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  • Review Article
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The human Y chromosome, in the light of evolution

Nature Reviews Genetics volume 2, pages 207–216 (2001)Cite this article

Abstract

Most eukaryotic chromosomes, akin to messy toolboxes, store jumbles of genes with diverse biological uses. The linkage of a gene to a particular chromosome therefore rarely hints strongly at that gene's function. One striking exception to this pattern of gene distribution is the human Y chromosome. Far from being random and diverse, known human Y-chromosome genes show just a few distinct expression profiles. Their relative functional conformity reflects evolutionary factors inherent to sex-specific chromosomes.

Key Points

  • Sex chromosomes have arisen many times in the living world and show striking examples of convergent similarity that reflect shared evolutionary modes in the emergence and maintenance of chromosomal sex determination.

  • Owing to reduced recombination, sex-specific chromosomes tend to be small and gene-poor overall, but might be relatively enriched for genes specifically benefiting the sex that harbours them.

  • The human X and Y chromosomes are the best-characterized sex-chromosome system. They have progressively diverged from each other, via blockwise recession of their mutually recombining regions towards each telomere, probably mediated by large-scale inversions of intervening sequence on the Y chromosome in particular.

  • Studies of the human Y chromosome highlight the accumulation of spermatogenesis genes and the overall functional decay typical of male-specific chromosomes.

  • The known active genes on the non-recombining portion of the human Y chromosome sort neatly, on the basis of tissue expression and homology to the X chromosome, into three basic classes.

    Class 1: housekeeping genes that have withstood the overall decay of the Y chromosome, attesting to its ancient homology with the X chromosome, on which highly similar copies of these genes elude inactivation.

    Class 2: testis-specific genes — generally recruited to the Y chromosome by translocation or retroposition — that specifically benefit male fitness.

    Class 3: genes variously similar to both classes 1 and 2, as well as other genes that might be decaying towards pseudogene status, or the persistence of which might reflect additional evolutionary factors at work on the Y chromosome.

  • Genes that belong to classes 1 and 2 seem to underlie the medical disorders Turner syndrome and male infertility, respectively.

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Figure 1: Active genes on the human Y chromosome.
Figure 2: Sex chromosomes in mammals.
Figure 3: Human sex-chromosome evolution.
Figure 4: Example of a Y-chromosome-linked trait.
Figure 5: Amelogenin gene-splicing patterns.

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Acknowledgements

We thank B. Charlesworth, S. Dorus, R. Hudson, M. Kreitman, E. Stahl, A. Veis, G. Wyckoff and S. Yi for stimulating discussion; G. Wyckoff for computational support; and C. Andrews and J. Socha for help with the guppies.

Author information

Authors and Affiliations

  1. Department of Human Genetics, Howard Hughes Medical Institute, University of Chicago, 920 East 58th Street, Chicago, 60637, Illinois, USA

    Bruce T. Lahn & Nathaniel M. Pearson

  2. Department of Ecology and Evolution, University of Chicago, 920 East 58th Street, Chicago, 60637, Illinois, USA

    Nathaniel M. Pearson

  3. National Human Genome Research Institute, National Institutes of Health, 9,000 Rockville Pike, Bethesda , 20892, Maryland, USA

    Karin Jegalian

Authors
  1. Bruce T. Lahn
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  2. Nathaniel M. Pearson
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  3. Karin Jegalian
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Related links

Related links

DATABASE LINKS

SYBL1

HSPRY3

SRY

SOX3

AMELY

PCDHY

AMELX

PCDHX

RBMY

VCY

RBMX

VCX

Zfy

Ube1y

Usp9y

CDY

DAZ

CDYL

DAZL

Turner syndrome

male infertility

SHOX

AZF

DBY

Stellate

crystal

FURTHER INFORMATION

Human Genome Project

Glossary

DIOECIOUS

Having separate male and female organisms.

BIPOTENTIAL GONAD

The last embryonic tissue precursor that can differentiate into either the ovary or the testis.

CLADE

An organismal lineage comprising an ancestor and all its descendants.

HOMEOTHERM

An organism that uses cellular metabolism specifically to stabilize its own body temperature.

PENETRANCE

The frequency of affected individuals among the carriers of a particular genotype.

MEROHAPLODIPLOID

Characterized by one sex lacking part, but less than half, of the diploid chromosome set typical of the other sex.

GENETIC DRIFT

The random fluctuation of allele frequencies across generations in a finite population.

EFFECTIVE POPULATION SIZE (Ne).

The theoretical number of organisms or copies of a locus for which the genetic variation in a given sample of the organisms or copies can be explained solely by mutation and genetic drift; Ne is related to, but never exceeds, the actual population size (N).

PARALOGUE

A locus that is homologous to another within the same haploid genome.

MARSUPIAL

Non-placental mammal whose liveborn young suckle in maternal pouches.

HAPLORHINE

A member of the clade comprising apes, monkeys and tarsiers only.

POLYANDRY

A population mating structure in which a female might mate with multiple males during her lifetime.

MEIOTIC DRIVE

Preferential transmission of one gamete genotype over another genotype, in which the genotypes in question might derive from the same meiosis.

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Lahn, B., Pearson, N. & Jegalian, K. The human Y chromosome, in the light of evolution. Nat Rev Genet 2, 207–216 (2001). https://doi.org/10.1038/35056058

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  • DOI: https://doi.org/10.1038/35056058

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