Teasing apart the joint effect of demography and natural selection in the birth of a contact zone

Vast population movements induced by recurrent climatic cycles have shaped the genetic structure of plant species. This is especially true in Scandinavia that was repeatedly glaciated. During glacial periods trees were confined to refugia, south and east of the ice sheet, from which they recolonized Scandinavia as the ice melted away. This multi-pronged recolonization led to large contact zones in most species. We leverage large genomic data from 5000 trees to reconstruct the demographic history of Norway spruce (Picea abies) and test for the presence of natural selection during the recolonization process and the establishment of the contact zone. Sweden is today made up of two large genetic clusters, a southern one originating from the Baltics and a Northern one originating from Northern Russia. The contact zone delineating these two clusters closely matches the limit between two major climatic regions. This suggests that natural selection contributed to the establishment and the maintenance of the contact zone. To test this hypothesis we first used Approximate Bayesian Computation; an Isolation-with migration model with genomewide linked selection fits the data better than a purely neutral one. Secondly, we identified loci characterized by both extreme allele frequency differences between geographic regions and association to the variables defining the climatic zones. These loci, many of which are related to phenology, form clusters present on all linkage groups. Altogether, the current genetic structure reflects the joint effect of climatic cycles, recolonization and selection on the establishment of strong local adaptation and con-tact zones.

Differential sensory and immune gene evolution in sea turtles with contrasting demographic and life histories

Marine turtles represent an ancient lineage of marine vertebrates that evolved from terrestrial ancestors over 100 MYA, yet the genomic basis of the unique physiological and ecological traits enabling these species to thrive in diverse marine habitats remain largely unknown. Additionally, many populations have declined drastically due to anthropogenic activities over the past two centuries, and their recovery is a high global conservation priority. We generated and analyzed high-quality reference genomes for green (Chelonia mydas) and leatherback (Dermochelys coriacea) turtles, representing the two extant marine turtle families (MRCA ~60 MYA). Generally, these genomes are highly syntenic and homologous. Non-collinearity was associated with higher copy numbers of immune, zinc-finger, or olfactory receptor (OR) genes in green turtles. Gene family analyses suggested that ORs related to waterborne odorants have expanded in green turtles and contracted in leatherbacks, which may underlie immunological and sensory adaptations assisting navigation and occupancy of neritic versus pelagic environments, and diet specialization. Microchromosomes showed reduced collinearity, and greater gene content, heterozygosity, and genetic distances between species, supporting their critical role in vertebrate evolutionary adaptation. Finally, demographic history and diversity analyses showed stark contrasts between species, indicating that leatherback turtles have had a low yet stable effective population size, extremely low diversity when compared to other reptiles, and a higher proportion of deleterious variants, reinforcing concern over the persistence of this species under future climate scenarios. These highly contiguous genomes provide invaluable resources for advancing our understanding of evolution and conservation best practices in an imperiled vertebrate lineage.

Contrasting whole-genome and reduced representation sequencing for population demographic inference: an alpine mammal example

Genomic approaches to the study of population demography rely on accurate SNP calling and by-proxy the site frequency spectrum (SFS). Two main questions for the design of such studies remain poorly investigated: do reduced genomic sequencing summary statistics reflect that of whole genome, and how do sequencing strategies and derived summary statistics impact demographic inferences? To address those questions, we applied the ddRAD sequencing approach to 254 individuals and whole genome resequencing approach to 35 mountain goat (Oreamnos americanus) individuals across the species range with a known demographic history. We identified SNPs with 5 different variant callers and used ANGSD to estimate the genotype likelihoods (GLs). We tested combinations of SNP filtering by linkage disequilibrium (LD), minor allele frequency (MAF) and the genomic region. We compared the resulting suite of summary statistics reflective of the SFS and quantified the relationship to demographic inferences by estimating the contemporary effective population size (Ne), isolation-by-distance and population structure, FST, and explicit modelling of the demographic history with δaδi. Filtering had a larger effect than sequencing strategy, with the former strongly influencing summary statistics. Estimates of contemporary Ne and isolation-by-distance patterns were largely robust to the choice of sequencing, pipeline, and filtering. Despite the high variance in summary statistics, whole genome and reduced representation approaches were overall similar in supporting a glacial induced vicariance and low Ne in mountain goats. We discuss why whole genome resequencing data is preferable, and reiterate support the use of GLs, in part because it limits user-determined filters.

Demographic history and conservation genomics of caribou (Rangifer tarandus) in Québec

The loss of genetic diversity is a challenge many species are facing, and genomics is a potential tool that can inform and prioritize decision making. Caribou populations have experienced significant recent declines throughout Québec, Canada, and some are considered threatened or endangered. We calculated the ancestral and contemporary patterns of genomic diversity of five caribou populations and applied a comparative framework to assess the interplay between demography and genomic diversity. We calculated a caribou specific mutation rate, μ, by extracting orthologous genes from related ungulates. Whole genome re-sequencing was completed on 67 caribou and genotype likelihoods were estimated. We calculated nucleotide diversity, θπ and estimated the coalescent or ancestral Ne, which ranged from 12,030 to 15,513. When compared to the census size, NC, the endangered Gaspésie Mountain caribou population had the highest Ne:NC ratio which is consistent with recent work suggesting high ancestral Ne:NC is of conservation concern. These ratios were highly correlated with genomic signatures (i.e. Tajima’s D) and explicit demographic model parameters. Values of contemporary Ne, estimated from linkage-disequilibrium, ranged from 11 to 162, with Gaspésie having among the highest contemporary Ne:NC ratio. Importantly, conservation genetics theory would predict this population to be of less concern based on this ratio. Of note, F varied only slightly between populations, and runs of homozygosity were not abundant in the genome. Our study highlights how genomic patterns are nuanced and misleading if viewed only through a contemporary lens; a holistic view should integrate ancestral Ne and Tajima’s D into conservation decisions.

Imputation Performance in Latin American Populations: Improving Rare Variants Representation With the Inclusion of Native American Genomes

Current Genome-Wide Association Studies (GWAS) rely on genotype imputation to increase statistical power, improve fine-mapping of association signals, and facilitate meta-analyses. Due to the complex demographic history of Latin America and the lack of balanced representation of Native American genomes in current imputation panels, the discovery of locally relevant disease variants is likely to be missed, limiting the scope and impact of biomedical research in these populations. Therefore, the necessity of better diversity representation in genomic databases is a scientific imperative. Here, we expand the 1,000 Genomes reference panel (1KGP) with 134 Native American genomes (1KGP + NAT) to assess imputation performance in Latin American individuals of mixed ancestry. Our panel increased the number of SNPs above the GWAS quality threshold, thus improving statistical power for association studies in the region. It also increased imputation accuracy, particularly in low-frequency variants segregating in Native American ancestry tracts. The improvement is subtle but consistent across countries and proportional to the number of genomes added from local source populations. To project the potential improvement with a higher number of reference genomes, we performed simulations and found that at least 3,000 Native American genomes are needed to equal the imputation performance of variants in European ancestry tracts. This reflects the concerning imbalance of diversity in current references and highlights the contribution of our work to reducing it while complementing efforts to improve global equity in genomic research.

Comparison of Genotype Imputation for SNP Array and Low-Coverage Whole-Genome Sequencing Data

Genotype imputation is the term used to describe the process of inferring unobserved genotypes in a sample of individuals. It is a key step prior to a genome-wide association study (GWAS) or genomic prediction. The imputation accuracy will directly influence the results from subsequent analyses. In this simulation-based study, we investigate the accuracy of genotype imputation in relation to some factors characterizing SNP chip or low-coverage whole-genome sequencing (LCWGS) data. The factors included the imputation reference population size, the proportion of target markers /SNP density, the genetic relationship (distance) between the target population and the reference population, and the imputation method. Simulations of genotypes were based on coalescence theory accounting for the demographic history of pigs. A population of simulated founders diverged to produce four separate but related populations of descendants. The genomic data of 20,000 individuals were simulated for a 10-Mb chromosome fragment. Our results showed that the proportion of target markers or SNP density was the most critical factor affecting imputation accuracy under all imputation situations. Compared with Minimac4, Beagle5.1 reproduced higher-accuracy imputed data in most cases, more notably when imputing from the LCWGS data. Compared with SNP chip data, LCWGS provided more accurate genotype imputation. Our findings provided a relatively comprehensive insight into the accuracy of genotype imputation in a realistic population of domestic animals.

Demographic history and range modelling of the East Mediterranean Abies cilicica

The Mediterranean Basin is one of the 36 global hotspots of biodiversity and it is rich in endemic tree species. The complex geological history of the region throughout the Neogene and Quaternary periods that were marked with several palaeoclimatic transformations was a major factor triggering the genetic divergence of lineages in tree species in the region. The ongoing global climate change is the main factor threatening Mediterranean biodiversity. The risk of population decline related to aridization is the highest in the case of endemics, especially for cold-adapted conifers, such as Abies cilicica. The Cilician fir grows in the East Mediterranean mountains that constitute a local centre of endemism within the region. The species range is fragmented and small-size populations prevail. Previous studies have suggested that the last glacial cycle led to a significant reduction in the species range and might have initiated genetic divergence. As a result, two lineages are currently recognized at the subspecies level, A. cilicica subsp. isaurica (Turkey) and A. cilicica subsp. cilicica (Turkey, Syria, and Lebanon). The predictions about the impact of future climate changes in the East Mediterranean suggest a profound reduction of precipitation and overall warming that may put the remnant populations of A. cilicica at a risk of decline. Here, we used the Bayesian approach to investigate the demographic history of endemic A. cilicica. Specifically, we estimated the probable time of the intraspecies divergence to verify previous assumptions about the species’ evolutionary history. Additionally, niche modelling was used to outline the potential range of changes in the past and to indicate glacial refugia in where the species persisted climate crisis. This approach was also used to explore the possible influence of the future climate changes on the distribution of A. cilicica in the region. Our results demonstrate that the divergence between the Lebanese and the Turkish populations that occurred ~220 ka years BP coincided with the Riss glaciation. According to palaeoecological data, in the East Mediterranean, that glacial period caused a severe reduction in the populations of woody species due to the aridity of the climate. At that time, the Lebanese-Syrian part of the range was likely disconnected from the main range. The second split was induced by the last glacial cycle ~60 ka years BP and led to the separation of the Central Taurus and East Taurus population and, consequently, to the formation of the two subspecies. Niche modelling for the last glacial maximum has allowed us to locate the probable refugia for A. cilicica in the western Anatolia and Syria-Lebanon area. A projection of the future possible distribution of the species indicates a serious reduction of the range during this century.