Diet evolution of carnivorous and herbivorous mammals in Laurasiatheria

Abstract

Background: Laurasiatheria contains taxa with diverse diets, while the molecular basis and evolutionary history underlying their dietary diversification are less clear.

Results: In this study, we used the recently developed molecular phyloecological approach to examine the adaptive evolution of digestive system-related genes across both carnivorous and herbivorous mammals within Laurasiatheria. Our results show an intensified selection of fat and/or protein utilization across all examined carnivorous lineages, which is consistent with their high-protein and high-fat diets. Intriguingly, for herbivorous lineages (ungulates), which have a high-carbohydrate diet, they show a similar selection pattern as that of carnivorous lineages. Our results suggest that for the ungulates, which have a specialized digestive system, the selection intensity of their digestive system-related genes does not necessarily reflect loads of the nutrient components in their diets but appears to be positively related to the loads of the nutrient components that are capable of being directly utilized by the herbivores themselves. Based on these findings, we reconstructed the dietary evolution within Laurasiatheria, and our results reveal the dominant carnivory during the early diversification of Laurasiatheria. In particular, our results suggest that the ancestral bats and the common ancestor of ruminants and cetaceans may be carnivorous as well. We also found evidence of the convergent evolution of one fat utilization-related gene, APOB, across carnivorous taxa.

Conclusions: Our molecular phyloecological results suggest that digestive system-related genes can be used to determine the molecular basis of diet differentiations and to reconstruct ancestral diets.

Keywords: Carnivores; Dietary evolution; Digestive system genes; Herbivores; Positive selection.

Fig. 1

Laurasiatheria phylogeny and reconstructed ancestral dietary categories based on molecular data. The phylogenetic relationships among species follow published studies [–96]. The branches under positive selection analyses are shown with letters (A–L). The dietary categories of each extant species and each mammalian order shown in the pet charts are based on one previous study [93]. Carnivores are shown in red, herbivores in green, and omnivores in violet. Black shows the species with no dietary categories available

Fig. 2

Digestive system pathways and positively selected genes found in ruminants (green) and cetaceans (red). Three digestive system pathways (A, B, and C) were modified from that of KEGG, including carbohydrate digestion and absorption (map04973), protein digestion and absorption (map04974), and fat digestion and absorption (map04975). Positively selected genes are shown in parentheses, and their corresponding proteins are highlighted in red (cetaceans) and green (ruminants)

Fig. 3

Maximum-likelihood phylogeny of the gene APOB. The phylogeny is based on 4550 amino-acid sites with the best-fit substitution model of the HIVb+F+R4 used. Red shows the clustering of four carnivory-dominant taxa