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Genomic and Phenotypic Evolution of Bonobos, Chimpanzees and Humans

Final Report Summary - TWOPAN (Genomic and Phenotypic Evolution of Bonobos, Chimpanzees and Humans)

Two African apes are the closest living relatives of humans: the chimpanzee and the bonobo. While chimpanzees are widespread across equatorial Africa, bonobos live only south of the Congo River in the Democratic Republic of Congo. Bonobos and chimpanzees are highly similar to each other in many respects. However, the behavior of the two species differs in important ways. For example, male chimpanzees use aggression to compete for dominance and sex, and to attack other groups. By contrast, bonobo males are commonly subordinate to females and there is no evidence for lethal aggression among bonobos who are playful throughout life and show intense sexual behavior that often involves same-sex partners. Thus, chimpanzees and bonobos each possess certain characteristics that are more similar to human traits than they are to one another. In order to better understand the evolutionary relationships of bonobos, chimpanzees and humans, we sequenced the genome from Ulindi, a female bonobo who lives in the Leipzig Zoo, and compared it to those of chimpanzees and humans. We find that 2.1% of the human genome are more closely related to either the bonobo or the chimpanzee genome than these are to each other while 2.3% of the human genome is more closely related to the chimpanzee than the bonobo genome. As a consequence, about 40% of all genes contain parts that show such “mixed relationships”. By sequencing several chimpanzees we used the bonobo genome to identify genomic regions that have positively selected in chimpanzees, several of which are involved in the immune system.
We also find that whereas chimpanzees retain genomic variation that predates bonobo-chimpanzee speciation, much of the bonobo genome traces its ancestry back to a single common ancestor that postdates their origin as a group separate from chimpanzees, suggesting that from a genomic perspective the chimpanzees are more similar to the common ancestor of the African apes than bonobos.
We have studied the behavioral and cognitive differences between the bonobos and chimpanzees, finding among other things that bonobos are more skilled at solving tasks related to social relationships, while chimpanzees were more skilled at tasks requiring the use of tools and an understanding of physical causality. To ask if the differences in social system in the two apes have affected the evolution of their genome, we sequenced the protein-coding genes of 20 chimpanzees and 20 bonobos. We find that the X chromosomes of bonobos carry a higher proportion of putatively deleterious alleles relative to the other chromosomes than chimpanzees or humans. By simulations we show that the explanation for this is likely that competition among males for mates is much less pronounced in bonobos than in chimpanzee and that mothers influence their son’s reproductive success in bonobos.
We have studied gene activity in six different tissues of apes and humans and find the evolutionary changes in gene activity have been most pronounced in the male germ line and the least pronounced in the brain. However, many genes related to the insulation of neurons from each other have changed in the ancestors of humans, perhaps playing a role in the fine-tuning of connectivity in the human brain.
We have analyzed health-related substances in the blood of 257 wild and captive-born apes and over 300 humans. This is the largest set of clinical data available from apes and will help in monitoring the health status of apes in sanctuaries as well as in the management of wild populations.