Strict evolutionary conservation followed rapid gene loss on human and rhesus Y chromosomes

The male-specific region of rhesus macaque and human Y chromosome (MSY) are sequenced and compared to the human MSY, showing that during the last 25 million years MSY gene loss in the rhesus and human lineages was limited to the youngest stratum (stratum 5), whereas gene loss in the older strata cea...

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Published inNature (London) Vol. 483; no. 7387; pp. 82 - 86
Main Authors Hughes, Jennifer F., Skaletsky, Helen, Brown, Laura G., Pyntikova, Tatyana, Graves, Tina, Fulton, Robert S., Dugan, Shannon, Ding, Yan, Buhay, Christian J., Kremitzki, Colin, Wang, Qiaoyan, Shen, Hua, Holder, Michael, Villasana, Donna, Nazareth, Lynne V., Cree, Andrew, Courtney, Laura, Veizer, Joelle, Kotkiewicz, Holland, Cho, Ting-Jan, Koutseva, Natalia, Rozen, Steve, Muzny, Donna M., Warren, Wesley C., Gibbs, Richard A., Wilson, Richard K., Page, David C.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.03.2012
Nature Publishing Group
Subjects
631/181/2474
631/337/103
Animals
Artificial chromosomes
Biological and medical sciences
Chimpanzees
Chromosome mapping
Chromosomes
Chromosomes, Human, Y - genetics
Classical genetics, quantitative genetics, hybrids
Cloning
Confidence intervals
Conserved Sequence - genetics
Crossing Over, Genetic - genetics
Evolution, Molecular
Evolutionary genetics
Fundamental and applied biological sciences. Psychology
Gene Amplification - genetics
Gene Deletion
Genes
Genetic aspects
Genetics
Genetics of eukaryotes. Biological and molecular evolution
Haplotypes
Human
Human chromosomes
Human genetics
Humanities and Social Sciences
Humans
Hybridization
In Situ Hybridization, Fluorescence
letter
Macaca mulatta - genetics
Male
Methods
Models, Genetic
Molecular Sequence Data
multidisciplinary
Pan troglodytes - genetics
Properties
Radiation Hybrid Mapping
Regression analysis
Rhesus monkey
Science
Science (multidisciplinary)
Selection, Genetic - genetics
Stratigraphy
Time Factors
Y chromosome
Y Chromosome - genetics
United States
Human
Molecular evolution
Vertebrata
Mammalia
Sex chromosome
Primates
Simioidea
Macaca mulatta
X-Chromosome
Y-Chromosome
Comparative study
Online AccessGet full text

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Abstract The male-specific region of rhesus macaque and human Y chromosome (MSY) are sequenced and compared to the human MSY, showing that during the last 25 million years MSY gene loss in the rhesus and human lineages was limited to the youngest stratum (stratum 5), whereas gene loss in the older strata ceased more than 25 million years ago. The fate of the Y chromosome The mammal sex-determining X and Y chromosomes evolved from a pair of autosomes ('normal' non-sex chromosomes), but as a result of genetic decay, the male-specific region of the human Y chromosome retains only 3% of the ancestral autosomal genes. Here, the authors have sequenced the corresponding region of the rhesus macaque Y, and reconstructed the trajectory of its evolution through an analysis of the rhesus, human and chimpanzee Y chromosomes. The results show that initial rapid loss of genes is followed by strict conservation through purifying selection. This runs counter to the view that the human Y chromosome is destined inevitably for extinction. The human X and Y chromosomes evolved from an ordinary pair of autosomes during the past 200–300 million years 1 , 2 , 3 . The human MSY (male-specific region of Y chromosome) retains only three percent of the ancestral autosomes’ genes owing to genetic decay 4 , 5 . This evolutionary decay was driven by a series of five ‘stratification’ events. Each event suppressed X–Y crossing over within a chromosome segment or ‘stratum’, incorporated that segment into the MSY and subjected its genes to the erosive forces that attend the absence of crossing over 2 , 6 . The last of these events occurred 30 million years ago, 5 million years before the human and Old World monkey lineages diverged. Although speculation abounds regarding ongoing decay and looming extinction of the human Y chromosome 7 , 8 , 9 , 10 , remarkably little is known about how many MSY genes were lost in the human lineage in the 25 million years that have followed its separation from the Old World monkey lineage. To investigate this question, we sequenced the MSY of the rhesus macaque, an Old World monkey, and compared it to the human MSY. We discovered that during the last 25 million years MSY gene loss in the human lineage was limited to the youngest stratum (stratum 5), which comprises three percent of the human MSY. In the older strata, which collectively comprise the bulk of the human MSY, gene loss evidently ceased more than 25 million years ago. Likewise, the rhesus MSY has not lost any older genes (from strata 1–4) during the past 25 million years, despite its major structural differences to the human MSY. The rhesus MSY is simpler, with few amplified gene families or palindromes that might enable intrachromosomal recombination and repair. We present an empirical reconstruction of human MSY evolution in which each stratum transitioned from rapid, exponential loss of ancestral genes to strict conservation through purifying selection.
AbstractList The human X and Y chromosomes evolved from an ordinary pair of autosomes during the past 200–300 million years 1 – 3 . Due to genetic decay, the human MSY (male-specific region of Y chromosome) retains only three percent of the ancestral autosomes’ genes 4 , 5 . This evolutionary decay was driven by a series of five “stratification” events. Each event suppressed X-Y crossing over within a chromosome segment or “stratum”, incorporated that segment into the MSY, and subjected its genes to the erosive forces that attend the absence of crossing over 2 , 6 . The last of these events occurred 30 million years ago (mya), or 5 million years before the human and Old World monkey (OWM) lineages diverged. Although speculation abounds regarding ongoing decay and looming extinction of the human Y chromosome 7 – 10 , remarkably little is known about how many MSY genes were lost in the human lineage in the 25 million years that have followed its separation from the OWM lineage. To explore this question, we sequenced the MSY of the rhesus macaque, an OWM, and compared it to the human MSY. We discovered that, during the last 25 million years, MSY gene loss in the human lineage was limited to the youngest stratum (stratum 5), which comprises three percent of the human MSY. Within the older strata, which collectively comprise the bulk of the human MSY, gene loss evidently ceased more than 25 mya. Likewise, the rhesus MSY has not lost any older genes (from strata 1–4) during the past 25 million years, despite major structural differences from the human MSY. The rhesus MSY is simpler, with few amplified gene families or palindromes that might enable intrachromosomal recombination and repair. We present an empirical reconstruction of human MSY evolution in which each stratum transitioned from rapid, exponential loss of ancestral genes to strict conservation through purifying selection.
[...] we searched for homologues of all known human X-linked genes, to identify any X-Y shared genes that had been lost in both the human and chimpanzee MSY but retained in the rhesus MSY. [...] we searched for additional rhesus-specific MSY genes using electronic prediction tools and high-throughput sequencing of rhesus testis complementary DNA (245 Mb in total).
The human X and Y chromosomes evolved from an ordinary pair of autosomes during the past 200-300 million years. The human MSY (male-specific region of Y chromosome) retains only three percent of the ancestral autosomes' genes owing to genetic decay. This evolutionary decay was driven by a series of five 'stratification' events. Each event suppressed X-Y crossing over within a chromosome segment or 'stratum', incorporated that segment into the MSY and subjected its genes to the erosive forces that attend the absence of crossing over. The last of these events occurred 30 million years ago, 5 million years before the human and Old World monkey lineages diverged. Although speculation abounds regarding ongoing decay and looming extinction of the human Y chromosome, remarkably little is known about how many MSY genes were lost in the human lineage in the 25 million years that have followed its separation from the Old World monkey lineage. To investigate this question, we sequenced the MSY of the rhesus macaque, an Old World monkey, and compared it to the human MSY. We discovered that during the last 25 million years MSY gene loss in the human lineage was limited to the youngest stratum (stratum 5), which comprises three percent of the human MSY. In the older strata, which collectively comprise the bulk of the human MSY, gene loss evidently ceased more than 25 million years ago. Likewise, the rhesus MSY has not lost any older genes (from strata 1-4) during the past 25 million years, despite its major structural differences to the human MSY. The rhesus MSY is simpler, with few amplified gene families or palindromes that might enable intrachromosomal recombination and repair. We present an empirical reconstruction of human MSY evolution in which each stratum transitioned from rapid, exponential loss of ancestral genes to strict conservation through purifying selection.
The male-specific region of rhesus macaque and human Y chromosome (MSY) are sequenced and compared to the human MSY, showing that during the last 25 million years MSY gene loss in the rhesus and human lineages was limited to the youngest stratum (stratum 5), whereas gene loss in the older strata ceased more than 25 million years ago. The fate of the Y chromosome The mammal sex-determining X and Y chromosomes evolved from a pair of autosomes ('normal' non-sex chromosomes), but as a result of genetic decay, the male-specific region of the human Y chromosome retains only 3% of the ancestral autosomal genes. Here, the authors have sequenced the corresponding region of the rhesus macaque Y, and reconstructed the trajectory of its evolution through an analysis of the rhesus, human and chimpanzee Y chromosomes. The results show that initial rapid loss of genes is followed by strict conservation through purifying selection. This runs counter to the view that the human Y chromosome is destined inevitably for extinction. The human X and Y chromosomes evolved from an ordinary pair of autosomes during the past 200–300 million years 1 , 2 , 3 . The human MSY (male-specific region of Y chromosome) retains only three percent of the ancestral autosomes’ genes owing to genetic decay 4 , 5 . This evolutionary decay was driven by a series of five ‘stratification’ events. Each event suppressed X–Y crossing over within a chromosome segment or ‘stratum’, incorporated that segment into the MSY and subjected its genes to the erosive forces that attend the absence of crossing over 2 , 6 . The last of these events occurred 30 million years ago, 5 million years before the human and Old World monkey lineages diverged. Although speculation abounds regarding ongoing decay and looming extinction of the human Y chromosome 7 , 8 , 9 , 10 , remarkably little is known about how many MSY genes were lost in the human lineage in the 25 million years that have followed its separation from the Old World monkey lineage. To investigate this question, we sequenced the MSY of the rhesus macaque, an Old World monkey, and compared it to the human MSY. We discovered that during the last 25 million years MSY gene loss in the human lineage was limited to the youngest stratum (stratum 5), which comprises three percent of the human MSY. In the older strata, which collectively comprise the bulk of the human MSY, gene loss evidently ceased more than 25 million years ago. Likewise, the rhesus MSY has not lost any older genes (from strata 1–4) during the past 25 million years, despite its major structural differences to the human MSY. The rhesus MSY is simpler, with few amplified gene families or palindromes that might enable intrachromosomal recombination and repair. We present an empirical reconstruction of human MSY evolution in which each stratum transitioned from rapid, exponential loss of ancestral genes to strict conservation through purifying selection.
The human X and Y chromosomes evolved from an ordinary pair of autosomes during the past 200-300 million years (1-3). The human MSY (male-specific region of Y chromosome) retains only three percent of the ancestral autosomes' genes owing to genetic decay (4,5). This evolutionary decay was driven by a series of five 'stratification' events. Each event suppressed X-Y crossing over within a chromosome segment or 'stratum', incorporated that segment into the MSY and subjected its genes to the erosive forces that attend the absence of crossing over (2,6). The last of these events occurred 30 million years ago, 5 million years before the human and Old World monkey lineages diverged. Although speculation abounds regarding ongoing decay and looming extinction of the human Y chromosome (7-10), remarkably little is known about how many MSY genes were lost in the human lineage in the 25 million years that have followed its separation from the Old World monkey lineage. To investigate this question, we sequenced the MSY of the rhesus macaque, an Old World monkey, and compared it to the human MSY. We discovered that during the last 25 million years MSY gene loss in the human lineage was limited to the youngest stratum (stratum 5), which comprises three percent of the human MSY. In the older strata, which collectively comprise the bulk of the human MSY, gene loss evidently ceased more than 25 million years ago. Likewise, the rhesus MSY has not lost any older genes (from strata 1-4) during the past 25 million years, despite its major structural differences to the human MSY. The rhesus MSY is simpler, with few amplified gene families or palindromes that might enable intrachromosomal recombination and repair. We present an empirical reconstruction of human MSY evolution in which each stratum transitioned from rapid, exponential loss of ancestral genes to strict conservation through purifying selection.
Audience Academic
Author Ding, Yan
Cree, Andrew
Villasana, Donna
Muzny, Donna M.
Page, David C.
Pyntikova, Tatyana
Hughes, Jennifer F.
Kremitzki, Colin
Skaletsky, Helen
Graves, Tina
Dugan, Shannon
Rozen, Steve
Gibbs, Richard A.
Cho, Ting-Jan
Wilson, Richard K.
Wang, Qiaoyan
Nazareth, Lynne V.
Veizer, Joelle
Koutseva, Natalia
Shen, Hua
Holder, Michael
Kotkiewicz, Holland
Brown, Laura G.
Courtney, Laura
Warren, Wesley C.
Fulton, Robert S.
Buhay, Christian J.
AuthorAffiliation 3 Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
2 The Genome Institute, Washington University School of Medicine, 4444 Forest Park Boulevard, St. Louis, Missouri 63108, USA
1 Howard Hughes Medical Institute, Whitehead Institute, and Department of Biology, Massachusetts Institute of Technology, 9 Cambridge Center, Cambridge, Massachusetts 02142, USA
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Keywords Human
Molecular evolution
Vertebrata
Mammalia
Sex chromosome
Primates
Simioidea
Macaca mulatta
X-Chromosome
Y-Chromosome
Comparative study
Language English
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Snippet The male-specific region of rhesus macaque and human Y chromosome (MSY) are sequenced and compared to the human MSY, showing that during the last 25 million...
The human X and Y chromosomes evolved from an ordinary pair of autosomes during the past 200-300 million years. The human MSY (male-specific region of Y...
The human X and Y chromosomes evolved from an ordinary pair of autosomes during the past 200-300 million years (1-3). The human MSY (male-specific region of Y...
[...] we searched for homologues of all known human X-linked genes, to identify any X-Y shared genes that had been lost in both the human and chimpanzee MSY...
The human X and Y chromosomes evolved from an ordinary pair of autosomes during the past 200–300 million years 1 – 3 . Due to genetic decay, the human MSY...
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crossref
pubmed
pascalfrancis
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StartPage 82
SubjectTerms 631/181/2474
631/337/103
Animals
Artificial chromosomes
Biological and medical sciences
Chimpanzees
Chromosome mapping
Chromosomes
Chromosomes, Human, Y - genetics
Classical genetics, quantitative genetics, hybrids
Cloning
Confidence intervals
Conserved Sequence - genetics
Crossing Over, Genetic - genetics
Evolution, Molecular
Evolutionary genetics
Fundamental and applied biological sciences. Psychology
Gene Amplification - genetics
Gene Deletion
Genes
Genetic aspects
Genetics
Genetics of eukaryotes. Biological and molecular evolution
Haplotypes
Human
Human chromosomes
Human genetics
Humanities and Social Sciences
Humans
Hybridization
In Situ Hybridization, Fluorescence
letter
Macaca mulatta - genetics
Male
Methods
Models, Genetic
Molecular Sequence Data
multidisciplinary
Pan troglodytes - genetics
Properties
Radiation Hybrid Mapping
Regression analysis
Rhesus monkey
Science
Science (multidisciplinary)
Selection, Genetic - genetics
Stratigraphy
Time Factors
Y chromosome
Y Chromosome - genetics
Title Strict evolutionary conservation followed rapid gene loss on human and rhesus Y chromosomes
URI https://link.springer.com/article/10.1038/nature10843
https://www.ncbi.nlm.nih.gov/pubmed/22367542
https://www.proquest.com/docview/953460014
https://pubmed.ncbi.nlm.nih.gov/PMC3292678
Volume 483
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