THE EVOLUTION OF HETEROMORPHIC SEX CHROMOSOMES

Abstract

The facts and ideas which have been discussed lead to the following synthesis and model. 1 Heteromorphic sex chromosomes evolved from a pair of homomorphic chromosomes which had an allelic difference at the sex-determining locus. 2 The first step in the evolution of sex-chromosome heteromorphism involved either a conformational or a structural difference between the homologues. A structural difference could have arisen through a rearrangement such as an inversion or a translocation. A conformational difference could have occurred if the sex-determining locus was located in a chromosomal domain which behaved as a single control unit and involved a substantial segment of the chromosome. It is assumed that any conformational difference present in somatic cells would have been maintained in meiotic prophase. 3 Lack of conformational or structural homology between the sex chromosomes led to meiotic pairing failure. Since pairing failure reduced fertility, mechanisms preventing it had a selective advantage. Meiotic inactivation (heterochromatinization) of the differential region of the X chromosome in species with heterogametic males and euchromatinization of the W in species with heterogametic females are such mechanisms, and through them the pairing problems are avoided. 4 Structural and conformational differences between the sex chromosomes in the heterogametic sex reduced recombination. In heterogametic males recombination was reduced still further by the heterochromatinization of the X chromosome, which evolved in response to selection against meiotic pairing failure. 5 Suppression of recombination resulted in an increase in the mutation rate and an increased rate of fixation of deleterious mutations in the recombination-free chromosome regions. Functional degeneration of the genetically isolated regions of the Y and W was the result. In XY males this often led to further meiotic inactivation of the differential region of the X chromosome, and in this way an evolutionary positive-feedback loop may have been established. 6 Structural degeneration (loss of material) followed functional degeneration of Y or W chromosomes either because the functionally degenerate genes had deleterious effects which made their loss a selective advantage, or because shorter chromosomes were selectively neutral and became fixed by chance. 7 The evolutionary routes to sex-chromosome heteromorphism in groups with female heterogamety are more limited than in those with male heterogamety. Oocytes are usually large and long-lived, and are likely to need the products of X- or Z-linked genes. Meiotic inactivation of these chromosomes is therefore unlikely. In the oocytes of ZW females, meiotic pairing failure is avoided through euchromatinization of the W rather than heterochromatinization of the Z chromosome. Since both chromosomes are euchromatic, recombination should occur. There is therefore no reason for the functional or structural degeneration of the W unless it is initiated by a reduction in crossing-over brought about by a structural change such as a paracentric inversion. A conformational difference between the homologues could have led to functional degeneration of the W only if meiotic pairing and recombination were uncoupled as they are in the Lepidoptera. 8 Sex-chromosome heteromorphism usually causes gene-dosage differences between males and females. In some organisms with male heterogamety, the mechanisms controlling meiotic X-inactivation in the spermatocyte were modified in ways which led to dosage compensation in the somatic cells. Since no meiotic inactivation mechanisms occur for Z chromosomes, dosage-compensation systems comparable to those found in species with male heterogamety could not evolve in species with femal heterogamety. 9 In marsupials, dosage compensation is brought about by preferential inactivation of the paternal X chromosomes in females. The general suppression of recombination observed in female marsupials could be a consequence of selection pressures resulting from preferential X-inactivation. 10 Sex-chromosome heteromorphism and the conformational changes of meiosis which are associated with it may be the reason why X chromosomes show more genomic imprinting than autosomes. The asymmetrical pattern of transmission of sex chromosomes may give parental imprinting a selective advantage. 11 Genetic changes affecting the conformation of sex chromosomes may be important causes of the sterility and inviability found in hybrids between individuals from populations which have diverged during periods of isolation.