Abstract

BackgroundThere 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.ResultsWe 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.ConclusionsOur 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-1071-4) contains supplementary material, which is available to authorized users.

Highlights

  • There are three main dietary groups in mammals: carnivores, omnivores, and herbivores

  • Leopard genome sequencing and assembly We built the reference leopard genome from a muscle sample obtained from a female Amur leopard from the Daejeon O-World of Korea (Additional file 1: Supplemental Methods for details of species identification using mitochondrial DNA gene analysis; Additional file 2: Figure S1)

  • We have investigated genetic diversity in Felidae and compared it to different dietary requirement groups, Fig. 3 Highly conserved region (HCR) in Felidae, Hominidae, and Bovidae

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Summary

Introduction

There are three main dietary groups in mammals: carnivores, omnivores, and herbivores. Several key diet-related physiological traits have been identified, including differences in digestive enzymes [7], shortened digestive tracts [8], changes in amino acid dietary requirements [9, 10], and alterations to taste bud sensitivities (including a heightened response to amino acids and a loss of response to many mono- and disaccharides) [11, 12], to name a few In addition to these characteristics, the morphology of cats is highly adapted to hunting and includes flexible bodies, fast reflexes, and strong muscular limbs. A high-quality domestic cat reference and a cheetah (Acinonyx jubatus) genome assembly have been added [17,18,19], making this group an ideal initial target for identifying molecular adaptations to extreme carnivory that can provide insight on human healthcare

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