Trends in Ecology & Evolution
ReviewThe evolution of restricted recombination in sex chromosomes
Section snippets
Introduction to separate sexes and sex chromosomes
Sex determination can be controlled by environmental cues, but is frequently genetic, often involving a pair of morphologically distinguishable ‘sex chromosomes’ (Box 1; Table 1). The XY chromosome systems of diploids such as mammals (Figure 1) are well known; males are ‘heterogametic,’ with the chromosome genotype XY, and females are XX. In some organisms, including birds and snakes, females are the heterogametic sex (ZW), whereas males are ZZ.
It has long been understood that, despite their
When did sex chromosomes evolve?
Transitions from hermaphroditism to dioecy have occurred in many animals, land plants and algae (Box 1). In mammals and birds, dioecy evolved long ago. The X (or W) chromosomes are homologous in different orders, and the XY (or ZW) pair is often heteromorphic. Identification and sequencing of genes in the MSY regions of several species ha allowed divergence to be measured between allelic X and Y (or Z and W) sequences, and the origins of some sex chromosomes can now be dated, using molecular
When did recombination stop? Evolutionary strata
A surprising revelation when divergence times of X-Y gene pairs were estimated (initially for human sex chromosomes) is that sex chromosomes do not have a single age, but that divergence levels of different genes vary (Figure 2), forming ‘evolutionary strata’ [3]. Specifically, gene pairs with X copies distant from one of the two human pseudo-autosomal regions (PAR1) have very high X-Y divergence, consistent with a pre-eutherian mammal origin, whereas pairs with X copies nearer this PAR are
Do small MSY regions represent young sex chromosomes?
In some birds and snakes, recombination is not suppressed throughout the whole ZW pair, and the sex chromosomes are cytologically similar and carry similar genes. The female-specific regions of their W chromosomes are therefore probably small (Table 1). However, these bird and snake taxa evolved long ago. Their sex chromosomes (clearly homologous to the heteromorphic ZW pairs of later-branching taxa) did not evolve recently (neglecting the unlikely possibility that the same chromosome evolved
Evolution of suppressed recombination
Box 3 outlines the theory for why natural selection reduces recombination as dioecy evolves. For selection to promote reduced recombination in a genome region, polymorphism at two or more different genes is required; certain combinations of alleles at these loci must be favoured, and recombinant combinations disfavoured. The evolution of dioecy probably involves sexually antagonistic genes; these are genes with alleles that have advantageous effects in one sex but disadvantageous effects in the
Modifications of sex chromosomes
Once sex chromosomes evolve, they are sometimes modified in further ways. Additions of autosomal regions, resulting in neo-sex chromosomes, have already been mentioned (Box 1). Changes from XY to ZW systems have repeatedly occurred, and modern methods such as chromosome in situ hybridisation are making it possible to study the details, although the evolutionary forces involved are not yet fully understood [23]. Another possibility is that a species with genetic sex determination evolves a new
Consequences of suppressed recombination. I. Genetic degeneration of sex chromosome regions
The evolution of non-recombining MSY regions profoundly affects evolution of the genes within them, especially if these are large genome regions containing many genes. Genetic degeneration of Y (and W) chromosomes (see Box 1) is one important effect. It was once thought that, in diploid organisms, the sex chromosome that is always heterozygous could lose genes or accumulate loss-of-function mutations without reduced fitness. However, such mutations are rarely completely recessive [28], so
Consequences of suppressed recombination. II. Changes in sex chromosome morphology
Heteromorphic sex chromosomes can arise when the sex chromosomes expand by translocations (Box 1). Heteromorphism can, however, evolve without such additions (Figure 3). After recombination stops between the sex chromosomes, repetitive sequences and transposable elements are predicted to accumulate rapidly (stage 3 of Figure 3). This may precede gene degeneration [34]. Several non-coding neo-Y regions of D. miranda have higher densities of transposable elements compared with the homologous X
Fungal mating-type regions
Some fungal mating-type regions evolve similarly to Y chromosomes in several respects, supporting the evidence (see above) that lack of recombination is the reason for these strange evolutionary behaviours. These regions may have evolved suppressed recombination to maintain correct combinations of mating pheromones and receptors (for references, see Table 1).
Like MSY regions, the homologous regions quickly become highly rearranged [45], and sometimes genes have been lost from one homologue or
Conclusions
It is clear that several events were involved in the loss of recombination between the sex chromosomes of mammals, plants and birds, and even in the mating-type region of a fungus [47]. In all three well-studied sex chromosome systems, divergence values of gene pairs increase with distance from the X or Z PAR (Figure 2). Even though there is always variability and uncertainty in divergence estimates, so that estimates of the times when recombination stopped in the strata are not precise, it is
Acknowledgements
We thank the BBSRC for support and Vera Kaiser for discussions.
Glossary
- BAC clone
- genome region of around 100 kb cloned in a bacterial artificial chromosome (for sequencing and detailed study).
- Dosage compensation
- altered gene expression in one or both of the two sexes that restores the proper balance between sex-linked and autosomal genes in both sexes.
- Evolutionary strata
- regions of the sex chromosomes which stopped recombining with their homologues at different times in the past, and therefore have different X-Y sequence divergence values.
- Fitness
- relative survival
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