More than one way to be an herbivore: convergent evolution of herbivory using different digestive strategies in prickleback fishes (Stichaeidae)

In fishes, the evolution of herbivory has occured within a spectrum of digestive strategies, with two extremes on opposite ends: (i) a rate-maximization strategy characterized by high intake, rapid throughput of food through the gut, and little reliance on microbial digestion or (ii) a yield-maximization strategy characterized by measured intake, slower transit of food through the gut, and more of a reliance on microbial digestion in the hindgut. One of these strategies tends to be favored within a given clade of fishes. Here, we tested the hypothesis that rate or yield digestive strategies can arise in convergently evolved herbivores within a given lineage. In the family Stichaeidae, convergent evolution of herbivory occured in Cebidichthys violaceus and Xiphister mucosus, and despite nearly identical diets, these two species have different digestive physiologies. We found that C. violaceus has more digesta in its distal intestine than other gut regions, has comparatively high concentrations (>11 mM) of short-chain fatty acids (SCFA, the endpoints of microbial fermentation) in its distal intestine, and a spike in β-glucosidase activity in this gut region, findings that, when coupled to long retention times (>20 h) of food in the guts of C. violaceus, suggest a yield-maximizing strategy in this species. X. mucosus showed none of these features and was more similar to its sister taxon, the omnivorous Xiphister atropurpureus, in terms of digestive enzyme activities, gut content partitioning, and concentrations of SCFA in their distal intestines. We also contrasted these herbivores and omnivores with other sympatric stichaeid fishes, Phytichthys chirus (omnivore) and Anoplarchus purpurescens (carnivore), each of which had digestive physiologies consistent with the consumption of animal material. This study shows that rate- and yield-maximizing strategies can evolve in closely related fishes and suggests that resource partitioning can play out on the level of digestive physiology in sympatric, closely related herbivores.