The male-specific Y chromosome plays a critical role in sex determination and male fertility. However, because of its repetitive nature, it is frequently absent from genome assemblies and remains enigmatic. In new research, a team of scientists at Penn State University has sequenced and assembled the Y chromosome of the bonobo (Pan paniscus) and the Sumatran orangutan (Pongo abelii). They’ve also reconstructed the ancestral Y chromosome of great apes by comparing three existing (gorilla, human, and chimpanzee) and two new Y chromosome assemblies, and found that many of their repetitive sequences and multicopy genes were likely already present in their common ancestor.
Cechova et al. reconstructed the ancestral sequence of the great ape Y chromosome by comparing three existing (gorilla, human, and chimpanzee) and two newly-generated (orangutan and bonobo) Y chromosome assemblies. Image credit: Dani Zemba and Monika Cechova, Penn State University.
The Y chromosome is unusual. It contains relatively few genes, many of which are involved in male sex determination and sperm production; large sections of repetitive DNA, short sequences repeated over and over again; and large DNA palindromes, inverted repeats that can be many thousands of letters long and read the same forwards and backwards.
A previous analysis of human, chimpanzee, and gorilla sequences revealed some unexpected patterns: humans are more closely related to chimpanzees, but for some characteristics, the human Y hromosome was more similar to the gorilla Y.
“If you just compare the sequence identity, humans are more similar to chimpanzees, as you would expect,” said senior author Professor Kateryna Makova, a researcher in the Department of Biology at Penn State University.
“But if you look at which genes are present, the types of repetitive sequences, and the shared palindromes, humans look more similar to gorillas. We needed the Y chromosome of more great ape species to tease out the details of what was going on.”
Professor Makova and colleagues sequenced the Y chromosome of a bonobo, a close relative of the chimpanzee, and an orangutan, a more distantly related great ape.
With these new sequences, they could see that the bonobo and chimpanzee shared the unusual pattern of accelerated rates of DNA sequence change and gene loss, suggesting that this pattern emerged prior to the evolutionary split between the two species.
The orangutan Y chromosome, on the other hand, which serves as an outgroup to ground the comparisons, looked about like what you expect based on its known relationship to the other great apes.
“Our hypothesis is that the accelerated change that we see in chimpanzees and bonobos could be related to their mating habits,” said co-author Rahulsimham Vegesna, a graduate student in the Department of Biology and the Intercollege Graduate Program in Bioinformatics and Genomics at Penn State University.
“In chimpanzees and bonobos, one female mates with multiple males during a single cycle. This leads to what we call ‘sperm competition,’ the sperm from several males trying to fertilize a single egg.”
“We think that this situation could provide the evolutionary pressure to accelerate change on the chimpanzee and bonobo Y chromosome, compared to other apes with different mating patterns, but this hypothesis, while consistent with our findings, needs to be evaluated in subsequent studies.”
In addition to teasing out some of the details of how the Y chromosome evolved in individual species, the team used the set of great ape sequences to reconstruct what the Y chromosome might have looked like in the ancestor of modern great apes.
“Having the ancestral great ape Y chromosome helps us to understand how the chromosome evolved,” Vegesna said.
“For example, we can see that many of the repetitive regions and palindromes on the Y were already present on the ancestral chromosome. This, in turn, argues for the importance of these features for the Y chromosome in all great apes and allows us to explore how they evolved in each of the separate species.”
“Working on the Y chromosome presents a lot of challenges,” said co-author Dr. Paul Medvedev, a reseatrcher in the Department of Computer Science and Engineering and the Department of Biochemistry and Molecular Biology at Penn State University.
“We had to develop specialized methods and computational analyses to account for the highly repetitive nature of the sequence of the Y. This project is truly cross-disciplinary and could not have happened without the combination of computational and biological scientists that we have on our team.”
“The Y chromosome contains a lot of repetitive sequences, which are challenging for DNA sequencing, assembling sequences, and aligning sequences for comparison,” said Monika Cechova, a graduate student in the Department of Biology at Penn State University.
“There aren’t out-of-the-box software packages to deal with the Y chromosome, so we had to overcome these hurdles and optimize our experimental and computational protocols, which allowed us to address interesting biological questions.”
The results were published in the Proceedings of the National Academy of Sciences.
Monika Cechova et al. Dynamic evolution of great ape Y chromosomes. PNAS, published online October 5, 2020; doi: 10.1073/pnas.2001749117