Extraordinary selection on the human X chromosome associated with archaic admixture

Area of Science:

• Human evolutionary genetics
• Population genetics
• Genomics

Background:

• The human X chromosome exhibits lower genetic diversity and Neanderthal introgression in non-African populations than predicted by neutral evolutionary models.
• Understanding the evolutionary forces shaping the X chromosome is crucial for comprehending human population history.

Purpose of the Study:

• To investigate the evolutionary mechanisms responsible for reduced diversity and archaic ancestry on the human X chromosome in non-African populations.
• To identify specific chromosomal regions and timeframes associated with strong selective pressures.

Main Methods:

• Analysis of 162 human male X chromosomes from global populations.
• Identification and characterization of high-frequency haplotypes across chromosomal regions.
• Comparison of archaic ancestry patterns between swept and non-swept haplotypes.
• Dating of selective events using ancient DNA (Ust'-Ishim male).

Main Results:

• Fourteen chromosomal regions with nearly identical, long haplotypes at high frequencies in non-Africans were identified.
• These haplotypes are devoid of archaic ancestry, contrasting with non-swept regions, indicating strong positive selection.
• Selection likely occurred between 45,000 and 55,000 years ago, as evidenced by the Ust'-Ishim individual.
• Selected regions overlap with known selective sweep hotspots in great ape evolution.

Conclusions:

• Strong positive selection, not just genetic drift, has significantly shaped the human X chromosome in non-African populations.
• Selective sweeps on the X chromosome led to reduced diversity and loss of archaic introgression.
• The findings suggest a unique X chromosome-specific selection mechanism potentially conserved across primate evolution.