Comparison of carnivore, omnivore, and herbivore mammalian genomes with a new leopard assembly

Soonok Kim, Yun Sung Cho, Hak-Min Kim, Oksung Chung, Hyunho Kim, Sungwoong Jho, Hong Seomun, Jeongho Kim, Woo Young Bang, Changmu Kim, Junghwa An, Chang Hwan Bae, Youngjune Bhak, Sungwon Jeon, Hyejun Yoon, Yumi Kim, JeHoon Jun, HyeJin Lee, Suan Cho, Olga Uphyrkina, Aleksey Kostyria, John Goodrich, Dale Miquelle, Melody Roelke, John Lewis, Andrey Yurchenko, Anton Bankevich, Juok Cho, Semin Lee, Jeremy S. Edwards, Jessica A. Weber, Jo Cook, Sangsoo Kim, Hang Lee, Andrea Manica, Ilbeum Lee, Stephen J. O’Brien, Jong Bhak, Joo-Hong Yeo

There are three main dietary groups in mammals: carnivores, omnivores, and herbivores. Currently, there is limited comparative genomics insight into the evolution of dietary specializations in mammals. Due to recent advances in sequencing technologies, we were able to perform in-depth whole genome analyses of representatives of these three dietary groups. We investigated the evolution of carnivory by comparing 18 representative genomes from across Mammalia with carnivorous, omnivorous, and herbivorous dietary specializations, focusing on Felidae (domestic cat, tiger, lion, cheetah, and leopard), Hominidae, and Bovidae genomes. We generated a new high-quality leopard genome assembly, as well as two wild Amur leopard whole genomes. In addition to a clear contraction in gene families for starch and sucrose metabolism, the carnivore genomes showed evidence of shared evolutionary adaptations in genes associated with diet, muscle strength, agility, and other traits responsible for successful hunting and meat consumption. Additionally, an analysis of highly conserved regions at the family level revealed molecular signatures of dietary adaptation in each of Felidae, Hominidae, and Bovidae. However, unlike carnivores, omnivores and herbivores showed fewer shared adaptive signatures, indicating that carnivores are under strong selective pressure related to diet. Finally, felids showed recent reductions in genetic diversity associated with decreased population sizes, which may be due to the inflexible nature of their strict diet, highlighting their vulnerability and critical conservation status. Our study provides a large-scale family level comparative genomic analysis to address genomic changes associated with dietary specialization. Our genomic analyses also provide useful resources for diet-related genetic and health research.