The Y chromosome is a shy thing, no matter that it plays a critical role in sex determination and male fertility. For example, the Y chromosome has hidden valuable clues to its ancestry in hard-to-sequence DNA, which is to say, DNA that contains few genes but lots of repetitive regions. Also, because of its haploid nature, the Y chromosome is frequently absent from many species’ genome assemblies, even those of charismatic great apes.

To lift the veil of mystery over the Y chromosome, a team of biologists and computer scientists at Penn State constructed a dataset including Y chromosomes from all extant great ape genera. The scientists, led by biologist Kateryna D. Makova, PhD, and computer scientist Paul Medvedev, PhD, generated assemblies of bonobo and orangutan Y chromosomes from short and long sequencing reads and aligned them with the publicly available human, chimpanzee, and gorilla Y chromosome assemblies.

By comparing these assemblies, the scientists discerned patterns of evolution that seem to fit with behavioral differences between the species. The scientists also reconstructed a model of what the Y chromosome might have looked like in the ancestor of all great apes.

Details of this work appeared October 5 in the journal Proceedings of the National Academy of Sciences, in an article titled, “Dynamic evolution of great ape Y chromosomes.” The article argues that a clearer picture of the evolution of the Y chromosome could improve our understanding of male fertility in humans. The article also presents findings that could clarify reproduction patterns and male lineages in the great apes, potentially aiding conservation efforts for these endangered species.

“We found that the genus Pan, which includes chimpanzee and bonobo, experienced accelerated substitution rates,” the article’s authors wrote. “Pan also exhibited elevated gene death rates. These observations are consistent with high levels of sperm competition in Pan.

“Furthermore, we inferred that the great ape common ancestor already possessed multicopy sequences homologous to most human and chimpanzee palindromes. Nonetheless, each species also acquired distinct ampliconic sequences. We also detected increased chromatin contacts between and within palindromes (from Hi-C data), likely facilitating gene conversion and structural rearrangements.”

To arrive at these results, the Penn State team had to deal with difficulties posed by the Y chromosome. Besides containing repetitive DNA, short sequences that occur over and over again, the Y chromosome includes large DNA palindromes, inverted repeats that can be many thousands of letters long and read the same forwards and backwards.

“There aren’t out-of-the-box software packages to deal with the Y chromosome,” said Monika Cechova, a graduate student at Penn State at the time of the research and co-first author of the paper. “So, we had to overcome these hurdles and optimize our experimental and computational protocols, which allowed us to address interesting biological questions.”

Previous work by the team comparing human, chimpanzee, and gorilla sequences had revealed some unexpected patterns. Humans are more closely related to chimpanzees, but for some characteristics, the human Y was more similar to the gorilla Y.

“If you just compare the sequence identity—comparing the As,Ts, Cs, and Gs of the chromosomes—humans are more similar to chimpanzees, as you would expect,” said Makova. “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.”

The team, therefore, 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, the researchers 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.

Researchers have 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. The new research shows that many gene families and multicopy sequences were already present in the great ape Y common ancestor and that the chimpanzee and bonobo lineages experienced accelerated gene death and nucleotide substitution rates after their divergence from the human lineage. [Dani Zemba and Monika Cechova, Penn State]

“Our hypothesis is that the accelerated change that we see in chimpanzees and bonobos could be related to their mating habits,” said Rahulsimham Vegesna, a graduate student at Penn State and co-first author of the paper. “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,” said Vegesna. “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.”

The Y chromosome is also unusual because, unlike most chromosomes, it doesn’t have a matching partner. We each get two copies of chromosomes 1 through 22, and then some of us (females) get two X chromosomes and some of us (males) get one X and one Y. Partner chromosomes can exchange sections in a process called “recombination,” which is important to preserve the chromosomes evolutionarily. Because the Y doesn’t have a partner, it had been hypothesized that the long palindromic sequences on the Y might be able to recombine with themselves and thus still be able to preserve their genes, but the mechanism was not known.

“We used the data from a technique called Hi-C, which captures the three-dimensional organization of the chromosome, to try to see how this ‘self-recombination’ is facilitated,” said Cechova. “What we found was that regions of the chromosome that recombine with each other are kept in close proximity to one another spatially by the structure of the chromosome.”

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