Y Chromosome Evolution

Before Y-chromosome

Many ectothermic vertebrates have no sex chromosomes. If they have different sexes, sex is determined environmentally rather than genetically. For some of them, especially reptiles, sex depends on the incubation temperature; others are hermaphroditic (meaning they contain both male and female gametes in the same individual).

Origin

The X and Y chromosomes evolved from a pair of identical chromosomes, termed autosomes, when an ancestral mammal developed an allelic variation, a so-called 'sex locus' - simply possessing this allele caused the organism to be male. The chromosome with this allele became the Y chromosome, while the other member of the pair became the X chromosome. Over time, genes which were beneficial for males and harmful to (or had no effect on) females either developed on the Y chromosome, or were acquired through the process of translocation..

Until recently, the X and Y chromosomes were thought to have diverged around 300 million years ago. However recent research, particularly that stemming from the sequencing of the platypus genome.

Recombination inhibition

Recombination between the X and Y chromosomes proved harmful - it resulted in males without necessary genes formerly found on the Y chromosome, and females with unnecessary or even harmful genes previously only found on the Y chromosome. As a result, genes beneficial to males accumulated near the sex-determining genes, and recombination in this region was suppressed in order to preserve this male specific region. Comparative genomic analysis, however, reveals that many mammalian species are experiencing a similar loss of function in their heterozygous sex chromosome. Degeneration may simply be the fate of all nonrecombining sex chromosomes due to three common evolutionary forces: high mutation rate, inefficient selection and genetic drift . On the other hand, recent comparisons of the human and chimpanzee Y chromosomes show that the human Y chromosome has not lost any genes since the divergence of humans and chimpanzees between 6-7 million years ago, providing direct evidence that the linear extrapolation model may be flawed.

High Mutation Rate

The human Y chromosome is particularly exposed to high mutation rates due to the environment that it is housed in. The Y chromosome is passed exclusively through sperm, which undergo multiple cell divisions during gametogenesis. Each cellular division provides further opportunity to accumulate base pair mutations. Additionally, sperm are stored in the highly oxidative environment of the testis, which encourages further mutation. These two conditions combined put the Y chromosome at a risk of mutation 4.8 times greater than the rest of the genome.

Inefficient Selection

Without the ability to recombine during meiosis, the Y chromosome is unable to expose individual alleles to natural selection. Deleterious alleles are allowed to "hitchhike" with beneficial neighbors, thus propagating maladapted alleles in to the next generation. Conversely, advantageous alleles may be selected against if they are surrounded by harmful alleles (background selection). This inability to sort through its gene content, the Y chromosome is particularly prone to the accumulation of "junk" DNA. Massive accumulations of retrotransposable elements are scattered throughout the Y . The random insertion of DNA segments often disrupt encoded gene sequences and render them nonfunctional. However, the Y chromosome has no way of weeding out these "jumping genes". Without the ability to isolate alleles, selection cannot effectively act upon them.

Genetic Drift

Even if a well adapted Y chromosome manages to maintain genetic activity by avoiding mutation accumulation, there is no guarantee it will be passed down to the next generation. The population size of the Y chromosome is inherently limited to 1/4 that of autosomes: diploid organisms contain two copies of autosomal chromosomes while only half the population contains 1 Y chromosome. Thus, genetic drift is an exceptionally strong force acting upon the Y chromosome. Through sheer random assortment, an adult male may never pass on his Y chromsome if he only has female offspring. Thus, although a male may have a well adapted Y chromosome free of excessive mutation, it may never make it in to the next gene pool. The repeat random loss of well-adapted Y chromosomes, coupled with the tendency of the Y chromosome to evolve to have more deleterious mutations rather than less for reasons described above, contributes to the species-wide degeneration of Y chromosomes through Muller's Ratchet.

Gene conversion

In 2003, researchers from MIT discovered a process which may slow down the process of degradation.

They found that human Y chromosome is able to "recombine" with itself, using palindrome base pair sequences. Such a "recombination" is called gene conversion or ''recombinational loss of heterozygosity'' (RecLOH).

In the case of the Y chromosomes, the palindromes are not junk DNA; these strings of bases contain functioning genes important for male fertility. Most of the sequence pairs are greater than 99.97% identical. The extensive use of gene conversion may play a role in the ability of the Y chromosome to edit out genetic mistakes and maintain the integrity of the relatively few genes it carries. In other words, since the Y chromosome is single, it has duplicates of its genes on itself instead of having a second, homologous, chromosome. When errors occur, it can use other parts of itself as a template to correct them.

Findings were confirmed by comparing similar regions of the Y chromosome in humans to the Y chromosomes of chimpanzees, bonobos and gorillas. The comparison demonstrated that the same phenomenon of gene conversion appeared to be at work more than 5 million years ago, when humans and the non-human primates diverged from each other.

Future evolution

In the terminal stages of the degeneration of the Y chromosome, other chromosomes increasingly take over genes and functions formerly associated with it. Finally, the Y chromosome disappears entirely, and a new sex-determining system arises. Several species of rodent in the sister families Muridae and Cricetidae have reached these stages, in the following ways:

The Transcaucasian mole vole, ''Ellobius lutescens'', the Zaisan mole vole, ''Ellobius tancrei'', and the Japanese spinous country rats ''Tokudaia osimensis'' and ''Tokudaia muenninki'', have lost the Y chromosome and SRY entirely. ''Tokudaia'' spp. have relocated some other genes ancestrally present on the Y chromosome to the X chromosome. Both genders of ''Tokudaia'' spp. and ''Ellobius lutescens'' have an XO genotype, whereas all ''Ellobius tancrei'' possess an XX genotype. The new sex-determining system for these rodents remains unclear.
The wood lemming ''Myopus schisticolor'', the arctic lemming, ''Dicrostonyx torquatus'', and multiple species in the grass mouse genus ''Akodon'' have evolved fertile females who possess the genotype generally coding for males, XY, in addition to the ancestral XX female, through a variety of modifications to the X and Y chromosomes.
In the creeping vole, ''Microtus oregoni'', the females, with just one X chromosome each, produce X gametes only, and the males, XY, produce Y gametes, or gametes devoid of any sex chromosome, through nondisjunction.

Outside of the rodent family, the black muntjac, ''Muntiacus crinifrons'', evolved new X and Y chromosomes through fusions of the ancestral sex chromosomes and autosomes. Primate Y chromosomes, including in humans, have degenerated so much that primates will also evolve new sex determination systems relatively soon, in about 14 million years in humans.