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Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration

Nature Reviews Genetics volume 14, pages 113–124 (2013)Cite this article

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Key Points

  • Recently developed genomic technologies have shed light on the genomic composition of the ancient Y chromosomes of some primates and Drosophila melanogaster and have shown that Y chromosomes in these species largely conform to the previously held view of being degenerate.

  • The presence of evolutionary strata confirmed by genome sequencing of the sex chromosomes supports that Y-chromosome degeneration occurred through successive arrest of recombination over time. In addition, the enrichment of Y chromosomes for genes of male-beneficial functions suggests that sexually antagonistic mutations may have a role in Y-chromosome evolution.

  • Genome sequencing of young Y chromosomes in plants and neo-Y chromosomes in Drosophila spp. have provided insight into the molecular processes that trigger initiation of Y-chromosome degeneration. Empirical evidence suggests that gene silencing occurs before pseudogenization.

  • Empirical observations in Drosophila neo-sex chromosomes, primate Y chromosomes and theoretical models and computer simulations show that degeneration is not a linear process, and so Y chromosomes in these species will probably not completely degenerate in the future.

Abstract

The human Y chromosome is intriguing not only because it harbours the master-switch gene that determines gender but also because of its unusual evolutionary history. The Y chromosome evolved from an autosome, and its evolution has been characterized by massive gene decay. Recent whole-genome and transcriptome analyses of Y chromosomes in humans and other primates, in Drosophila species and in plants have shed light on the current gene content of the Y chromosome, its origins and its long-term fate. Furthermore, comparative analysis of young and old Y chromosomes has given further insights into the evolutionary and molecular forces triggering Y-chromosome degeneration and into the evolutionary destiny of the Y chromosome.

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Figure 1: A model for the differentiation of sex chromosomes.
Figure 2: Neo-sex chromosomes in Drosophila spp.
Figure 3: Evolutionary dynamics of Y-chromosome degeneration.

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Acknowledgements

The author is funded by US National Institutes of Health grants (R01GM076007 and R01GM093182) and a Packard Fellowship.

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    Doris Bachtrog

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Glossary

Sex chromosomes

A pair of chromosome that determines the sex of an individual.

Genomic conflict

Conflict of different genes within an organism that arises when genes inside a genome are not transmitted by the same rules (such as mitochondria or nuclear genes) or when the transmission of a particular gene is increased to the detriment of other parts of the genome.

Y-chromosome degeneration

The process of gene loss from the Y chromosome.

Recombination

The breaking and rejoining of DNA strands to form a new combination of genetic information.

Heterochromatic

Heterochromatin is a tightly packed form of DNA that is typically genetically inactive and contains repetitive sequences and few genes.

B chromosome

A supernumerary chromosome that is not essential for the life of a species and that is present in only some of the individuals of a species.

Position effect variegation

(PEV). The variable, heritable suppression of genes by their juxtaposition to heterochromatin or telomeres or by movement of a gene into a different nuclear domain or chromosomal context.

Palindromes

A DNA sequence composed of two inverted repeats (arms) separated by a short spacer.

Heteromorphic sex chromosomes

A pair of chromosomes that is morphologically distinct.

Homomorphic sex chromosomes

A pair of chromosomes that is morphologically indistinguishable.

Proto-sex chromosomes

A new pair of chromosomes that (recently) acquired a sex-determining function but that otherwise contains identical genes.

Sexually antagonistic mutations

A mutation that is beneficial to one sex but detrimental to the other.

Genetic linkage

The tendency of genes that are proximal to each other on a chromosome to be inherited together.

Chromosomal inversions

A chromosome rearrangement in which a segment of a chromosome is reversed end to end.

Beneficial mutation

A mutation that increases the survivorship or fecundity (fitness) of its carrier.

Deleterious mutation

A mutation that decreases the survivorship or fecundity (fitness) of its carrier.

Dosage compensation

A process that balances expression of sex-linked and autosomal genes in the heterogametic sex.

Muller's ratchet

The irreversible accumulation of deleterious mutations in a non-recombining population.

Genetic hitchhiking

The fixation of a deleterious mutation that is linked to a beneficial allele.

Ruby in the rubbish model

The selective elimination of a beneficial mutation that is linked to a deleterious allele.

Female heterogametic

Female heterogamety describes a species in which males have two Z chromosomes and females have a Z and a W chromosome.

Male heterogamety

A species in which females have two X chromosomes and males have an X and a Y chromosome.

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Bachtrog, D. Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat Rev Genet 14, 113–124 (2013). https://doi.org/10.1038/nrg3366

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