Comparative transcriptomics shows the evolutionary origin of acoustic fat bodies through a trade-off with skull muscles in toothed whales

Toothed whales (odontocetes) have developed acoustic fat bodies, which include forehead melon, extra-mandibular fat body and intra-mandibular fat body. These contribute to the sound transmission pathways in the unique echolocation process of toothed whales. The acoustic fat bodies of Odontocetes accumulate unusual fatty acids, making them novel traits with unique functional anatomy and chemistry. This study provides new insights into the evolutionary origin and lipid utilisation of acoustic fat bodies in harbour porpoise (Phocoena phocoena) and Pacific white-sided dolphin (Lagenorhynchus obliquidens) using comparative transcriptomics. Comprehensive gene expression analyses indicated that the acoustic fat bodies of toothed whales are composites of muscle and adipose tissues, mainly composed of intramuscular fat. The extra-mandibular fat body is a homologue of the masseter muscle. Additionally, we demonstrated that gene expression-based functional enrichments for specialised branched-chain amino acid metabolism, endocytosis, lysosomes and peroxisomes contribute to the maintenance of the unique fatty characteristics of the acoustic fat bodies of toothed whales. A trade-off occurred in the evolution of acoustic fat bodies as a result of the fatty reorganisation of head muscles involved in aquatic adaptation in toothed whales.