Segregation distortion in chicken and the evolutionary consequences of female meiotic drive in birds

Erik Gunnar Axelsson; Anders Albrechtsen; A. P. Van; L. Li; H. J. Megens; A. L. J. Vereijken; R. P. M. A. Crooijmans; M. A. M. Groenen; H. Ellegren; Eske Willerslev; R. Nielsen

doi:10.1038/hdy.2009.193

Segregation distortion in chicken and the evolutionary consequences of female meiotic drive in birds

Erik Gunnar Axelsson, Anders Albrechtsen, A. P. Van, L. Li, H. J. Megens, A. L. J. Vereijken, R. P. M. A. Crooijmans, M. A. M. Groenen, H. Ellegren, Eske Willerslev, R. Nielsen

Section of Biostatistics

22 Citations (Scopus)

Abstract

As all four meiotic products give rise to sperm in males, female meiosis result in a single egg in most eukaryotes. Any genetic element with the potential to influence chromosome segregation, so that it is preferentially included in the egg, should therefore gain a transmission advantage; a process termed female meiotic drive. We are aware of two chromosomal components, centromeres and telomeres, which share the potential to influence chromosome movement during meioses and make the following predictions based on the presence of female meiotic drive: (1) centromere-binding proteins should experience rapid evolution as a result of a conflict between driving centromeres and the rest of the genome; and (2) segregation patterns should be skewed near centromeres and telomeres. To test these predictions, we first analyze the molecular evolution of seven centromere-binding proteins in nine divergent bird species. We find strong evidence for positive selection in two genes, lending support to the genomic conflict hypothesis. Then, to directly test for the presence of segregation distortion, we also investigate the transmission of 9000 single-nucleotide polymorphisms in 197 chicken families. By simulating fair Mendelian meioses, we locate chromosomal regions with statistically significant transmission ratio distortion. One region is located near the centromere on chromosome 1 and a second region is located near the telomere on the p-arm of chromosome 1. Although these observations do not provide conclusive evidence in favour of the meiotic drive/genome conflict hypothesis, they do lend support to the hypothesis that centromeres and telomeres drive during female meioses in chicken.

Original language	English
Journal	Heredity
Volume	105
Issue number	3
Pages (from-to)	290-298
Number of pages	9
ISSN	0018-067X
DOIs	https://doi.org/10.1038/hdy.2009.193
Publication status	Published - Sept 2010

Keywords

Animals
Biological Evolution
Centromere
Chickens
Chromosomes, Mammalian
Computer Simulation
Female
Genetic Markers
Meiosis
Polymorphism, Single Nucleotide
Sex Factors

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title = "Segregation distortion in chicken and the evolutionary consequences of female meiotic drive in birds",

abstract = "As all four meiotic products give rise to sperm in males, female meiosis result in a single egg in most eukaryotes. Any genetic element with the potential to influence chromosome segregation, so that it is preferentially included in the egg, should therefore gain a transmission advantage; a process termed female meiotic drive. We are aware of two chromosomal components, centromeres and telomeres, which share the potential to influence chromosome movement during meioses and make the following predictions based on the presence of female meiotic drive: (1) centromere-binding proteins should experience rapid evolution as a result of a conflict between driving centromeres and the rest of the genome; and (2) segregation patterns should be skewed near centromeres and telomeres. To test these predictions, we first analyze the molecular evolution of seven centromere-binding proteins in nine divergent bird species. We find strong evidence for positive selection in two genes, lending support to the genomic conflict hypothesis. Then, to directly test for the presence of segregation distortion, we also investigate the transmission of 9000 single-nucleotide polymorphisms in 197 chicken families. By simulating fair Mendelian meioses, we locate chromosomal regions with statistically significant transmission ratio distortion. One region is located near the centromere on chromosome 1 and a second region is located near the telomere on the p-arm of chromosome 1. Although these observations do not provide conclusive evidence in favour of the meiotic drive/genome conflict hypothesis, they do lend support to the hypothesis that centromeres and telomeres drive during female meioses in chicken.",

keywords = "Animals, Biological Evolution, Centromere, Chickens, Chromosomes, Mammalian, Computer Simulation, Female, Genetic Markers, Meiosis, Polymorphism, Single Nucleotide, Sex Factors",

author = "Axelsson, {Erik Gunnar} and Anders Albrechtsen and Van, {A. P.} and L. Li and Megens, {H. J.} and Vereijken, {A. L. J.} and Crooijmans, {R. P. M. A.} and Groenen, {M. A. M.} and H. Ellegren and Eske Willerslev and R. Nielsen",

year = "2010",

month = sep,

doi = "10.1038/hdy.2009.193",

language = "English",

volume = "105",

pages = "290--298",

journal = "Heredity",

issn = "0018-067X",

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number = "3",

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TY - JOUR

T1 - Segregation distortion in chicken and the evolutionary consequences of female meiotic drive in birds

AU - Axelsson, Erik Gunnar

AU - Albrechtsen, Anders

AU - Van, A. P.

AU - Li, L.

AU - Megens, H. J.

AU - Vereijken, A. L. J.

AU - Crooijmans, R. P. M. A.

AU - Groenen, M. A. M.

AU - Ellegren, H.

AU - Willerslev, Eske

AU - Nielsen, R.

PY - 2010/9

Y1 - 2010/9

N2 - As all four meiotic products give rise to sperm in males, female meiosis result in a single egg in most eukaryotes. Any genetic element with the potential to influence chromosome segregation, so that it is preferentially included in the egg, should therefore gain a transmission advantage; a process termed female meiotic drive. We are aware of two chromosomal components, centromeres and telomeres, which share the potential to influence chromosome movement during meioses and make the following predictions based on the presence of female meiotic drive: (1) centromere-binding proteins should experience rapid evolution as a result of a conflict between driving centromeres and the rest of the genome; and (2) segregation patterns should be skewed near centromeres and telomeres. To test these predictions, we first analyze the molecular evolution of seven centromere-binding proteins in nine divergent bird species. We find strong evidence for positive selection in two genes, lending support to the genomic conflict hypothesis. Then, to directly test for the presence of segregation distortion, we also investigate the transmission of 9000 single-nucleotide polymorphisms in 197 chicken families. By simulating fair Mendelian meioses, we locate chromosomal regions with statistically significant transmission ratio distortion. One region is located near the centromere on chromosome 1 and a second region is located near the telomere on the p-arm of chromosome 1. Although these observations do not provide conclusive evidence in favour of the meiotic drive/genome conflict hypothesis, they do lend support to the hypothesis that centromeres and telomeres drive during female meioses in chicken.

AB - As all four meiotic products give rise to sperm in males, female meiosis result in a single egg in most eukaryotes. Any genetic element with the potential to influence chromosome segregation, so that it is preferentially included in the egg, should therefore gain a transmission advantage; a process termed female meiotic drive. We are aware of two chromosomal components, centromeres and telomeres, which share the potential to influence chromosome movement during meioses and make the following predictions based on the presence of female meiotic drive: (1) centromere-binding proteins should experience rapid evolution as a result of a conflict between driving centromeres and the rest of the genome; and (2) segregation patterns should be skewed near centromeres and telomeres. To test these predictions, we first analyze the molecular evolution of seven centromere-binding proteins in nine divergent bird species. We find strong evidence for positive selection in two genes, lending support to the genomic conflict hypothesis. Then, to directly test for the presence of segregation distortion, we also investigate the transmission of 9000 single-nucleotide polymorphisms in 197 chicken families. By simulating fair Mendelian meioses, we locate chromosomal regions with statistically significant transmission ratio distortion. One region is located near the centromere on chromosome 1 and a second region is located near the telomere on the p-arm of chromosome 1. Although these observations do not provide conclusive evidence in favour of the meiotic drive/genome conflict hypothesis, they do lend support to the hypothesis that centromeres and telomeres drive during female meioses in chicken.

KW - Animals

KW - Biological Evolution

KW - Centromere

KW - Chickens

KW - Chromosomes, Mammalian

KW - Computer Simulation

KW - Female

KW - Genetic Markers

KW - Meiosis

KW - Polymorphism, Single Nucleotide

KW - Sex Factors

U2 - 10.1038/hdy.2009.193

DO - 10.1038/hdy.2009.193

M3 - Journal article

C2 - 20104236

SN - 0018-067X

VL - 105

SP - 290

EP - 298

JO - Heredity

JF - Heredity

IS - 3

ER -

Segregation distortion in chicken and the evolutionary consequences of female meiotic drive in birds

Abstract

Keywords

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