Evolutionary and cellular mechanisms regulating intestinal performance of amphibians and reptiles

Abstract

Vertebrate intestinal tracts possess an array of structural and functional adaptations to the wide diversity of food and feeding habits. In addition to well-described differences in form and function between herbivores and carnivores, the intestine exhibits adaptive plasticity to variation in digestive demand. The capacity to which intestinal performance responds to changes in digestive demands is a product of evolutionary and cellular mechanisms. In this report, I have taken an integrative approach to exploring the mechanisms responsible for the regulation of intestinal performance with feeding and fasting among amphibians and reptiles. Intestinal performance is presented as the total small intestinal capacity to absorb nutrients, quantified as a product of small intestinal mass and mass-specific rates of nutrient uptake. For sit-and-wait foraging snakes and estivating anurans, both of which naturally experience long episodes of fasting, the dramatic downregulation of intestinal morphology and function with fasting reduces energy expenditure during extended fasts. In contrast, frequently-feeding species modestly regulate intestinal performance with fasting and feeding, trading higher basal rates of metabolism during fasting for the frequent expense of upregulating the gut with feeding. Surveying the magnitude by which intestinal uptake capacity is regulated among 26 families of amphibians and reptiles has revealed potentially five lineages that have independently evolved the capacity to widely regulate intestinal performance. The extent to which intestinal performance is downregulated with fasting among amphibians and reptiles, ranging from 0 to 90%, is largely a function of the degree by which mass-specific rates of nutrient transport are depressed, given that loss of intestinal mass with fasting is a common characteristic of vertebrates. In exploring the underlying mechanisms regulating intestinal nutrient uptake, use of the Burmese python has revealed a temporal match between microvillus surface area and intestinal nutrient transport. With feeding, pythons experience a five-fold lengthening of intestinal microvilli, with subsequent reduction after completing digestion. Identifying for the python the cellular processes responsible for the dramatic remodeling of the microvilli would assist in elucidating the mechanisms by which intestinal performance is regulated, as well as identify whether similar steps are employed by other species to regulate their intestines. In finishing, I propose three studies of digestive response: (1) investigate the responses of the ectotherm intestine to hibernation; (2) evaluate whether functional capacities of tissues are matched to digestive demands; and, (3) apply microarray technology to explore the functional genomics of intestinal adaptation.