Community ecology and the evolution of molecules of keystone significance

Molecules of keystone significance are vital in structuring ecological communities. Select bioactive compounds can cause disproportionately large effects by connecting such seemingly disparate processes as microbial loop dynamics and apex predation. Here, we develop a general theory and propose mechanisms that could lead to the evolution of keystone molecules. Introduced into a respective community by one, or only a few, autotrophic or microbial species, these compounds often originate as chemical defenses. When co-opted by resistant consumer species, however, they are used either in chemical defense against higher-order predators or as chemosensory cues that elicit courtship and mating, alarm, and predatory search. Requisite to these multifunctional properties, biosynthetic capacity evolves along with mechanisms for resistance and/or toxin storage in primary producers. Subsequently, consumers acquire resistances or tolerances, and the toxins are transferred through food webs via trophic interactions. In consumers, mechanisms eventually evolve for recognizing toxins as feeding cues and, ultimately, as signals or pheromones in chemical communication within or between species. One, or a few, active compounds can thus mediate a vast array of physiological traits, expressed differentially across many species in a given community. Through convergent evolution, molecules of keystone significance provide critical information to phylogenetically diverse species, initiate major trophic cascades, and structure communities within terrestrial, freshwater, coastal-ocean and open-ocean habitats.