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

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The agricultural revolution led to more copies of amylase genes in humans, aiding starch digestion. These gene duplications, driven by positive selection, rapidly increased in frequency over the last 12,000 years.

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Area of Science:

  • Human Evolutionary Genetics
  • Genomics
  • Archaeological Science

Background:

  • The shift to agriculture dramatically altered human diets, increasing reliance on starch.
  • Amylase genes are crucial for starch digestion, with copy number variations linked to dietary habits.
  • Previous evidence for recent selection on amylase gene copy number was limited.

Purpose of the Study:

  • To investigate the diversity and evolutionary history of structural variations at the amylase locus.
  • To understand the impact of the agricultural revolution on human amylase gene copy number.
  • To identify evidence of selection acting on amylase gene structural variation.

Main Methods:

  • Analysis of 94 long-read haplotype-resolved assemblies and ~5,600 short-read human genome data (contemporary and ancient).
  • Pangenome-based approach to infer structural haplotypes across diverse human populations.
  • Leveraging 533 ancient human genomes to track haplotype frequency changes over 12,000 years.

Main Results:

  • Identified 28 distinct amylase gene structural architectures, with recurrent evolution of similar structures.
  • Agricultural populations exhibit higher amylase gene copy numbers compared to non-agricultural groups.
  • Duplication-containing haplotypes, associated with increased gene copies, rapidly rose in frequency in West Eurasians over the past 12,000 years.

Conclusions:

  • Human amylase gene copy number and structure have undergone significant adaptation since the agricultural revolution.
  • Structural variation at the amylase locus shows strong signals of positive selection in response to dietary changes.
  • This study underscores the role of structural variation in human adaptation to major lifestyle shifts.