Sugar assimilation underlying dietary evolution of Neotropical bats

Abstract

SummarySpecializations in animal diets drive selective demands on morphology, anatomy, and physiology. Studying adaptations linked to diet evolution benefits from examining Neotropical bats, a remarkable group with high taxonomic and trophic diversity. In this study we performed glucose tolerance tests on wild-caught bats, which revealed distinct responses to three sugars present in different foods: trehalose (insects), sucrose and glucose (fruits and nectar). Insect eating bats responded most strongly to trehalose, while bats with nectar and fruit-based diets exhibited heightened response to glucose and sucrose, reaching blood sugar levels over 600 mg/dL. To reveal positive selection in sugar assimilation genes we performed genome analysis of 22 focal bat species and 2 outgroup species. We identified selection in the ancestral vespertilionid branch (insect-eaters) for the digestive enzyme Trehalase, while sucrase-isomaltase exhibited selection in branches leading to omnivorous and nectar diets. Unexpectedly, the insect-eating lineageMyotisexhibited sucrase-isomaltase selection, potentially explaining their heightened sucrose assimilation. Furthermore, the glucose transporters SLC2A3 and SLC2A2 showed selection in lineages associated with nectar and blood diets. By examining cellular features of the small intestine, we discovered that sugar consumption strongly impacted numerous digestive traits, providing valuable insight into the physiological implications of the identified molecular adaptations. To elucidate this further, we used HCR RNA-FISH to perform single moleculeex vivogene expression analysis of enterocyte response to a glucose meal in three focal species. We observed unusually high activity in the glucose transporterSlc2a2during the fasted state of nectar bats that did not change upon feeding. Comparatively, nectar bats exhibited an enhanced capacity for intestinal absorption of dietary sugar primarily throughSlc2a2, while fruit bats relied on increasing levels ofSlc5a1. Overall, this study highlights the intricate interplay between molecular, morphological, and physiological aspects of diet evolution and provides new insights to our understanding of sugar assimilation mechanisms in mammals.HighlightsSugar assimilation differences emphasize metabolic adaptations to dietGlucose tolerance tests provide a quick and practical assessment of dietary ecologyBat genomes exhibit positive selection on digestive enzymes and glucose transportersGlucose absorption differences can be explained by gut anatomyExtreme blood glucose (>650 mg/dL) coincides with constitutive expression of apicalSlc2a2The regulation ofSglt1and apicalSlc2a2highlights differences in blood glucose levelsGraphical Abstract