Recurrent evolution and selection shape structural diversity at the amylase locus.

The adoption of agriculture triggered a rapid shift towards starch-rich diets in human populations1. Amylase genes facilitate starch digestion, and increased amylase copy number has been observed in some modern human populations with high-starch intake2, although evidence of recent selection is lacking3,4. Here, using 94 long-read haplotype-resolved assemblies and short-read data from approximately 5,600 contemporary and ancient humans, we resolve the diversity and evolutionary history of structural variation at the amylase locus. We find that amylase genes have higher copy numbers in agricultural populations than in fishing, hunting and pastoral populations. We identify 28 distinct amylase structural architectures and demonstrate that nearly identical structures have arisen recurrently on different haplotype backgrounds throughout recent human history. AMY1 and AMY2A genes each underwent multiple duplication/deletion events with mutation rates up to more than 10,000-fold the single-nucleotide polymorphism mutation rate, whereas AMY2B gene duplications share a single origin. Using a pangenome-based approach, we infer structural haplotypes across thousands of humans identifying extensively duplicated haplotypes at higher frequency in modern agricultural populations. Leveraging 533 ancient human genomes, we find that duplication-containing haplotypes (with more gene copies than the ancestral haplotype) have rapidly increased in frequency over the past 12,000 years in West Eurasians, suggestive of positive selection. Together, our study highlights the potential effects of the agricultural revolution on human genomes and the importance of structural variation in human adaptation.

African climate and geomorphology drive evolution and ghost introgression in sable antelope.

The evolutionary history of African ungulates has been explained largely in the light of Pleistocene climatic oscillations and the way these influenced the distribution of vegetation types, leading to range expansions and/or isolation in refugia. In contrast, comparatively fewer studies have addressed the continent's environmental heterogeneity and the role played by its geomorphological barriers. In this study, we performed a range-wide analysis of complete mitogenomes of sable antelope (Hippotragus niger) to explore how these different factors may have contributed as drivers of evolution in southcentral Africa. Our results supported two sympatric and deeply divergent mitochondrial lineages in west Tanzanian sables, which can be explained as the result of introgressive hybridization of a mitochondrial ghost lineage from an archaic, as-yet-undefined, congener. Phylogeographical subdivisions into three main lineages suggest that sable diversification may not have been driven solely by climatic events affecting populations differently across a continental scale. Often in interplay with climate, geomorphological features have also clearly shaped the species' patterns of vicariance, where the East Africa Rift System and the Eastern Arc Mountains acted as geological barriers. Subsequent splits among southern populations may be linked to rearrangements in the Zambezi system, possibly framing the most recent time when the river attained its current drainage profile. This work underlines how the use of comprehensive mitogenomic data sets on a model species with a wide geographical distribution can contribute to a much-enhanced understanding of environmental, geomorphological and evolutionary patterns in Africa throughout the Quaternary.

Global diversity, recurrent evolution, and recent selection on amylase structural haplotypes in humans.

The adoption of agriculture, first documented ~12,000 years ago in the Fertile Crescent, triggered a rapid shift toward starch-rich diets in human populations. Amylase genes facilitate starch digestion and increased salivary amylase copy number has been observed in some modern human populations with high starch intake, though evidence of recent selection is lacking. Here, using 52 long-read diploid assemblies and short read data from ~5,600 contemporary and ancient humans, we resolve the diversity, evolutionary history, and selective impact of structural variation at the amylase locus. We find that amylase genes have higher copy numbers in populations with agricultural subsistence compared to fishing, hunting, and pastoral groups. We identify 28 distinct amylase structural architectures and demonstrate that nearly identical structures have arisen recurrently on different haplotype backgrounds throughout recent human history. AMY1 and AMY2A genes each exhibit multiple duplications/deletions with mutation rates >10,000-fold the SNP mutation rate, whereas AMY2B gene duplications share a single origin. Using a pangenome graph-based approach to infer structural haplotypes across thousands of humans, we identify extensively duplicated haplotypes present at higher frequencies in modern day populations with traditionally agricultural diets. Leveraging 533 ancient human genomes we find that duplication-containing haplotypes (i.e. haplotypes with more amylase gene copies than the ancestral haplotype) have increased in frequency more than seven-fold over the last 12,000 years providing evidence for recent selection in West Eurasians. Together, our study highlights the potential impacts of the agricultural revolution on human genomes and the importance of long-read sequencing in identifying signatures of selection at structurally complex loci.

Life in Deserts: The Genetic Basis of Mammalian Desert Adaptation.

Deserts are among the harshest environments on Earth. The multiple ages of different deserts and their global distribution provide a unique opportunity to study repeated adaptation at different timescales. Here, we summarize recent genomic research on the genetic mechanisms underlying desert adaptations in mammals. Several studies on different desert mammals show large overlap in functional classes of genes and pathways, consistent with the complexity and variety of phenotypes associated with desert adaptation to water and food scarcity and extreme temperatures. However, studies of desert adaptation are also challenged by a lack of accurate genotype-phenotype-environment maps. We encourage development of systems that facilitate functional analyses, but also acknowledge the need for more studies on a wider variety of desert mammals.