Genetic and phenotypic adaptation of intestinal nutrient transport to diet in fish

Abstract

1. Herbivores have higher rates of intestinal sugar transport and lower rates of amino acid transport than carnivores, if each are studied while eating their respective natural diets. It was unclear whether these species differences involve a genetic contribution, since when omnivores are switched from a high-protein to a high-carbohydrate diet they reversibly increase sugar transport and suppress amino acid transport. Hence we studied eight fish species of differing natural diets while all were eating the same manufactured diet. 2. Na+-dependent L-proline uptake and active D-glucose uptake, measured in vitro by the everted intestinal sleeve technique, followed Michaelis-Menten kinetics. Values of the apparent Michaelis-Menten constant increased with values of the maximal transport rate, probably as a result of unstirred layer effects. 3. The ratio of proline to glucose uptake decreased in the sequence: carnivores greater than omnivores greater than herbivores. The intestine's uptake capacity for the non-essential nutrient glucose was much higher in herbivores than in carnivores, correlated with species differences in carbohydrate content of the natural diet. Proline uptake varied much less among species, since species with different natural diets still have similar protein requirements. 4. Since all species were studied while eating the same diet, these species differences in uptake are not phenotypic but genetic adaptations to the different natural diets. 5. In two fish species which normally switch from carnivory towards herbivory or omnivory as they mature, we observe a 'hard-wired' developmental change in intestinal uptake. Larger animals had lower proline uptake relative to glucose uptake than did smaller animals, even though both were being maintained on the same diet in the laboratory. 6. Carnivorous fish tend to allocate absorptive tissue to pyloric caeca or a thick mucosa, while herbivorous fish tend towards a long thin intestine.