Evolutionary Strata on the Mouse X Chromosome Correspond to Strata on the Human X Chromosome

Abstract

Lahn and Page previously observed that genes on the human X chromosome were physically arranged along the chromosome in "strata," roughly ordered by degree of divergence from related genes on the Y chromosome. They hypothesized that this ordering results from a historical series of suppressions of recombination along the mammalian Y chromosome, thereby allowing formerly recombining X and Y chromosomal genes to diverge independently. Here predictions of this hypothesis are confirmed in a nonprimate mammalian order, Rodentia, through an analysis of eight gene pairs from the X and Y chromosomes of the house mouse, Mus musculus. The mouse X chromosome has been rearranged relative to the human X, so strata were not found in the same physical order on the mouse X. However, based on synonymous evolutionary distances, X-linked genes in M. musculus fall into the same strata as orthologous genes in humans, as predicted. The boundary between strata 2 and 3 is statistically significant, but the boundary between strata 1 and 2 is not significant in mice. An analysis of smaller fragments of Smcy, Smcx, Zfy, and Zfx from seven species of Mus confirmed that the strata in Mus musculus were representative of the genus Mus.

The Chicken (Gallus gallus) Z Chromosome Contains at Least Three Nonlinear Evolutionary Strata

“…In mammals, the evolutionary strata identified on the human X chromosome are also seen on the mouse X chromosome (Sandstedt and Tucker 2004). However, these strata are not ordered linearly along the mouse X, similar to what we observe for the chicken Z.…”

“…However, these strata are not ordered linearly along the mouse X, similar to what we observe for the chicken Z. This has been explained by X chromosome rearrangements in the rodent lineage subsequent to the split from primates, breaking up the strict correlation between divergence of X-Y gametologs and physical position on the X (Sandstedt and Tucker 2004). A similar explanation is also reasonable for birds.…”

“…Moreover, the consistent observation of a Z-linked gametolog for genes on the chicken W chromosome suggests that the proteincoding content of avian W largely derives from a degenerating protosex chromosome, without the addition of autosomal sequences, through processes that include translocation or transposition. The consecutive expansions of the nonrecombining region on the avian Z chromosome mirrors the situation in both mammals (Lahn and Page 1999;Sandstedt and Tucker 2004;Ross et al 2005) and dioecious plants of the genus Silene (Filatov 2005;Nicolas et al 2005;Zluvova et al 2005;Bergero et al 2007), two systems with male heterogamety. The observation of this pattern in highly divergent phylogenetic lineages of male as well as female heterogamety suggests that progressive restriction of recombination generating evolutionary strata is an inherent theme of sex chromosome evolution (Charlesworth et al 2005).…”

Rapid divergence and expansion of the X chromosome in papaya

“…In mammals, the gene order in the X chromosomes has been conserved across such distantly related species as human, cat, horse, cattle, and elephant, with the exception of mouse (22)(23)(24)(25)(26). In the human X and chicken Z, gene trafficking and sequence expansion have been detected, using comparisons with orthologous autosomal segments of other species (12)(13)(14).…”

Evolutionary Strata in a Small Mating-Type-Specific Region of the Smut Fungus Microbotryum violaceum

“…Regardless of the phylogenetic position of a species, such nonrecombining regions are known to follow similar evolutionary trajectories. The nonrecombining region on the sexspecific chromosome expands in several steps, forming evolutionary strata-regions of different X/Y (or Z/W) divergence (Lahn and Page 1999;Handley et al 2004;Sandstedt and Tucker 2004;Nicolas et al 2005)-and genes in the nonrecombining regions gradually accumulate deleterious mutations that eventually render them dysfunctional Charlesworth 2008).…”