SNP-level FST outperforms window statistics for detecting soft sweeps in local adaptation

Local adaptation can lead to elevated genetic differentiation at the targeted genetic variant and nearby sites. Selective sweeps come in different forms, and depending on the initial and final frequencies of a favored variant, very different patterns of genetic variation may be produced. If local selection favors an existing variant that had already recombined onto multiple genetic backgrounds, then the width of elevated genetic differentiation (high FST) may be too narrow to detect using a typical windowed genome scan, even if the targeted variant becomes highly differentiated. We therefore used a simulation approach to investigate the power of SNP-level FST (specifically, the maximum SNP FST value within a window) to detect diverse scenarios of local adaptation, and compared it against whole-window FST and the Comparative Haplotype Identity statistic. We found that SNP FST had superior power to detect complete or mostly complete soft sweeps, but lesser power than window-wide statistics to detect partial hard sweeps. To investigate the relative enrichment and nature of SNP FST outliers from real data, we applied the two FST statistics to a panel of Drosophila melanogaster populations. We found that SNP FST had a genome-wide enrichment of outliers compared to demographic expectations, and though it yielded a lesser enrichment than window FST, it detected mostly unique outlier genes and functional categories. Our results suggest that SNP FST is highly complementary to typical window-based approaches for detecting local adaptation, and merits inclusion in future genome scans and methodologies.

Two modes of evolution shape bacterial strain diversity in the gut for thousands of generations

How and at what pace bacteria evolve when colonizing healthy hosts remains unclear. Here, by monitoring evolution for more than six thousand generations in the mouse gut, we show that the successful colonization of an invader Escherichia coli depends on the diversity of the existing microbiota and the presence of a closely related strain. Following colonization, two modes of evolution were observed: one in which diversifying selection leads to long-term coexistence of ecotypes and a second in which directional selection propels selective sweeps. These modes can be quantitatively distinguished by the statistics of mutation trajectories. In our experiments, diversifying selection was marked by the emergence of metabolic mutations, and directional selection by acquisition of prophages, which bring their own benefits and costs. In both modes, we observed parallel evolution, with mutation accumulation rates comparable to those typically observed in vitro on similar time scales. Our results show that gut environments can rapidly generate diversifying selection and ecotype formation.

Genetic Diversity, Structure, and Selective Sweeps in Spinacia turkestanica Associated With the Domestication of Cultivated Spinach

Genotype-by-sequencing (GBS) was used to explore the genetic diversity and structure of Spinacia turkestanica, and the selective sweeps involved in domestication of cultivated spinach, S. oleracea, from S. turkestanica. A total 7,065 single nucleotide polymorphisms (SNPs) generated for 16 Spinacia oleracea and 76 S. turkestanica accessions placed the S. oleracea accessions in one group, Q1, and the 76 S. turkestanica accessions, which originated from Central Asia, in two distinct groups, Q2 and Q3. The Q2 group shared greater genetic identity with the S. oleracea accessions, Q1, than the Q3 S. turkestanica group. Likewise, the S. oleracea Q1 group had a smaller Fst (0.008) with the Q2 group than with the Q3 group (Fst = 0.012), and a greater gene flow (Nm = 30.13) with the Q2 group than with the Q3 group (Nm = 21.83). The Q2 accessions originated primarily from Uzbekistan while the Q3 accessions originated mostly from Tajikistan. The Zarafshan Mountain Range appears to have served as a physical barrier that largely separated members of the Q2 and Q3 groups of S. turkestanica. Accessions with admixtures of Q2 and Q3 were collected primarily from lower elevations at the southern end of the Zarafshan Mountain Range in Uzbekistan. Selective sweep regions identified at 32, 49, and 52 Mb on chromosomes 1, 2, and 3, respectively, appear to have played a vital role in the domestication of S. oleracea as they are correlated with important domestication traits, including day length sensitivity for bolting (flowering). High XP-CLR scores at the 52 Mb genomic region of chromosome three suggest that a selective sweep at this region was responsible for early differentiation of S. turkestanica into two groups in Central Asia.

Genetic diversity and selective sweeps in historical and modern Canadian spring wheat cultivars using the 90K SNP array

Previous molecular characterization studies conducted in Canadian wheat cultivars shed some light on the impact of plant breeding on genetic diversity, but the number of varieties and markers used was small. Here, we used 28,798 markers of the wheat 90K single nucleotide polymorphisms to (a) assess the extent of genetic diversity, relationship, population structure, and divergence among 174 historical and modern Canadian spring wheat varieties registered from 1905 to 2018 and 22 unregistered lines (hereinafter referred to as cultivars), and (b) identify genomic regions that had undergone selection. About 91% of the pairs of cultivars differed by 20–40% of the scored alleles, but only 7% of the pairs had kinship coefficients of < 0.250, suggesting the presence of a high proportion of redundancy in allelic composition. Although the 196 cultivars represented eight wheat classes, our results from phylogenetic, principal component, and the model-based population structure analyses revealed three groups, with no clear structure among most wheat classes, breeding programs, and breeding periods. FST statistics computed among different categorical variables showed little genetic differentiation (< 0.05) among breeding periods and breeding programs, but a diverse level of genetic differentiation among wheat classes and predicted groups. Diversity indices were the highest and lowest among cultivars registered from 1970 to 1980 and from 2011 to 2018, respectively. Using two outlier detection methods, we identified from 524 to 2314 SNPs and 41 selective sweeps of which some are close to genes with known phenotype, including plant height, photoperiodism, vernalization, gluten strength, and disease resistance.

Selective Sweeps and Polygenic Adaptation Drive Local Adaptation along Moisture and Temperature Gradients in Natural Populations of Coast Redwood and Giant Sequoia

Dissecting the genomic basis of local adaptation is a major goal in evolutionary biology and conservation science. Rapid changes in the climate pose significant challenges to the survival of natural populations, and the genomic basis of long-generation plant species is still poorly understood. Here, we investigated genome-wide climate adaptation in giant sequoia and coast redwood, two iconic and ecologically important tree species. We used a combination of univariate and multivariate genotype–environment association methods and a selective sweep analysis using non-overlapping sliding windows. We identified genomic regions of potential adaptive importance, showing strong associations to moisture variables and mean annual temperature. Our results found a complex architecture of climate adaptation in the species, with genomic regions showing signatures of selective sweeps, polygenic adaptation, or a combination of both, suggesting recent or ongoing climate adaptation along moisture and temperature gradients in giant sequoia and coast redwood. The results of this study provide a first step toward identifying genomic regions of adaptive significance in the species and will provide information to guide management and conservation strategies that seek to maximize adaptive potential in the face of climate change.

Effects of Selection at Linked Sites on Patterns of Genetic Variability

Patterns of variation and evolution at a given site in a genome can be strongly influenced by the effects of selection at genetically linked sites. In particular, the recombination rates of genomic regions correlate with their amount of within-population genetic variability, the degree to which the frequency distributions of DNA sequence variants differ from their neutral expectations, and the levels of adaptation of their functional components. We review the major population genetic processes that are thought to lead to these patterns, focusing on their effects on patterns of variability: selective sweeps, background selection, associative overdominance, and Hill–Robertson interference among deleterious mutations. We emphasize the difficulties in distinguishing among the footprints of these processes and disentangling them from the effects of purely demographic factors such as population size changes. We also discuss how interactions between selective and demographic processes can significantly affect patterns of variability within genomes.

Decreased recent adaptation at human mendelian disease genes as a possible consequence of interference between advantageous and deleterious variants

Advances in genome sequencing have dramatically improved our understanding of the genetic basis of human diseases, and thousands of human genes have been associated with different diseases. Despite our expanding knowledge of gene-disease associations, and despite the medical importance of disease genes, their recent evolution has not been thoroughly studied across diverse human populations. In particular, recent genomic adaptation at disease genes has not been characterized as well as purifying selection and long-term adaptation. Understanding the relationship between disease and adaptation at the gene level in the human genome is hampered by the fact that we don’t know whether disease genes have experienced more, less, or as much adaptation as non-disease genes during the last ~50,000 years of recent human evolution. Here, we compare the rate of strong recent adaptation in the form of selective sweeps between mendelian, non-infectious disease genes and non-disease genes across 26 distinct human populations from the 1,000 Genomes Project. We find that mendelian disease genes have experienced far less selective sweeps compared to non-disease genes especially in Africa. This sweep deficit at mendelian disease genes is less visible in East Asia or Europe. Investigating further the possible causes of the sweep deficit at disease genes, we find that this deficit is very strong at disease genes with both low recombination rates and with high numbers of associated disease variants, but is almost non-existent at disease genes with higher recombination rates or lower numbers of associated disease variants. Because segregating recessive deleterious variants have the ability to interfere with adaptive ones, these observations strongly suggest that adaptation has been slowed down by the presence of interfering recessive deleterious variants at disease genes. This is further supported by population simulations that show that interference at disease genes is expected to be lower in East Asia and Europe. These results clarify the evolutionary relationship between disease genes and recent genomic adaptation, and suggest that disease genes suffer not only from a higher load of segregating deleterious mutations, but also from a transient inability to adapt as much, and/or as fast as the rest of the genome.

Sporadic Occurrence of Recent Selective Sweeps from Standing Variation in Humans as Revealed by an Approximate Bayesian Computation Approach

During their dispersals over the last 100,000 years, modern humans have been exposed to a large variety of environments, resulting in genetic adaptation. While genome-wide scans for the footprints of positive Darwinian selection have increased knowledge of genes and functions potentially involved in human local adaptation, they have globally produced evidence of a limited contribution of selective sweeps in humans. Conversely, studies based on machine learning algorithms suggest that recent sweeps from standing variation are widespread in humans, an observation that has been recently questioned. Here, we sought to formally quantify the number of recent selective sweeps in humans, by leveraging approximate Bayesian computation and whole-genome sequence data. Our computer simulations revealed suitable ABC estimations, regardless of the frequency of the selected alleles at the onset of selection and the completion of sweeps. Under a model of recent selection from standing variation, we inferred that an average of 68 (from 56 to 79) and 140 (from 94 to 198) sweeps occurred over the last 100,000 years of human history, in African and Eurasian populations, respectively. The former estimation is compatible with human adaptation rates estimated since divergence with chimps, and reveal numbers of sweeps per generation per site in the range of values estimated in Drosophila. Our results confirm the rarity of selective sweeps in humans and show a low contribution of sweeps from standing variation to recent human adaptation.