Niche construction and the transition to herbivory: Phenotype switching and the organization of new nutritional modes

Abstract

Gut microbiota have played important roles in the evolutionary transition from carnivory to herbivory. In the evolution of ruminants, three modes of macrobe-microbe symbiosis have facilitated the phenotypic switch into a new nutritional mode. Mutualistic microbes acquired during birth enable the building of the rumen (developmental symbiosis), the digestion of plant fiber (nutritional symbiosis), and the detoxification of plant toxins (protective symbiosis). These symbioses created a new plant dietary niche through two types of niche construction: “perturbational niche construction,” a phenotypic process whereby gut microbes initiate the building of a mature rumen from the nonfunctional anlagen of this stomach region; and “mediational niche construction,” whereby microbe-induced changes alter how the animal experiences environmental resources without actual modification of the environment. Thanks to microbes, plants are now edible. We argue that the reciprocal niche construction of the host and its associated microbial organisms (i.e., the “holobiont”) scaffold each other’s developmental and phenotypic processes as well as organize a new selective environment of the holobiont as a whole.