Renovating a runt - the extreme evolution of the Y chromosome


Men who think that size really matters should probably not think too hard about the Y chromosome. This bundle of genes is the ultimate determinant of manliness, and it happens to be a degenerate runt.  Over a few hundred million years, it has shrunk considerably, jettisoning around 97% of its original genes. Where it was once a large library of genes, now it's more a struggling independent bookstore. This loss of information defined the youth of the Y chromosome but nowadays, things are different. Renovation is the order of the day.

Jennifer Hughes from MIT revealed the recent history of the Y chromosome by comparing the human and chimp versions. They are incredibly different. They have rapidly evolved since the two species last shared a common ancestor 6 million years ago. In this relatively short span of time, the two Ys have accumulated differences that other chromosomes would take 310 million years to build up. It's the sort of genetic disparity you'd expect to see between humans and chickens, not between us and our closest relatives!

This drastic remodelling contradicts the current view of Y evolution, which suggests that the chromosome has stagnated. It has lost so many of its genes that some scientists thought it might waste away altogether within another 10 million years. But rumours of its impending demise had been greatly exaggerated. In 2005, Hughes showed that Y isn't shrinking at the breakneck pace of old.

That result was based on a comparison of individual genes on the two chromosomes. Since then, Hughes has managed to fully sequence the chimp Y, the first time this has been accomplished for a non-human animal. Considering how small the chromosome is, sequencing it is remarkably tricky. It has lots of long, repetitive sequences that are subtly different and hard to tell apart through conventional means.

Nonetheless, Hughes managed it. By comparing the two sequences, she found that the Y chromosome is an island of difference in a sea of resemblance. The chimp and human genomes are famous for their similarity; they're a 98.8% match for each other. And indeed, where the chimp and human Y sequences align, they are a 98% match, just like the rest of the genome. But they don't align very well. Around 30% of the chimp Y chromosome has no human counterpart and vice versa.

This flies in the face of the idea that the Y chromosome is evolutionarily stagnant. Since our ancestors split from those of chimps, our Y chromosomes have become hotbeds of genetic change. They have gained and lost sequences with wanton abandon, to a much greater extent than the rest of the genome. Even the sequences that have remained have been grossly rearranged. If you looked at chromosome 21 from both species (which has also been thoroughly sequenced), you'd think you were looking at a pair of identical twins. If you looked at the two Y chromosomes, you'd think you were looking at distant and barely related cousins.

Despite these renovations, the human Y chromosome hasn't actually lost any of the genes that its ancestor had 6 million years ago (although it has picked up a few). The chimp Y chromosome, on the other hand, has lost or disabled many of its genes, so it has a much smaller portfolio than ours does.

The DNA of the Y chromosome falls into two main groups. The first group - the "X-degenerate segments" -contain versions of genes found on the X chromosome. They reflect the shared evolutionary history of the two sex chromosomes, both having evolved from a single ancestor that had nothing to do with determining sex.

The second group - the "ampliconic segments" - are more interesting and not just because they make Y so hard to sequence. These large, repetitive chunks of DNA contain many copies of genes that are activated in the testes. They have been the focus on much of the Y chromosome's recent remodelling. Half of the ampliconic sequences in the chimp Y have no human equivalent and vice versa.

What is it about the Y chromosome (and the chimp one, in particular) that makes it such an evolutionary hotbed? Hughes suggests three reasons. Firstly, its genes are incredibly important for making sperm and sperm is incredibly important for chimpanzees. Many males mate with the same female and it's the quality of their sperm that decides whether they actually father the next generation. This fierce competition is why a chimp's testicles are three times larger than a human's relative to its body size. It also means there's a lot of evolutionary pressure acting on the genes that produce the sperm.

Secondly, most chromosomes come in pairs. When they're duplicated, they temporarily fuse and cross over, providing an opportunity to exchange and shuffle their genes. But the Y chromosome is one-of-a-kind; it has nothing to cross over with. This makes any beneficial mutation on a Y gene all the more impactful. As this mutation spreads throughout the population, it drags nearby sequences along with it as genetic hitchhikers. In this way, a single mutation could change the evolutionary fate of the entire chromosome.

Finally, as I've mentioned, the Y chromosome is riddled with repetitive sequences. To understand their impact, imagine you had to copy out a long string of numbers. If groups of digits were repeated again and again, at some point you would probably copy a bit you'd already done, or mistakenly skip ahead and miss out an entire group of numbers.  The same things happen when your cells duplicate chromosomes with lots of repetitive DNA. Some bits go missing, some are duplicated, and some are flipped around. In DNA, repetition drives change.

Reference: Hughes et al. 2010. Chimpanzee and human Y chromosomes are remarkably divergent in structure and gene content. Nature

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Well -- this is interesting. If humans and chimps diverged 6mya, but gene flows between humans and chimps continued until 2mya -- then maybe the Y chromosome drove much of the speciation? Since you can't have crossover, maybe it can act as an island of stability to split and identify populations?

Maybe it continued to have such an effect in hominid evolution, given the bushiness of the human family tree (it would be even surprising that H. erectus & sapiens were mutually infertile -- so something must have been keeping the populations from merging).

Amazing! 23andMe posted this on their Facebook page. Then, I saw Science Blogs attached to it and immediately clicked the link.

Great post on genetics and evolution.

By Doug Pepe (not verified) on 13 Jan 2010 #permalink

I wonder if you'd find similar differences in the Y chromosomes of animals that have otherwise extremely similar genomes. For example, how different are the Y chromosomes of dogs versus wolves?

There are all kinds of implications coming from this wicked quick evolution of the human Y chromosome.
"Changes in sex chomosomes are often implicated in speciation through Haldanes rule." is a quote from John Hawks.
Is that the fat lady I hear singing for the multi regionalists? Was the human bottleneck of some 80,000 years ago caused by stress or a mutation/speciation event. Maybe all the human evolution theorists just have to wait for the science of genetics to advance further before making any conclusions.

By dave chamberlin (not verified) on 14 Jan 2010 #permalink

Gee, Interesting read... This is my first scienceblog. I forgot that tht Y Chromosome is such a small part of the equation!!! It good to hear that the male isn't going to be extinct soon.

Ed, you're making a basic error in interpretation in this piece. You cannot simply compare chimp and human sequence and deduce how much human sequence has changed since the lines diverged. Chimp sequence is not the same as the common ancestor sequence. The way genomicists deal with this question is to use the genomic sequence of a third (or better still a third and fourth species) to figure out what was the ancestral sequence. In that way we can work out which one, the human or the chimp, has changed. This has been done with the autosomal sequences but not the Y chromosome.
The large differences seen in this paper could, in theory be due to only one species, either the chimp or the human, showing large changes since divergence. Most likely both species have changed (the regions of difference are gene poor genomic deserts and as such are probably under little selective constraint and thus liable to pick up repetitive sequences). I'm also a little wary about the theory that chimps large testicle size has much to do with their Y chromosome. It's possible, of course but we have to remember that most of the genes associated with sperm production and testicle development are located not on the Y chromosome but on the autosomes.

Hmm - you could use this to argue that men are less like animals (or at least chimpanzees) than women, contrary to stereotypes that men are animals :)

"Hmm - you could use this to argue that men are less like animals (or at least chimpanzees) than women, contrary to stereotypes that men are animals :)"

Absolutely not. You could only say the Y chromosome has changed more; you can't make any claim about what direction it has changed in. For all we know it's made men *more* like chickens than chimps. =)