Epigenetics drive the evolution of sex chromosomes in animals and plants

Abstract

We review how epigenetics affect sex chromosome evolution in animals and plants. In a few species, sex is determined epigenetically through the action of Y-encoded small RNAs. Epigenetics is also responsible for changing the sex of individuals through time, even in species that carry sex chromosomes, and could favour species adaptation through breeding system plasticity. The Y chromosome accumulates repeats that become epigenetically silenced which leads to an epigenetic conflict with the expression of Y genes and could accelerate Y degeneration. Y heterochromatin can be lost through ageing, which activates transposable elements and lowers male longevity. Y chromosome degeneration has led to the evolution of meiotic sex chromosome inactivation in eutherians (placentals) and marsupials, and dosage compensation mechanisms in animals and plants. X-inactivation convergently evolved in eutherians and marsupials via two independently evolved non-coding RNAs. In Drosophila, male X upregulation by the male specific lethal (MSL) complex can spread to neo-X chromosomes through the transposition of transposable elements that carry an MSL-binding motif. We discuss similarities and possible differences between plants and animals and suggest future directions for this dynamic field of research. This article is part of the theme issue 'How does epigenetics influence the course of evolution?'

Keywords: X chromosome inactivation; X upregulation; Y degeneration; Y toxicity; imprinting; meiotic sex chromosome inactivation.

Figure 1.

Epigenetic mechanisms of sex determination in animals and plants. (a) In persimmons and poplars. (b) In silkworms. In all cases, sex-specific non-coding RNAs encoded by the Y or W chromosome regulate gene expression of genes located elsewhere in the genome (either on autosomes, on the pseudoautosomal region or on the X/Z) and determine the sex of individuals (see text for details).

Figure 2.

Epigenetics of Y degeneration and Y toxicity. (a) In moderately young Y chromosomes, numerous actively transcribed genes prevent the formation of heterochromatin on nearby TEs. This may lead to active TE transposition. (b) In moderately old Y chromosomes, few Y genes are surrounded by TEs. Heterochromatin marks spread to genes and prevent their expression, leading to further Y degeneration. (c) Heterochromatin marks get lost through ageing leading to active transposition of TEs. This phenomenon will be particularly prevalent in males with a Y chromosome and lead to Y toxicity. (Online version in colour.)

Figure 3.

Evolution of the epigenetics of dosage compensation in Drosophila and mammals. (a) In D. miranda, the neo-X chromosome evolved dosage compensation through transposition of a TE that carries an MSL-binding site. (b) In mammals, XCI evolved twice convergently in eutherians and marsupials through different mechanisms relying on different ncRNA (X-inactive specific transcript (Xist) and RNA-on-the-silent X (RSX)). In marsupials, XCI is imprinted where the paternal X (X_p) is inactivated while the maternal X (X_m) is upregulated compared to the autosomes (A). In eutherians, the active X (X_A) is upregulated compared to autosomes and the inactive X (X_I) is randomly picked between X_m or X_p in most cases. However, in mice, XCI is imprinted in the preimplantation embryo and in the extraembryonic lineages (see text). (Online version in colour.)