We carried out whole genome resequencing of 127 chicken including red jungle fowl and multiple populations of commercial broilers and layers to perform a systematic screening of adaptive changes in modern chicken (Gallus gallus domesticus). We uncovered >21 million high quality SNPs of which 34% are newly detected variants. This panel comprises >115,000 predicted amino-acid altering substitutions as well as 1,100 SNPs predicted to be stop-gain or -loss, several of which reach high frequencies. Signatures of selection were investigated both through analyses of fixation and differentiation to reveal selective sweeps that may have had prominent roles during domestication and breed development. Contrasting wild and domestic chicken we confirmed selection at the BCO2 and TSHR loci and identified 34 putative sweeps co-localized with ALX1, KITLG, EPGR, IGF1, DLK1, JPT2, CRAMP1, and GLI3, among others. Analysis of enrichment between groups of wild vs. commercials and broilers vs. layers revealed a further panel of candidate genes including CORIN, SKIV2L2 implicated in pigmentation and LEPR, MEGF10 and SPEF2, suggestive of production-oriented selection. SNPs with marked allele frequency differences between wild and domestic chicken showed a highly significant deficiency in the proportion of amino-acid altering mutations (P<2.5×10⁻⁶). The results contribute to the understanding of major genetic changes that took place during the evolution of modern chickens and in poultry breeding. Domestic chickens (Gallus gallus domesticus) provide a critical resource for animal proteins for human nutrition worldwide. Chickens were primarily domesticated from the red jungle fowl (Gallus gallus gallus), a bird that still runs wild in most of Southeast Asia. Human driven selection during domestication and subsequent specialization into meat type (broilers) and egg layer (layers) birds has left detectable signatures of selection within the genome of modern chicken. In this study, we performed whole genome sequencing of 127 chicken including the red jungle fowl and multiple populations of commercial broilers and layers to perform a systematic screening of adaptive changes in modern chicken. Analysis of selection provided a comprehensive list of several tens of independent loci that are likely to have contributed to domestication or improving production. SNP by SNP comparison of allele frequency between groups of wild and domestic chicken showed a highly significant deficiency of the proportion of amino acid altering mutations. This implies that commercial birds have undergone purifying selection reducing the frequency of deleterious variants.

Since domestication, chickens did not only disperse into the different parts of the world but they have also undergone significant genomic changes in this process. Many breeds, strains or lines have been formed and those represent the diversity of the species. However, other than the natural evolutionary forces, management practices (including those that threaten the persistence of genetic diversity) following domestication have shaped the genetic make-up of and diversity between today’s chicken breeds. As part of the SYNBREED project, samples from a wide variety of chicken populations have been collected across the globe and were genotyped with a high density SNP array. The panel consists of the wild type, commercial layers and broilers, indigenous village/local type and fancy chicken breeds. The SYNBREED chicken diversity panel (SCDP) is made available to serve as a public basis to study the genetic structure of chicken diversity. In the current study we analyzed the genetic diversity between and within the populations in the SCDP, which is important for making informed decisions for effective management of farm animal genetic resources. Many of the fancy breeds cover a wide spectrum and clustered with other breeds of similar supposed origin as shown by the phylogenetic tree and principal component analysis. However, the fancy breeds as well as the highly selected commercial layer lines have reduced genetic diversity within the population, with the average observed heterozygosity estimates lower than 0.205 across their breeds’ categories and the average proportion of polymorphic loci lower than 0.680. We show that there is still a lot of genetic diversity preserved within the wild and less selected African, South American and some local Asian and European breeds with the average observed heterozygosity greater than 0.225 and the average proportion of polymorphic loci larger than 0.720 within their breeds’ categories. It is important that such highly diverse breeds are maintained for the sustainability and flexibility of future chicken breeding. This diversity panel provides opportunities for exploitation for further chicken molecular genetic studies. With the possibility to further expand, it constitutes a very useful community resource for chicken genetic diversity research.

Single nucleotide polymorphisms (SNPs), genotyped with arrays, have become a widely used marker type in population genetic analyses over the last 10 years. However, compared to whole genome re-sequencing data, arrays are known to lack a substantial proportion of globally rare variants and tend to be biased towards variants present in populations involved in the development process of the respective array. This affects population genetic estimators and is known as SNP ascertainment bias. We investigated factors contributing to ascertainment bias in array development by redesigning the Axiom^™Genome-Wide Chicken Arrayin silicoand evaluating changes in allele frequency spectra and heterozygosity estimates in a stepwise manner. A sequential reduction of rare alleles during the development process was shown. This was mainly caused by the identification of SNPs in a limited set of populations and a within-population selection of common SNPs when aiming for equidistant spacing. These effects were shown to be less severe with a larger discovery panel. Additionally, a generally massive overestimation of expected heterozygosity for the ascertained SNP sets was shown. This overestimation was 24% higher for populations involved in the discovery process than not involved populations in case of the original array. The same was observed after the SNP discovery step in the redesign. However, an unequal contribution of populations during the SNP selection can mask this effect but also adds uncertainty. Finally, we make suggestions for the design of specialized arrays for large scale projects where whole genome re-sequencing techniques are still too expensive.

Single nucleotide polymorphism (SNP) panels have been widely used to study genomic variations within and between populations. Methods of SNP discovery have been a matter of debate for their potential of introducing ascertainment bias, and genetic diversity results obtained from the SNP genotype data can be misleading. We used a total of 42 chicken populations where both individual genotyped array data and pool whole genome resequencing (WGS) data were available. We compared allele frequency distributions and genetic diversity measures (expected heterozygosity (H e ), fixation index (F ST ) values, genetic distances and principal components analysis (PCA)) between the two data types. With the array data, we applied different filtering options (SNPs polymorphic in samples of two Gallus gallus wild populations, linkage disequilibrium (LD) based pruning and minor allele frequency (MAF) filtering, and combinations thereof) to assess their potential to mitigate the ascertainment bias. Rare SNPs were underrepresented in the array data. Array data consistently overestimated H e compared to WGS data, however, with a similar ranking of the breeds, as demonstrated by Spearman’s rank correlations ranging between 0.956 and 0.985. LD based pruning resulted in a reduced overestimation of H e compared to the other filters and slightly improved the relationship with the WGS results. The raw array data and those with polymorphic SNPs in the wild samples underestimated pairwise F ST values between breeds which had low F ST (0.15). LD based pruned data underestimated F ST in a consistent manner. The genetic distance matrix from LD pruned data was more closely related to that of WGS than the other array versions. PCA was rather robust in all array versions, since the population structure on the PCA plot was generally well captured in comparison to the WGS data. Among the tested filtering strategies, LD based pruning was found to account for the effects of ascertainment bias in the relatively best way, producing results which are most comparable to those obtained from WGS data and therefore is recommended for practical use.

Global climate change is increasing the magnitude of environmental stressors, such as temperature, pathogens, and drought, that limit the survivability and sustainability of livestock production. Poultry production and its expansion is dependent upon robust animals that are able to cope with stressors in multiple environments. Understanding the genetic strategies that indigenous, noncommercial breeds have evolved to survive in their environment could help to elucidate molecular mechanisms underlying biological traits of environmental adaptation. We examined poultry from diverse breeds and climates of Africa and Northern Europe for selection signatures that have allowed them to adapt to their indigenous environments. Selection signatures were studied using a combination of population genomic methods that employed F_ST, integrated haplotype score (iHS), and runs of homozygosity (ROH) procedures. All the analyses indicated differences in environment as a driver of selective pressure in both groups of populations. The analyses revealed unique differences in the genomic regions under selection pressure from the environment for each population. The African chickens showed stronger selection toward stress signaling and angiogenesis, while the Northern European chickens showed more selection pressure toward processes related to energy homeostasis. The results suggest that chromosomes 2 and 27 are the most diverged between populations and the most selected upon within the African (chromosome 27) and Northern European (chromosome 2) birds. Examination of the divergent populations has provided new insight into genes under possible selection related to tolerance of a population’s indigenous environment that may be baselines for examining the genomic contribution to tolerance adaptions.