Genome‐wide detection of signatures of selection in Korean Hanwoo cattle

The Korean Hanwoo cattle have been intensively selected for production traits, especially high intramuscular fat content. It is believed that ancient crossings between different breeds contributed to forming the Hanwoo, but little is known about the genomic differences and similarities between other cattle breeds and the Hanwoo. In this work, cattle breeds were grouped by origin into four types and used for comparisons: the Europeans (represented by six breeds), zebu (Nelore), African taurine (N'Dama) and Hanwoo. All animals had genotypes for around 680 000 SNPs after quality control of genotypes. Average heterozygosity was lower in Nelore and N'Dama (0.22 and 0.21 respectively) than in Europeans (0.26–0.31, with Shorthorn as outlier at 0.24) and Hanwoo (0.29). Pairwise F_ST analyses demonstrated that Hanwoo are more related to European cattle than to Nelore, with N'Dama in an intermediate position. This finding was corroborated by principal components and unsupervised hierarchical clustering. Using genome‐wide smoothed F_ST, 55 genomic regions potentially under positive selection in Hanwoo were identified. Among these, 29 were regions also detected in previous studies. Twenty‐four regions were exclusive to Hanwoo, and a number of other regions were shared with one or two of the other groups. These regions overlap a number of genes that are related to immune, reproduction and fatty acid metabolism pathways. Further analyses are needed to better characterize the ancestry of the Hanwoo cattle and to define the genes responsible to the identified selection peaks.     

Screening for signatures of selection of Tianzhu white yak using genome‐wide re‐sequencing

The Tianzhu white yak, a domestic yak indigenous to the Qilian Mountains, migrated inland from the Qinghai‐Tibet Plateau. Specific ecological and long‐term artificial selection influenced the evolution of its pure white coat and physiological characteristics. Therefore, it is not only a natural population that represents a genomic selective region of environmental adaptability but is also an animal model for studying the pigmentation of the yak coat. A total of 24 261 829 variants, including 22 445 252 SNPs, were obtained from 29 yaks by genome‐wide re‐sequencing. According to the results of a selective sweep analysis of Tianzhu white yak in comparison to Tibetan yaks, nine candidate genes under selection in Tianzhu white yak were identified by combining π, Tajima's D, πA/πB and F_ST statistics, with threshold standards of 5%. These genes include PDCD1, NUP210, ABCG8, NEU4, LOC102287650, D2HGDH, COL4A1, RTP5 and HDAC11. Five of the nine genes were classified into 12 molecular signaling pathways, and most of these signaling pathways are involved in environmental information processing, organismal systems and metabolism. A majority of these genes has not been implicated in previous studies of yak coat color and high‐altitude animals. Our findings are helpful not only for explaining the molecular mechanism of yak coat pigmentation but also for exploring the genetic changes in Tianzhu white yak due to environmental adaptation.     

Spatially varying selection shapes life history clines among populations of Drosophila melanogaster from sub‐Saharan Africa

Clines in life history traits, presumably driven by spatially varying selection, are widespread. Major latitudinal clines have been observed, for example, in Drosophila melanogaster, an ancestrally tropical insect from Africa that has colonized temperate habitats on multiple continents. Yet, how geographic factors other than latitude, such as altitude or longitude, affect life history in this species remains poorly understood. Moreover, most previous work has been performed on derived European, American and Australian populations, but whether life history also varies predictably with geography in the ancestral Afro‐tropical range has not been investigated systematically. Here, we have examined life history variation among populations of D. melanogaster from sub‐Saharan Africa. Viability and reproductive diapause did not vary with geography, but body size increased with altitude, latitude and longitude. Early fecundity covaried positively with altitude and latitude, whereas lifespan showed the opposite trend. Examination of genetic variance–covariance matrices revealed geographic differentiation also in trade‐off structure, and Q_ST‐F_ST analysis showed that life history differentiation among populations is likely shaped by selection. Together, our results suggest that geographic and/or climatic factors drive adaptive phenotypic differentiation among ancestral African populations and confirm the widely held notion that latitude and altitude represent parallel gradients.     

Genome‐wide variability and selection signatures in Italian island cattle breeds

In the present study, a sample of 88 animals belonging to four local (Modicana, Sarda, Sardo‐Bruna and Sardo‐Modicana) and one cosmopolitan (Italian Brown Swiss) cattle breeds were genotyped with a medium density SNP beadchip and compared to investigate their genetic diversity and the existence of selection signatures. A total of 43 012 SNPs distributed across all 29 autosomal chromosomes were retained after data quality control. Basic population statistics, Wright fixation index and runs of homozygosity (ROH) analyses confirmed that the Italian Brown Swiss genome was shaped mainly by selection, as underlined by the low values of heterozygosity and minor allele frequency. As expected, local cattle exhibited a large within‐breed genetic heterogeneity. The F_ST comparison revealing the largest number of significant SNPs was Sardo‐Bruna vs. Sardo‐Modicana, whereas the smallest was observed for Italian Brown Swiss vs. Sardo‐Modicana. Modicana exhibited the largest number of detected ROHs, whereas the smallest was observed for Sardo‐Modicana. Signatures of selection were detected in genomic regions that harbor genes involved in milk production traits for Italian Brown Swiss and fitness traits for local breeds. According to the results of multi‐dimensional scaling and the admixture analysis the Sardo‐Bruna is more similar to the Sarda than to the Italian Brown Swiss breed. Moreover, the Sardo‐Modicana is genetically closer to the Modicana than to the Sarda breed. Results of the present work confirm the usefulness of single nucleotide polymorphisms in deciphering the genetic architecture of livestock breeds.     

Genomic signatures of fine‐scale local selection in Atlantic salmon suggest involvement of sexual maturation,energy homeostasis and immune defence‐related genes

Elucidating the genetic basis of adaptation to the local environment can improve our understanding of how the diversity of life has evolved. In this study, we used a dense SNP array to identify candidate loci potentially underlying fine‐scale local adaptation within a large Atlantic salmon (Salmo salar) population. By combining outlier, gene–environment association and haplotype homozygosity analyses, we identified multiple regions of the genome with strong evidence for diversifying selection. Several of these candidate regions had previously been identified in other studies, demonstrating that the same loci could be adaptively important in Atlantic salmon at subdrainage, regional and continental scales. Notably, we identified signals consistent with local selection around genes associated with variation in sexual maturation, energy homeostasis and immune defence. These included the large‐effect age‐at‐maturity gene vgll3, the known obesity gene mc4r, and major histocompatibility complex II. Most strikingly, we confirmed a genomic region on Ssa09 that was extremely differentiated among subpopulations and that is also a candidate for local selection over the global range of Atlantic salmon. This region colocalized with a haplotype strongly associated with spawning ecotype in sockeye salmon (Oncorhynchus nerka), with circumstantial evidence that the same gene (six6) may be the selective target in both cases. The phenotypic effect of this region in Atlantic salmon remains cryptic, although allelic variation is related to upstream catchment area and covaries with timing of the return spawning migration. Our results further inform management of Atlantic salmon and open multiple avenues for future research.     

Genome‐wide signature of local adaptation linked to variable CpG methylation in oak populations

It has long been known that adaptive evolution can occur through genetic mutations in DNA sequence, but it is unclear whether adaptive evolution can occur through analogous epigenetic mechanisms, such as through DNA methylation. If epigenetic variation contributes directly to evolution, species under threat of disease, invasive competition, climate change or other stresses would have greater stores of variation from which to draw. We looked for evidence of natural selection acting on variably methylated DNA sites using population genomic analysis across three climatologically distinct populations of valley oaks. We found patterns of genetic and epigenetic differentiations that indicate local adaptation is operating on large portions of the oak genome. While CHG methyl polymorphisms are not playing a significant role and would make poor targets for natural selection, our findings suggest that CpG methyl polymorphisms as a whole are involved in local adaptation, either directly or through linkage to regions under selection.     

Genome‐wide selection components analysis in a fish with male pregnancy

A major goal of evolutionary biology is to identify the genome‐level targets of natural and sexual selection. With the advent of next‐generation sequencing, whole‐genome selection components analysis provides a promising avenue in the search for loci affected by selection in nature. Here, we implement a genome‐wide selection components analysis in the sex role reversed Gulf pipefish, Syngnathus scovelli. Our approach involves a double‐digest restriction‐site associated DNA sequencing (ddRAD‐seq) technique, applied to adult females, nonpregnant males, pregnant males, and their offspring. An F_ST comparison of allele frequencies among these groups reveals 47 genomic regions putatively experiencing sexual selection, as well as 468 regions showing a signature of differential viability selection between males and females. A complementary likelihood ratio test identifies similar patterns in the data as the F_ST analysis. Sexual selection and viability selection both tend to favor the rare alleles in the population. Ultimately, we conclude that genome‐wide selection components analysis can be a useful tool to complement other approaches in the effort to pinpoint genome‐level targets of selection in the wild.     

Genome‐wide evidence for divergent selection between populations of a major agricultural pathogen

The genetic and environmental homogeneity in agricultural ecosystems is thought to impose strong and uniform selection pressures. However, the impact of this selection on plant pathogen genomes remains largely unknown. We aimed to identify the proportion of the genome and the specific gene functions under positive selection in populations of the fungal wheat pathogen Zymoseptoria tritici. First, we performed genome scans in four field populations that were sampled from different continents and on distinct wheat cultivars to test which genomic regions are under recent selection. Based on extended haplotype homozygosity and composite likelihood ratio tests, we identified 384 and 81 selective sweeps affecting 4% and 0.5% of the 35 Mb core genome, respectively. We found differences both in the number and the position of selective sweeps across the genome between populations. Using a XtX‐based outlier detection approach, we identified 51 extremely divergent genomic regions between the allopatric populations, suggesting that divergent selection led to locally adapted pathogen populations. We performed an outlier detection analysis between two sympatric populations infecting two different wheat cultivars to identify evidence for host‐driven selection. Selective sweep regions harboured genes that are likely to play a role in successfully establishing host infections. We also identified secondary metabolite gene clusters and an enrichment in genes encoding transporter and protein localization functions. The latter gene functions mediate responses to environmental stress, including interactions with the host. The distinct gene functions under selection indicate that both local host genotypes and abiotic factors contributed to local adaptation.     

Genome‐wide selection footprints and deleterious variations in young Asian allotetraploid rapeseed

Brassica napus (AACC, 2n = 38) is an important oilseed crop grown worldwide. However, little is known about the population evolution of this species, the genomic difference between its major genetic groups, such as European and Asian rapeseed, and the impacts of historical large‐scale introgression events on this young tetraploid. In this study, we reported the de novo assembly of the genome sequences of an Asian rapeseed (B. napus), Ningyou 7, and its four progenitors and compared these genomes with other available genomic data from diverse European and Asian cultivars. Our results showed that Asian rapeseed originally derived from European rapeseed but subsequently significantly diverged, with rapid genome differentiation after hybridization and intensive local selective breeding. The first historical introgression of B. rapa dramatically broadened the allelic pool but decreased the deleterious variations of Asian rapeseed. The second historical introgression of the double‐low traits of European rapeseed (canola) has reshaped Asian rapeseed into two groups (double‐low and double‐high), accompanied by an increase in genetic load in the double‐low group. This study demonstrates distinctive genomic footprints and deleterious SNP (single nucleotide polymorphism) variants for local adaptation by recent intra‐ and interspecies introgression events and provides novel insights for understanding the rapid genome evolution of a young allopolyploid crop.     

Genome‐wide analyses suggest parallel selection for universal traits may eclipse local environmental selection in a highly mobile carnivore

Ecological and environmental heterogeneity can produce genetic differentiation in highly mobile species. Accordingly, local adaptation may be expected across comparatively short distances in the presence of marked environmental gradients. Within the European continent, wolves (Canis lupus) exhibit distinct north–south population differentiation. We investigated more than 67‐K single nucleotide polymorphism (SNP) loci for signatures of local adaptation in 59 unrelated wolves from four previously identified population clusters (northcentral Europe n = 32, Carpathian Mountains n = 7, Dinaric‐Balkan n = 9, Ukrainian Steppe n = 11). Our analyses combined identification of outlier loci with findings from genome‐wide association study of individual genomic profiles and 12 environmental variables. We identified 353 candidate SNP loci. We examined the SNP position and neighboring megabase (1 Mb, one million bases) regions in the dog (C. lupus familiaris) genome for genes potentially under selection, including homologue genes in other vertebrates. These regions included functional genes for, for example, temperature regulation that may indicate local adaptation and genes controlling for functions universally important for wolves, including olfaction, hearing, vision, and cognitive functions. We also observed strong outliers not associated with any of the investigated variables, which could suggest selective pressures associated with other unmeasured environmental variables and/or demographic factors. These patterns are further supported by the examination of spatial distributions of the SNPs associated with universally important traits, which typically show marked differences in allele frequencies among population clusters. Accordingly, parallel selection for features important to all wolves may eclipse local environmental selection and implies long‐term separation among population clusters.     

A genome‐wide scan for signatures of recent selection in Holstein cattle

The data from the newly available 50 K SNP chip was used for tagging the genome‐wide footprints of positive selection in Holstein–Friesian cattle. For this purpose, we employed the recently described Extended Haplotype Homozygosity test, which detects selection by measuring the characteristics of haplotypes within a single population. To assess formally the significance of these results, we compared the combination of frequency and the Relative Extended Haplotype Homozygosity value of each core haplotype with equally frequent haplotypes across the genome. A subset of the putative regions showing the highest significance in the genome‐wide EHH tests was mapped. We annotated genes to identify possible influence they have in beneficial traits by using the Gene Ontology database. A panel of genes, including FABP3, CLPN3, SPERT, HTR2A5, ABCE1, BMP4 and PTGER2, was detected, which overlapped with the most extreme P‐values. This panel comprises some interesting candidate genes and QTL, representing a broad range of economically important traits such as milk yield and composition, as well as reproductive and behavioural traits. We also report high values of linkage disequilibrium and a slower decay of haplotype homozygosity for some candidate regions harbouring major genes related to dairy quality. The results of this study provide a genome‐wide map of selection footprints in the Holstein genome, and can be used to better understand the mechanisms of selection in dairy cattle breeding.     

A resource of genome‐wide single‐nucleotide polymorphisms generated by RAD tag sequencing in the critically endangered European eel

Reduced representation genome sequencing such as restriction‐site‐associated DNA (RAD) sequencing is finding increased use to identify and genotype large numbers of single‐nucleotide polymorphisms (SNPs) in model and nonmodel species. We generated a unique resource of novel SNP markers for the European eel using the RAD sequencing approach that was simultaneously identified and scored in a genome‐wide scan of 30 individuals. Whereas genomic resources are increasingly becoming available for this species, including the recent release of a draft genome, no genome‐wide set of SNP markers was available until now. The generated SNPs were widely distributed across the eel genome, aligning to 4779 different contigs and 19 703 different scaffolds. Significant variation was identified, with an average nucleotide diversity of 0.00529 across individuals. Results varied widely across the genome, ranging from 0.00048 to 0.00737 per locus. Based on the average nucleotide diversity across all loci, long‐term effective population size was estimated to range between 132 000 and 1 320 000, which is much higher than previous estimates based on microsatellite loci. The generated SNP resource consisting of 82 425 loci and 376 918 associated SNPs provides a valuable tool for future population genetics and genomics studies and allows for targeting specific genes and particularly interesting regions of the eel genome.     

Both life‐history plasticity and local adaptation will shape range‐wide responses to climate warming in the tundra plant Silene acaulis

Many predictions of how climate change will impact biodiversity have focused on range shifts using species‐wide climate tolerances, an approach that ignores the demographic mechanisms that enable species to attain broad geographic distributions. But these mechanisms matter, as responses to climate change could fundamentally differ depending on the contributions of life‐history plasticity vs. local adaptation to species‐wide climate tolerances. In particular, if local adaptation to climate is strong, populations across a species’ range—not only those at the trailing range edge—could decline sharply with global climate change. Indeed, faster rates of climate change in many high latitude regions could combine with local adaptation to generate sharper declines well away from trailing edges. Combining 15 years of demographic data from field populations across North America with growth chamber warming experiments, we show that growth and survival in a widespread tundra plant show compensatory responses to warming throughout the species’ latitudinal range, buffering overall performance across a range of temperatures. However, populations also differ in their temperature responses, consistent with adaptation to local climate, especially growing season temperature. In particular, warming begins to negatively impact plant growth at cooler temperatures for plants from colder, northern populations than for those from warmer, southern populations, both in the field and in growth chambers. Furthermore, the individuals and maternal families with the fastest growth also have the lowest water use efficiency at all temperatures, suggesting that a trade‐off between growth and water use efficiency could further constrain responses to forecasted warming and drying. Taken together, these results suggest that populations throughout species’ ranges could be at risk of decline with continued climate change, and that the focus on trailing edge populations risks overlooking the largest potential impacts of climate change on species’ abundance and distribution.     

A genome‐wide scan for selection signatures in Nellore cattle

Brazilian Nellore cattle (Bos indicus) have been selected for growth traits for over more than four decades. In recent years, reproductive and meat quality traits have become more important because of increasing consumption, exports and consumer demand. The identification of genome regions altered by artificial selection can potentially permit a better understanding of the biology of specific phenotypes that are useful for the development of tools designed to increase selection efficiency. Therefore, the aims of this study were to detect evidence of recent selection signatures in Nellore cattle using extended haplotype homozygosity methodology and BovineHD marker genotypes (>777 000 single nucleotide polymorphisms) as well as to identify corresponding genes underlying these signals. Thirty‐one significant regions (P < 0.0001) of possible recent selection signatures were detected, and 19 of these overlapped quantitative trait loci related to reproductive traits, growth, feed efficiency, meat quality, fatty acid profiles and immunity. In addition, 545 genes were identified in regions harboring selection signatures. Within this group, 58 genes were associated with growth, muscle and adipose tissue metabolism, reproductive traits or the immune system. Using relative extended haplotype homozygosity to analyze high‐density single nucleotide polymorphism marker data allowed for the identification of regions potentially under artificial selection pressure in the Nellore genome, which might be used to better understand autozygosity and the effects of selection on the Nellore genome.     

Genomic signatures of local adaptation in the Drosophila immune response

As environments and pathogen landscapes shift, host defenses must evolve to remain effective. Due to this selection pressure, among-species comparisons of genetic sequence data often find immune genes to be among the fastest evolving genes across the genome. The full extent and nature of these immune adaptations, however, remain largely unexplored. In a recent study, we analyzed patterns of selection within distinct components of the Drosophila melanogaster immune pathway. While we found evidence of positive selection within some immune processes, immune genes were not universally characterized by signatures of strong selection. On the contrary, we even found that some immune functions show greater than expected constraint. Overall these results highlight 2 major factors that appear to play an outsize role in determining a gene's evolutionary rate: the type of pathogen the gene targets and the gene's position within the immune network. These results join a growing body of literature that highlight the complexity of immune adaptation. Rather than there being uniformly strong selection across all immune genes, a combination of pathogen-specificity and host genetic constraints appear to play key roles in determining each immune gene's individual evolutionary trajectory.     

Genome‐wide DNA methylation signatures of infection status in Trinidadian guppies (Poecilia reticulata)

Epigenetic modification, especially DNA methylation, can play an important role in mediating gene regulatory response to environmental stressors and may be a key process affecting phenotypic plasticity and adaptation. Parasites are potent stressors with profound physiological and ecological effects on their hosts, yet it remains unclear how parasites influence host methylation patterns. Here, we used a well‐studied host–parasite system, the guppy Poecilia reticulata and its ectoparasitic monogenean Gyrodactylus turnbulli to gain mechanistic insight into the dynamics of DNA methylation in host–parasite interactions. To explore this, we quantitatively measured genome‐wide DNA methylation in guppy skin tissue using reduced representation bisulphite sequencing and characterized differential methylation patterns in guppies during distinct phases of infection. We identified 365, 313, and 741 differentially methylated regions (DMRs) between infected and control fish in early infection, peak infection and recovery phases, respectively. The magnitude of the methylation difference was moderate in DMRs, with an average of 29% (early infection), 27% (peak infection) and 30% (recovery) differential methylation per DMR. Approximately 50% of DMRs overlapped with CpG islands, and over half of the DMRs overlapped with gene bodies, several of which encode proteins relevant to immune response. These findings provide the first evidence of an epigenetic signature of infection by ectoparasites and demonstrate the changing relationship between epigenetic variation and immune response in distinct phases of infection.     

Genome‐wide mosaicism in divergence between zoonotic malaria parasite subpopulations with separate sympatric transmission cycles

Plasmodium knowlesi is a significant cause of human malaria transmitted as a zoonosis from macaque reservoir hosts in South‐East Asia. Microsatellite genotyping has indicated that human infections in Malaysian Borneo are an admixture of two highly divergent sympatric parasite subpopulations that are, respectively, associated with long‐tailed macaques (Cluster 1) and pig‐tailed macaques (Cluster 2). Whole‐genome sequences of clinical isolates subsequently confirmed the separate clusters, although fewer of the less common Cluster 2 type were sequenced. Here, to analyse population structure and genomic divergence in subpopulation samples of comparable depth, genome sequences were generated from 21 new clinical infections identified as Cluster 2 by microsatellite analysis, yielding a cumulative sample size for this subpopulation similar to that for Cluster 1. Profound heterogeneity in the level of intercluster divergence was distributed across the genome, with long contiguous chromosomal blocks having high or low divergence. Different mitochondrial genome clades were associated with the two major subpopulations, but limited exchange of haplotypes from one to the other was evident, as was also the case for the maternally inherited apicoplast genome. These findings indicate deep divergence of the two sympatric P. knowlesi subpopulations, with introgression likely to have occurred recently. There is no evidence yet of specific adaptation at any introgressed locus, but the recombinant mosaic types offer enhanced diversity on which selection may operate in a currently changing landscape and human environment. Loci responsible for maintaining genetic isolation of the sympatric subpopulations need to be identified in the chromosomal regions showing fixed differences.