A single theory for the evolution of sex chromosomes and the two rules of speciation.

Abstract

Sex chromosomes are involved in three major empirical patterns: (i) Y (or W) chromosomes are often nonrecombining and degenerate; (ii) heterogametic offspring (XY or ZW) from interspecific crosses are more often sterile or inviable compared with homogametic offspring (Haldane's rule); and (iii) the X (or Z) has a disproportionately large effect on reproductive isolation between species compared with autosomes (the large X effect). Each observation has received its own tailored explanation involving multiple genetic and evolutionary causes. In this work, we show that these empirical patterns all emerge from a single theory for sex chromosome evolution incorporating the coevolution of cis- and trans-acting regulators of gene expression and leading to systematic misexpression of dosage-compensated genes in heterogametic F1 hybrids, for both young and old sex chromosomes.