Rodents Race to Survive

September 19th, 2006 Placozoan Posted in News |

RECENTLY PURDUE UNIVERSITY published a short news article talking about the unusual evolutionary track of the vole. Apparently the vole has been evolving at high speed, speciating 60-100 times faster than other vertebrates. A key factor in this high rate of speciation is variable chromosome numbers, as with the domestic mouse. The chromosome number ranges from 17-64, although the vole common ancestor probably had 56.

It’s been known for quite a while that several species of rodent rearrange their chromosomes frequently. A recent study on the common vole and one of the rodents most famous for this, the northern mole vole, shows that this is probably due to environmental stress related to population demographics and population cycles (Bol’shakov, V.; Gileva, E.; Yalkovshaya, L. “Species-specific features of inter- and intrapopulation variation in the level of chromosome instability in rodents.” Russian Journal of Ecology. 2003, 34, 314-319.) These rodents’ ability to reproduce and evolve very rapidly have enabled them to spread over wide ranges, and in the case of the domestic mouse, worldwide.

Some of the extraordinary variation in the vole is due to remodeling of the sex chromosomes. From the Purdue article:

A review of the literature shows that in the creeping vole, whose males and females have different chromosome numbers, the cause is a mutant X chromosome called X’. Females in this species are X’0, males are X’Y. The original X chromosome has been lost. Nondisjunction occurs during meosis 1 so that in females, XX and 00 daughter cells are produced. The 00 cell is nonviable, so the X’X’ cell produces two X’ carrying gametes. In the male, X’X'Y and 0Y daughter cells are produced. The X’X'Y cell is nonviable so only 0 and Y gametes are produced. The mutant X’ probably built up in the population until genetic drift in subpopulations amplified X’ to a high enough frequency that it swamped out the now extinct X chromosome. (“A model of the evolution of the unusual sex chromosome system of Microtus oregoni.” Charlesworth, B.; Dempsey, N. Heredity. 2001, 86, 387-394.)

This is just one of the usual detours the sex chromosomes have taken during evolutionary history. This topic is truly fascinating, but unfortunately there is no way I could adequately cover this topic in a blog article, so I’ll point you towards an excellent review article by Jennifer Graves and Swathi Shetty (“Sex from W to Z: evolution of vertebrate sex chromosomes and sex determining genes.” Graves, J; Shetty, S. Journal of Experimental Zoology. 2001, 290, 449-462.)

For a very brief summary, our X:Y chromosomal system is a fairly recent development. Among the reptiles one of a variety of different sex determination systems may be used. These include a ZZ male:ZW female system, a XY male:XX female system, genetic sex determination by genes not on a sex chromosome, and temperature sex determination. The birds apparently branched off from a group of reptiles using the ZZ:ZW system and still have similar sex chromosomes. The branch that led to the mammals apparently started off with an XX:XY system. A region of the X chromosome conserved in placental mammals, marsupials, and monotremes was determined to be at least 170 million years old.

The monotremes, the echidna and platypus, have a relatively large Y chromosome whose long arm pairs with the X chromosome short arm. This is unfortunately a dramatic simplification of their sex chromosome system, since platypuses actually have five types of X chromosomes and five types of Y chromosomes! One X and one Y have been determined to be the “real” X and Y, the others have been described as “hijacked autosomes.” These were originally autosomal chromosomes that got drafted into being sex chromosomes after a Robertsonian translocation stuck an arm onto them that was homologous with the Y chromosome long arm/X chromosome short arm. Echidnas likewise have multiple sex chromosomes. Another oddity is that monotremes don’t seem to have the SRY gene that is critical for testis development in placental mammals. This has led to speculation that the mammal common ancestor may not have been committed to either the XX:XY or WW:WZ system, and monotremes got the WW:WZ system while the other mammals got the XX:XY system. However, it appears that the largest X chromosome and the first in the monotreme chromosomal chain is homologous to the other mammals’ X chromosome, casting doubt on this hypothesis (“Autosomal location of genes from the conserved mammalian X in the platypus (Ornithorhynchus anatinus): implications for mammalian sex chromosome evolution.” Waters, P., et al. Chromosome Research. 2005, 13, 401-410.) Unfortunately there’s again not enough room to discuss the monotreme sex chromosome system in detail, but you can read about it in “Chromosome chains and platypus sex: kinky connections” (Ashley, T. BioEssays. 2005, 27, 681-684.)

The marsupials, which arrived later on the evolutionary scene, are unusual in having a tiny, degenerate Y chromosome that completely fails to pair and recombine with the X chromosome. However, the sex chromosomes operate slightly different from placental mammals’ sex chromosomes. The Y chromosome controls testis development, but a gene on the X chromosome controls whether the marsupial embryo develops a scrotum or a pouch with mammary glands.

The placental mammal Y chromosome is slightly larger by virtue of its appropriation of a section of autosomal DNA since the divergence of mammals and marsupials. The X chromosome likewise contains some genetic material that appears on autosomal chromosomes in marsupials. The placental mammal Y chromosome pairs with the X chromosome and recombines over a small segment called the pseudoautosomal region.

This failure to recombine leads to a dilemma for the Y chromosome. According to the principle of Muller’s ratchet, DNA that doesn’t recombine (whether in a species reproducing asexually or on a non-recombining chromosome) tends to build up negative mutations and gradually shorten with imperfect replication. The Y chromosome has survived this long by appropriating material from other chromosomes and by having a good part of its sequence be palindromic, so it can turn back in a hairpin and recombine with itself! However, the Y chromosome’s millions of years may be numbered. The mole vole, mentioned above, has managed to do away with the Y chromosome, including the SRY gene that is critical for sex determination in other mammals. Apparently a new sex determination gene has originated on some other autosomal chromosome–which may be destined to be the future Y chromosome as the inevitable process of sex-related gene isolation and inhibition of recombination which produced the original Y chromosome runs its course. It’s quite likely in the future that other species will likewise eliminate the Y chromosome, and eventually the XX:XY chromosome set that we know will be extinct.

In some species a lot of Y chromosome material has been transferred to the X chromosome, including the genes usually used in sex determination in the male. In others, the X chromosome packs onto it much more information than usually is present. While the first may result in the eventual death of the Y chromosome and the dawn of a new Y chromosome with a new sex determining master gene, the second is more likely to result in further autosomal rearrangement in future as the X chromosome jettisons some of its heavy load. While it would be fascinating to see what will happen, we are unfortunately limited to peering into the past. Fortunately voles and other chromosomally unstable rodents have given us a lot of insight into chromosome remodelling and its role in past speciation events, including our own.