Recurrent evolution and selection shape structural diversity at the amylase locus

Davide Bolognini, Alma Halgren, Runyang Nicolas Lou, Alessandro Raveane, Joana L. Rocha, Andrea Guarracino, Nicole Soranzo, Chen-Shan Chin, Erik Garrison () and Peter H. Sudmant ()
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Davide Bolognini: Human Technopole
Alma Halgren: University of California Berkeley
Runyang Nicolas Lou: University of California Berkeley
Alessandro Raveane: Human Technopole
Joana L. Rocha: University of California Berkeley
Andrea Guarracino: University of Tennessee Health Science Center
Nicole Soranzo: Human Technopole
Chen-Shan Chin: Foundation for Biological Data Science
Erik Garrison: University of Tennessee Health Science Center
Peter H. Sudmant: University of California Berkeley

Nature, 2024, vol. 634, issue 8034, 617-625

Abstract: Abstract 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.

Date: 2024
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DOI: 10.1038/s41586-024-07911-1

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