A high-quality bonobo genome refines the analysis of hominid evolution

Abstract

The divergence of chimpanzee and bonobo provides one of the few examples of recent hominid speciation1,2. Here we describe a fully annotated, high-quality bonobo genome assembly, which was constructed without guidance from reference genomes by applying a multiplatform genomics approach. We generate a bonobo genome assembly in which more than 98% of genes are completely annotated and 99% of the gaps are closed, including the resolution of about half of the segmental duplications and almost all of the full-length mobile elements. We compare the bonobo genome to those of other great apes1,3–5 and identify more than 5,569 fixed structural variants that specifically distinguish the bonobo and chimpanzee lineages. We focus on genes that have been lost, changed in structure or expanded in the last few million years of bonobo evolution. We produce a high-resolution map of incomplete lineage sorting and estimate that around 5.1% of the human genome is genetically closer to chimpanzee or bonobo and that more than 36.5% of the genome shows incomplete lineage sorting if we consider a deeper phylogeny including gorilla and orangutan. We also show that 26% of the segments of incomplete lineage sorting between human and chimpanzee or human and bonobo are non-randomly distributed and that genes within these clustered segments show significant excess of amino acid replacement compared to the rest of the genome.

Evolution of host-microbe cell adherence by receptor domain shuffling

“…Reads were not available for the genome assembly from which bonobo CEACAM sequences were identified for the evolutionary analyses described here. However, a more recent assembly of a different bonobo individual became available during the course of this study and sequencing reads for this new de novo assembly were deposited ( Mao et al, 2021 ). The CEACAM1 genomic region of the newer assembly was 99% identical to the older version while the coding sequences differ at only a single nucleotide outside of the N-domain.…”

Current Progress in Evolutionary Comparative Genomics of Great Apes

“… Kronenberg et al (2018) generated the genome assemblies of human, chimpanzee, and orangutan using SMRT long-read sequencing with over 65-fold coverage. Mao et al (2021) reported a new high-quality bonobo genome assembly using the long-read PacBio platform with 74-fold sequence coverage. The details of recently assembled genomes of great apes can be found in Table 1 .…”

“…They also found that the small past Ne correlates with a larger number of deleterious alleles and the genes enriched with bonobo-specific non-synonymous changes are related to age at menarche in humans. Based on a new bonobo genome assembly, Mao et al (2021) identified some novel genes and found that most of the novel genes showed selective sweeps in bonobo, such as DIRC1 , GULP1 , and ERC2 .…”

“…Deletion SVs showed overrepresentation in “sensory perception of smell” and “G-protein coupled receptor signaling pathway.” Furthermore, some of the genes impacted by SVs appeared likely targets of natural selection, which is suggestive of the significance of SVs in impacting the chimpanzee adaptation during the course of evolution. Comparing the bonobo genome to the other great apes’ genomes, Mao et al (2021) identified 22,868 bonobo-specific SVs with size >50 bp (including 7,082 deletions and 15,786 insertions), among which there are 1,965 fixed deletions and 3,604 fixed insertions.…”

Evolution of host-microbe cell adherence by receptor domain shuffling

“…Bonobo genomic DNA was not available for direct sequencing of CEACAM1, so currently available bonobo genome sequence data was used for sequence verification. While the genome assembly from which bonobo CEACAM sequences were identified for evolutionary analyses did not have reads available, a more recent assembly of a different bonobo individual became available during the course of this study which did deposit sequencing reads along with a de novo genome assembly (Mao et al, 2021). The CEACAM1 1 genomic region of the newer assembly was 99% identical to the older version while the coding sequences differ at only a single nucleotide outside of the N-domain.…”