Extreme selective sweeps independently targeted the X chromosomes of the great apes

Great Ape Genome Diversity Project

Research output: Contribution to journalArticle

35 Citations (Scopus)

Abstract

The unique inheritance pattern of the X chromosome exposes it to natural selection in a way that is different from that of the autosomes, potentially resulting in accelerated evolution. We perform a comparative analysis of X chromosome polymorphism in 10 great ape species, including humans. In most species, we identify striking megabase-wide regions, where nucleotide diversity is less than 20% of the chromosomal average. Such regions are found exclusively on the X chromosome. The regions overlap partially among species, suggesting that the underlying targets are partly shared among species. The regions have higher proportions of singleton SNPs, higher levels of population differentiation, and a higher nonsynonymous-to-synonymous substitution ratio than the rest of the X chromosome. We show that the extent to which diversity is reduced is incompatible with direct selection or the action of background selection and soft selective sweeps alone, and therefore, we suggest that very strong selective sweeps have independently targeted these specific regions in several species. The only genomic feature that we can identify as strongly associated with loss of diversity is the location of testis-expressed ampliconic genes, which also have reduced diversity around them. We hypothesize that these genes may be responsible for selective sweeps in the form of meiotic drive caused by an intragenomic conflict in male meiosis.

Original languageEnglish (US)
Pages (from-to)6413-6418
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume112
Issue number20
DOIs
StatePublished - May 19 2015
Externally publishedYes

Fingerprint

Hominidae
X Chromosome
Inheritance Patterns
Genetic Selection
Meiosis
Genes
Single Nucleotide Polymorphism
Testis
Nucleotides
Population

Keywords

  • Ampliconic genes
  • Great apes
  • Meiotic drive
  • Selective sweeps
  • X-chromosome evolution

ASJC Scopus subject areas

  • General

Cite this

Extreme selective sweeps independently targeted the X chromosomes of the great apes. / Great Ape Genome Diversity Project.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, No. 20, 19.05.2015, p. 6413-6418.

Research output: Contribution to journalArticle

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abstract = "The unique inheritance pattern of the X chromosome exposes it to natural selection in a way that is different from that of the autosomes, potentially resulting in accelerated evolution. We perform a comparative analysis of X chromosome polymorphism in 10 great ape species, including humans. In most species, we identify striking megabase-wide regions, where nucleotide diversity is less than 20{\%} of the chromosomal average. Such regions are found exclusively on the X chromosome. The regions overlap partially among species, suggesting that the underlying targets are partly shared among species. The regions have higher proportions of singleton SNPs, higher levels of population differentiation, and a higher nonsynonymous-to-synonymous substitution ratio than the rest of the X chromosome. We show that the extent to which diversity is reduced is incompatible with direct selection or the action of background selection and soft selective sweeps alone, and therefore, we suggest that very strong selective sweeps have independently targeted these specific regions in several species. The only genomic feature that we can identify as strongly associated with loss of diversity is the location of testis-expressed ampliconic genes, which also have reduced diversity around them. We hypothesize that these genes may be responsible for selective sweeps in the form of meiotic drive caused by an intragenomic conflict in male meiosis.",
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AU - Lachmann, M.

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AU - Hormozdiari, Fereydoun

AU - Fernandez-Callejo, M.

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AU - Carvalho, T.

AU - Ruiz-Herrera, A.

AU - Vives, L.

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