We complemented these mapping experiments with population genetic analyses of quantitative trait locus regions and gene ontology enrichment analysis, generating strong hypotheses for specific genes and functional processes that may have contributed to these adaptive trait changes. Finally, we find that the genetic architectures indicated by our quantitative trait locus mapping results for size traits mirror those from similar experiments on other recently evolved traits in this species. Collectively, these studies suggest a recurring pattern of polygenic adaptation in this species, in which causative variants do not approach fixation and moderately strong effect loci are present.

The distribution of mutational effects on fitness in Caenorhabditis elegans inferred from standing genetic variation.

The distribution of fitness effects (DFE) for new mutations is one of the most theoretically important but difficult to estimate properties in population genetics. A crucial challenge to inferring the DFE from natural genetic variation is the sensitivity of the site frequency spectrum to factors like population size change, population substructure, genome structure, and nonrandom mating. Although inference methods aim to control for population size changes, the influence of nonrandom mating remains incompletely understood, despite being a common feature of many species. We report the DFE estimated from 326 genomes of Caenorhabditis elegans, a nematode roundworm with a high rate of self-fertilization. We evaluate the robustness of DFE inferences using simulated data that mimics the genomic structure and reproductive life history of C. elegans. Our observations demonstrate how the combined influence of self-fertilization, genome structure, and natural selection on linked sites can conspire to compromise estimates of the DFE from extant polymorphisms with existing methods. These factors together tend to bias inferences toward weakly deleterious mutations, making it challenging to have full confidence in the inferred DFE of new mutations as deduced from standing genetic variation in species like C. elegans. Improved methods for inferring the DFE are needed to appropriately handle strong linked selection and selfing. These results highlight the importance of understanding the combined effects of processes that can bias our interpretations of evolution in natural populations.

Rapid divergent evolution of an annual plant across a latitudinal gradient revealed by seed resurrection.

Global change is expected to drive short-term evolution of natural populations. However, it remains unclear whether different populations are changing in unison. Here, we study contemporary evolution of growth-related and reproductive traits of three populations of Cyanus segetum facing warming and pollinator decline across a latitudinal gradient in France. We resurrected stored seeds sampled up to 24 years apart from northern, central-western, and southern populations and conducted an in situ common-garden experiment. To disentangle neutral from selection-driven differentiation, we calculated neutral genetic differentiation (FST ) and quantitative trait differentiation (QST ) between temporal samples. We found that phenotypic evolution was divergent across populations exhibiting different trends for rosette size, date of flowering, and capitula size. By measuring seed set as a proxy of fitness, we showed that samples with larger mean capitula size outperformed samples with smaller mean capitula size in the western and southern populations. Regression of traits on seed set showed that flowering date and capitula size are the primary determinants of fitness, and QST -FST comparisons indicated that natural selection has likely contributed to the shifts in flowering phenology and rosette size. These findings outline the potential for rescue of natural populations through contemporary evolution and emphasize the complex interplay between spatial and temporal variation in species' responses to global change.

Brain size variation along altitudinal gradients in the Asiatic Toad (Bufo gargarizans).

Size changes in brain and brain regions along altitudinal gradients provide insight into the trade‐off between energetic expenditure and cognitive capacity. We investigated the brain size variations of the Asiatic Toad (Bufo gargarizans) across altitudes from 700 m to 3,200 m. A total of 325 individuals from 11 sites and two transects were sampled. To reduce confounding factors, all sampling sites within each transect were within a maximum distance of 85 km and an altitudinal difference close to 2,000 m. Brains were dissected, and five regions were both measured directly and with 3D CT scan. There is a significant negative correlation between the relative whole‐brain volume (to snout‐vent length) and altitude. Furthermore, the relative volumes (to whole‐brain volume) of optic tectum and cerebellum also decrease along the altitudinal gradients, while the telencephalon increases its relative volume along the gradients. Therefore, our results are mostly consistent with the expensive brain hypothesis and the functional constraint hypothesis. We suggest that most current hypotheses are not mutually exclusive and data supporting one hypothesis are often partially consistent with others. More studies on mechanisms are needed to explain the brain size evolution in natural populations.

Polygenic adaptation of rosette growth in Arabidopsis thaliana

The rate at which plants grow is a major functional trait in plant ecology. However, little is known about its evolution in natural populations. Here, we investigate evolutionary and environmental factors shaping variation in the growth rate of Arabidopsis thaliana. We used plant diameter as a proxy to monitor plant growth over time in environments that mimicked latitudinal differences in the intensity of natural light radiation, across a set of 278 genotypes sampled within four broad regions, including an outgroup set of genotypes from China. A field experiment conducted under natural conditions confirmed the ecological relevance of the observed variation. All genotypes markedly expanded their rosette diameter when the light supply was decreased, demonstrating that environmental plasticity is a predominant source of variation to adapt plant size to prevailing light conditions. Yet, we detected significant levels of genetic variation both in growth rate and growth plasticity. Genome-wide association studies revealed that only 2 single nucleotide polymorphisms associate with genetic variation for growth above Bonferroni confidence levels. However, marginally associated variants were significantly enriched among genes with an annotated role in growth and stress reactions. Polygenic scores computed from marginally associated variants confirmed the polygenic basis of growth variation. For both light regimes, phenotypic divergence between the most distantly related population (China) and the various regions in Europe is smaller than the variation observed within Europe, indicating that the evolution of growth rate is likely to be constrained by stabilizing selection. We observed that Spanish genotypes, however, reach a significantly larger size than Northern European genotypes. Tests of adaptive divergence and analysis of the individual burden of deleterious mutations reveal that adaptive processes have played a more important role in shaping regional differences in rosette growth than maladaptive evolution.

Tissue-specific patterns of regulatory changes underlying gene expression differences among Ficedula flycatchers and their naturally occurring F1 hybrids.

Changes in interacting cis- and trans-regulatory elements are important candidates for Dobzhansky-Muller hybrid incompatibilities and may contribute to hybrid dysfunction by giving rise to misexpression in hybrids. To gain insight into the molecular mechanisms and determinants of gene expression evolution in natural populations, we analyzed the transcriptome from multiple tissues of two recently diverged Ficedula flycatcher species and their naturally occurring F1 hybrids. Differential gene expression analysis revealed that the extent of differentiation between species and the set of differentially expressed genes varied across tissues. Common to all tissues, a higher proportion of Z-linked genes than autosomal genes showed differential expression, providing evidence for a fast-Z effect. We further found clear signatures of hybrid misexpression in brain, heart, kidney, and liver. However, while testis showed the highest divergence of gene expression among tissues, it showed no clear signature of misexpression in F1 hybrids, even though these hybrids were found to be sterile. It is therefore unlikely that incompatibilities between cis-trans regulatory changes explain the observed sterility. Instead, we found evidence that cis-regulatory changes play a significant role in the evolution of gene expression in testis, which illustrates the tissue-specific nature of cis-regulatory evolution bypassing constraints associated with pleiotropic effects of genes.

Rapid evolutionary changes in gene expression in response to climate fluctuations.

There is now abundant evidence of rapid evolution in natural populations, but the genetic mechanisms of these changes remain unclear. One possible route to rapid evolution is through changes in the expression of genes that influence traits under selection. We examined contemporary evolutionary gene expression changes in plant populations responding to environmental fluctuations. We compared genome‐wide gene expression, using RNA‐seq, in two populations of Brassica rapa collected over four time points between 1997 and 2014, during which precipitation in southern California fluctuated dramatically and phenotypic and genotypic changes occurred. By combining transcriptome profiling with the resurrection approach, we directly examined evolutionary changes in gene expression over time. For both populations, we found a substantial number of differentially expressed genes between generations, indicating rapid evolution in the expression of many genes. Using existing gene annotations, we found that many changes occurred in genes involved in regulating stress responses and flowering time. These appeared related to the fluctuations in precipitation and were potentially adaptive. However, the evolutionary changes in gene expression differed across generations within and between populations, indicating largely independent evolutionary trajectories across populations and over time. Our study provides strong evidence for rapid evolution in gene expression, and indicates that changes in gene expression can be one mechanism of rapid evolutionary responses to selection episodes. This study also illustrates that combining resurrection studies with transcriptomics is a powerful approach for investigating evolutionary changes at the gene regulatory level, and will provide new insights into the genetic basis of contemporary evolution.

The evolutionary plasticity of chromosome metabolism allows adaptation to constitutive DNA replication stress.

Many biological features are conserved and thus considered to be resistant to evolutionary change. While rapid genetic adaptation following the removal of conserved genes has been observed, we often lack a mechanistic understanding of how adaptation happens. We used the budding yeast, Saccharomyces cerevisiae, to investigate the evolutionary plasticity of chromosome metabolism, a network of evolutionary conserved modules. We experimentally evolved cells constitutively experiencing DNA replication stress caused by the absence of Ctf4, a protein that coordinates the enzymatic activities at replication forks. Parallel populations adapted to replication stress, over 1000 generations, by acquiring multiple, concerted mutations. These mutations altered conserved features of two chromosome metabolism modules, DNA replication and sister chromatid cohesion, and inactivated a third, the DNA damage checkpoint. The selected mutations define a functionally reproducible evolutionary trajectory. We suggest that the evolutionary plasticity of chromosome metabolism has implications for genome evolution in natural populations and cancer.

Senescence in immunity against helminth parasites predicts adult mortality in a wild mammal.

Our understanding of the deterioration in immune function in old age-immunosenescence-derives principally from studies of modern human populations and laboratory animals. The generality and significance of this process for systems experiencing complex, natural infections and environmental challenges are unknown. Here, we show that late-life declines in an important immune marker of resistance to helminth parasites in wild Soay sheep predict overwinter mortality. We found senescence in circulating antibody levels against a highly prevalent nematode worm, which was associated with reduced adult survival probability, independent of changes in body weight. These findings establish a role for immunosenescence in the ecology and evolution of natural populations.