Literature DB >> 25941379

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

Kiwoong Nam1, Kasper Munch2, Asger Hobolth2, Julien Yann Dutheil3, Krishna R Veeramah4, August E Woerner4, Michael F Hammer4, Thomas Mailund2, Mikkel Heide Schierup5.   

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.

Entities:  

Keywords:  X-chromosome evolution; ampliconic genes; great apes; meiotic drive; selective sweeps

Mesh:

Year:  2015        PMID: 25941379      PMCID: PMC4443357          DOI: 10.1073/pnas.1419306112

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  40 in total

1.  Allele frequency distribution under recurrent selective sweeps.

Authors:  Yuseob Kim
Journal:  Genetics       Date:  2005-12-15       Impact factor: 4.562

Review 2.  Evolution on the X chromosome: unusual patterns and processes.

Authors:  Beatriz Vicoso; Brian Charlesworth
Journal:  Nat Rev Genet       Date:  2006-08       Impact factor: 53.242

3.  Causes of sex ratio bias may account for unisexual sterility in hybrids: a new explanation of Haldane's rule and related phenomena.

Authors:  L D Hurst; A Pomiankowski
Journal:  Genetics       Date:  1991-08       Impact factor: 4.562

4.  Variances of the average numbers of nucleotide substitutions within and between populations.

Authors:  M Nei; L Jin
Journal:  Mol Biol Evol       Date:  1989-05       Impact factor: 16.240

5.  Mathematical model for studying genetic variation in terms of restriction endonucleases.

Authors:  M Nei; W H Li
Journal:  Proc Natl Acad Sci U S A       Date:  1979-10       Impact factor: 11.205

6.  Chromosome-wide linkage disequilibrium as a consequence of meiotic drive.

Authors:  Kelly A Dyer; Brian Charlesworth; John Jaenike
Journal:  Proc Natl Acad Sci U S A       Date:  2007-01-22       Impact factor: 11.205

7.  Genetic conflict and sex chromosome evolution.

Authors:  Colin D Meiklejohn; Yun Tao
Journal:  Trends Ecol Evol       Date:  2009-11-26       Impact factor: 17.712

8.  Reduced levels of DNA polymorphism and fixed between-population differences in the centromeric region of Drosophila ananassae.

Authors:  W Stephan; S J Mitchell
Journal:  Genetics       Date:  1992-12       Impact factor: 4.562

9.  A scan for positively selected genes in the genomes of humans and chimpanzees.

Authors:  Rasmus Nielsen; Carlos Bustamante; Andrew G Clark; Stephen Glanowski; Timothy B Sackton; Melissa J Hubisz; Adi Fledel-Alon; David M Tanenbaum; Daniel Civello; Thomas J White; John J Sninsky; Mark D Adams; Michele Cargill
Journal:  PLoS Biol       Date:  2005-05-03       Impact factor: 8.029

10.  The multicopy gene Sly represses the sex chromosomes in the male mouse germline after meiosis.

Authors:  Julie Cocquet; Peter J I Ellis; Yasuhiro Yamauchi; Shantha K Mahadevaiah; Nabeel A Affara; Monika A Ward; Paul S Burgoyne
Journal:  PLoS Biol       Date:  2009-11-17       Impact factor: 8.029

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  32 in total

Review 1.  The eXceptional nature of the X chromosome.

Authors:  Bradley P Balaton; Thomas Dixon-McDougall; Samantha B Peeters; Carolyn J Brown
Journal:  Hum Mol Genet       Date:  2018-08-01       Impact factor: 6.150

2.  Evidence that the rate of strong selective sweeps increases with population size in the great apes.

Authors:  Kiwoong Nam; Kasper Munch; Thomas Mailund; Alexander Nater; Maja Patricia Greminger; Michael Krützen; Tomàs Marquès-Bonet; Mikkel Heide Schierup
Journal:  Proc Natl Acad Sci U S A       Date:  2017-01-30       Impact factor: 11.205

3.  Changes in life history and population size can explain the relative neutral diversity levels on X and autosomes in extant human populations.

Authors:  Guy Amster; David A Murphy; William R Milligan; Guy Sella
Journal:  Proc Natl Acad Sci U S A       Date:  2020-08-03       Impact factor: 11.205

4.  Genomic Signatures of Sexual Conflict.

Authors:  Katja R Kasimatis; Thomas C Nelson; Patrick C Phillips
Journal:  J Hered       Date:  2017-10-30       Impact factor: 2.645

5.  Gene-dense autosomal chromosomes show evidence for increased selection.

Authors:  M Reza Jabalameli; Clare Horscroft; Alejandra Vergara-Lope; Reuben J Pengelly; Andrew Collins
Journal:  Heredity (Edinb)       Date:  2019-10-01       Impact factor: 3.821

6.  Meiotic drive mechanisms: lessons from Drosophila.

Authors:  Cécile Courret; Ching-Ho Chang; Kevin H-C Wei; Catherine Montchamp-Moreau; Amanda M Larracuente
Journal:  Proc Biol Sci       Date:  2019-10-23       Impact factor: 5.349

7.  Contrasting patterns of X-chromosome divergence underlie multiple sex-ratio polymorphisms in stalk-eyed flies.

Authors:  K A Paczolt; J A Reinhardt; G S Wilkinson
Journal:  J Evol Biol       Date:  2017-08-04       Impact factor: 2.411

Review 8.  Spermatogenesis and the Evolution of Mammalian Sex Chromosomes.

Authors:  Erica L Larson; Emily E K Kopania; Jeffrey M Good
Journal:  Trends Genet       Date:  2018-08-01       Impact factor: 11.639

9.  Sequence and Structural Diversity of Mouse Y Chromosomes.

Authors:  Andrew P Morgan; Fernando Pardo-Manuel de Villena
Journal:  Mol Biol Evol       Date:  2017-12-01       Impact factor: 16.240

10.  Contrasting Levels of Molecular Evolution on the Mouse X Chromosome.

Authors:  Erica L Larson; Dan Vanderpool; Sara Keeble; Meng Zhou; Brice A J Sarver; Andrew D Smith; Matthew D Dean; Jeffrey M Good
Journal:  Genetics       Date:  2016-06-17       Impact factor: 4.562

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