Convergent gene losses illuminate metabolic and physiological changes in herbivores and carnivores

Significance Mammals repeatedly adapted to specialized diets, including plant-based diets for herbivores and meat- or insect-based diets for carnivores. Apart from consuming diets with different nutritional compositions, obligate herbivores and carnivores differ in other aspects, such as the time spent feeding, regularity of pancreatic juice secretion, exposure to toxic plant-derived compounds, and gut microbiome diversity. To better understand how diet-related changes evolved, we performed genome-wide screens for convergent gene losses that happened preferentially in herbivores or in carnivores. We discovered repeated losses of genes involved in fat digestion, pancreatic juice secretion, glucose homeostasis, appetite regulation, detoxification, and gut microbiome diversity. Our results reveal genomic changes associated with dietary specialization and illuminate metabolic and physiological changes in herbivorous and carnivorous mammals.
The repeated evolution of dietary specialization represents a hallmark of mammalian ecology. To detect genomic changes that are associated with dietary adaptations, we performed a systematic screen for convergent gene losses associated with an obligate herbivorous or carnivorous diet in 31 placental mammals. For herbivores, our screen discovered the repeated loss of the triglyceride lipase inhibitor PNLIPRP1, suggesting enhanced triglyceride digestion efficiency. Furthermore, several herbivores lost the pancreatic exocytosis factor SYCN, providing an explanation for continuous pancreatic zymogen secretion in these species. For carnivores, we discovered the repeated loss of the hormone-receptor pair INSL5–RXFP4 that regulates appetite and glucose homeostasis, which likely relates to irregular feeding patterns and constant gluconeogenesis. Furthermore, reflecting the reduced need to metabolize plant-derived xenobiotics, several carnivores lost the xenobiotic receptors NR1I3 and NR1I2. Finally, the carnivore-associated loss of the gastrointestinal host defense gene NOX1 could be related to a reduced gut microbiome diversity. By revealing convergent gene losses associated with differences in dietary composition, feeding patterns, and gut microbiomes, our study contributes to understanding how similar dietary specializations evolved repeatedly in mammals.