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.

Genomic Signatures of Domestication Selection in the Australasian Snapper (Chrysophrys auratus)

Domestication of teleost fish is a recent development, and in most cases started less than 50 years ago. Shedding light on the genomic changes in key economic traits during the domestication process can provide crucial insights into the evolutionary processes involved and help inform selective breeding programmes. Here we report on the recent domestication of a native marine teleost species in New Zealand, the Australasian snapper (Chrysophrys auratus). Specifically, we use genome-wide data from a three-generation pedigree of this species to uncover genetic signatures of domestication selection for growth. Genotyping-By-Sequencing (GBS) was used to generate genome-wide SNP data from a three-generation pedigree to calculate generation-wide averages of FST between every generation pair. The level of differentiation between generations was further investigated using ADMIXTURE analysis and Principal Component Analysis (PCA). After that, genome scans using Bayescan, LFMM and XP-EHH were applied to identify SNP variants under putative selection following selection for growth. Finally, genes near candidate SNP variants were annotated to gain functional insights. Analysis showed that between generations FST values slightly increased as generational time increased. The extent of these changes was small, and both ADMIXTURE analysis and PCA were unable to form clear clusters. Genome scans revealed a number of SNP outliers, indicative of selection, of which a small number overlapped across analyses methods and populations. Genes of interest within proximity of putative selective SNPs were related to biological functions, and revealed an association with growth, immunity, neural development and behaviour, and tumour repression. Even though few genes overlapped between outlier SNP methods, gene functionalities showed greater overlap between methods. While the genetic changes observed were small in most cases, a number of outlier SNPs could be identified, of which some were found by more than one method. Multiple outlier SNPs appeared to be predominately linked to gene functionalities that modulate growth and survival. Ultimately, the results help to shed light on the genomic changes occurring during the early stages of domestication selection in teleost fish species such as snapper, and will provide useful candidates for the ongoing selective breeding in the future of this and related species.

Comparing genome scans among species of the stickleback order reveals three different patterns of genetic diversity

Comparing genome scans among species is a powerful approach for investigating the patterns left by evolutionary processes. In particular, this offers a way to detect candidate genes that drive convergent evolution. We compared genome scan results to investigate if patterns of genetic diversity and divergence are shared among divergent species within the stickleback order (Gasterosteiformes): the threespine stickleback (Gasterosteus aculeatus), ninespine stickleback (Pungitius pungitus) and tubesnout (Aulorhynchus flavidus). Populations were sampled from the southern and northern edges of each species’ range, to identify patterns associated with latitudinal changes in genetic diversity. Weak correlations in genetic diversity (F and expected heterozygosity) and three different patterns in the genomic landscape were found among these species. Additionally, no candidate genes for convergent evolution were detected. This is a counterexample to the growing number of studies that have shown overlapping genetic patterns, demonstrating that genome scan comparisons can be noisy due to the effects of several interacting evolutionary forces.

Genome scans of facial features in East Africans and cross-population comparisons reveal novel associations

Facial morphology is highly variable, both within and among human populations, and a sizable portion of this variation is attributable to genetics. Previous genome scans have revealed more than 100 genetic loci associated with different aspects of normal-range facial variation. Most of these loci have been detected in Europeans, with few studies focusing on other ancestral groups. Consequently, the degree to which facial traits share a common genetic basis across diverse sets of humans remains largely unknown. We therefore investigated the genetic basis of facial morphology in an East African cohort. We applied an open-ended data-driven phenotyping approach to a sample of 2,595 3D facial images collected on Tanzanian children. This approach segments the face into hierarchically arranged, multivariate features that capture the shape variation after adjusting for age, sex, height, weight, facial size and population stratification. Genome scans of these multivariate shape phenotypes revealed significant (p < 2.5 × 10−8) signals at 20 loci, which were enriched for active chromatin elements in human cranial neural crest cells and embryonic craniofacial tissue, consistent with an early developmental origin of the facial variation. Two of these associations were in highly conserved regions showing craniofacial-specific enhancer activity during embryological development (5q31.1 and 12q21.31). Six of the 20 loci surpassed a stricter threshold accounting for multiple phenotypes with study-wide significance (p < 6.25 × 10−10). Cross-population comparisons indicated 10 association signals were shared with Europeans (seven sharing the same associated SNP), and facilitated fine-mapping of causal variants at previously reported loci. Taken together, these results may point to both shared and population-specific components to the genetic architecture of facial variation.

Genes and pathways associated with pregnancy loss in dairy cattle

Pregnancy loss directly impairs reproductive performance in dairy cattle. Here, we investigated genetic factors associated with pregnancy loss following detection of a viable embryo around 42 days of gestation. The objectives of this study were to perform whole-genome scans and subsequent gene-set analyses for identifying candidate genes, functional gene-sets and gene signaling pathways implicated in pregnancy loss in US Holstein cows. Data consisted of about 58,000 pregnancy/abortion records distributed over nulliparous, primiparous, and multiparous cows. Threshold models were used to assess the binary response of pregnancy loss. Whole‐genome scans identified at least seven genomic regions on BTA2, BTA10, BTA14, BTA16, BTA21, BTA24 and BTA29 associated with pregnancy loss in heifers and lactating cows. These regions harbor several candidate genes that are directly implicated in pregnancy maintenance and fetal growth, such as CHST14, IGF1R, IGF2, PSEN2, SLC2A5 and WNT4. Moreover, the enrichment analysis revealed at least seven significantly enriched processes, containing genes associated with pregnancy loss, including calcium signaling, cell–cell attachment, cellular proliferation, fetal development, immunity, membrane permeability, and steroid metabolism. Additionally, the pathway analysis revealed a number of significant gene signaling pathways that regulate placental development and fetal growth, including Wnt, Hedgehog, Notch, MAPK, Hippo, mTOR and TGFβ pathways. Overall, our findings contribute to a better understanding of the genetic and biological basis of pregnancy loss in dairy cattle and points out novel strategies for improving pregnancy maintenance via marker‐assisted breeding.

Rapid parallel adaptation despite gene flow in silent crickets

Gene flow is predicted to impede parallel adaptation via de novo mutation, because it can introduce pre-existing adaptive alleles from population to population. We test this using Hawaiian crickets (Teleogryllus oceanicus) in which ‘flatwing’ males that lack sound-producing wing structures recently arose and spread under selection from an acoustically-orienting parasitoid. Morphometric and genetic comparisons identify distinct flatwing phenotypes in populations on three islands, localized to different loci. Nevertheless, we detect strong, recent and ongoing gene flow among the populations. Using genome scans and gene expression analysis we find that parallel evolution of flatwing on different islands is associated with shared genomic hotspots of adaptation that contain the gene doublesex, but the form of selection differs among islands and corresponds to known flatwing demographics in the wild. We thus show how parallel adaptation can occur on contemporary timescales despite gene flow, indicating that it could be less constrained than previously appreciated.

The de novo genome assembly of Tapiscia sinensis and the transcriptomic and developmental bases of androdioecy

Tapiscia sinensis (Tapisciaceae) possesses an unusual androdioecious breeding system that has attracted considerable interest from evolutionary biologists. Key aspects of T. sinensis biology, including its biogeography, genomics, and sex-linked genes, are unknown. Here, we report the first de novo assembly of the genome of T. sinensis. The genome size was 410 Mb, with 22,251 predicted genes. Based on whole-genome resequencing of 55 trees from 10 locations, an analysis of population genetic structure indicated that T. sinensis has fragmented into five lineages, with low intrapopulation genetic diversity and little gene flow among populations. By comparing whole-genome scans of male versus hermaphroditic pools, we identified 303 candidate sex-linked genes, 79 of which (25.9%) were located on scaffold 25. A 24-kb region was absent in hermaphroditic individuals, and five genes in that region, TsF-box4, TsF-box10, TsF-box13, TsSUT1, and TsSUT4, showed expression differences between mature male and hermaphroditic flowers. The results of this study shed light on the breeding system evolution and conservation genetics of the Tapisciaceae.