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A high-resolution map of small-scale inversions in the gibbon genome.

Gibbons are the most speciose family of living apes, characterized by a strikingly diverse chromosome number and rapid rate of large-scale rearrangements. Here we performed single-cell template strand sequencing (Strand-seq), molecular cytogenetics and deep in silico analysis of a southern white-cheeked gibbon genome providing the first comprehensive map of 238 previously hidden small-scale inversions. We determined that more than half are gibbon-specific, at least 5-fold higher than shown for other primate lineage specific inversions, with a significant high number of small heterozygous inversions, suggesting that accelerated evolution of inversions may have played a role in the high sympatric diversity of gibbons. Although the precise mechanisms underlying these inversions are not yet understood, it is clear that segmental duplication-mediated NAHR only accounts for a small fraction of events. Several genomic features including gene density and repeat (e.g. LINE1) content might render these regions more break-prone and susceptible to inversion formation. In the attempt to characterize interspecific variation between southern and northern white-cheeked gibbons, we identify several large assembly errors in the current GGSC Nleu3.0/nomLeu3 reference genome comprising over 49 megabases of DNA. Finally, we provide a list of 182 candidate genes potentially involved in gibbons diversification and speciation.