Coevolution as an engine of biodiversity and a cornucopia of ecosystem services

Abstract

Societal Impact StatementCoevolutionary processes, which have governed interactions between organisms throughout the history of life, also serve as an engine of ecosystem services for humans. The escalating arms races between plants and herbivores, flowers and pollinators, have generated a cornucopia of foods, raw materials, perfumes, spices, ornamentals, medicines, and drugs. Human history is replete with aesthetic as well as economic inspiration drawn from such plants. Our future may depend on similar inspiration, as we confront novel health, agricultural, and environmental challenges in the face of global change. Summary “Coevolution” was coined to conceptualize escalating arms races between plants and herbivores in evolutionary time, often mediated by natural products. Our current view embraces broader coevolutionary relationships between obligate mutualists, symbionts, parasites, and enemies, which frequently increase rates of diversification in coevolving lineages. Because humans benefit from the foods, materials, and drugs produced by plants in response to reciprocal selective pressures, coevolutionary “escape and radiate” diversification may amplify ecosystem services along with species richness, with humans as beneficiaries. For example, coevolutionary escalation of defenses between Burseraceae and their herbivores resulted in hundreds of resinous tree species, anchoring the trade of copal, frankincense, and myrrh across the ancient world. Examination of three diverse angiosperm orders (Asparagales, Malpighiales, and Gentianales), reveals ecosystem services in the form of alkaloids and hallucinogens, perfumes, spices, coffee, and rubber. Pollinator‐mediated selection by hawk moths and bats gave rise to heavily perfumed “moonflowers” (gardenias and jasmines) with aesthetic appeal to humans, and to immense blooming displays by agave plants, co‐opted by humans as a source of tequila and mezcal. Even when pollinator‐mediated diversification does not arise through coevolution, the resulting biotic richness provides evolutionary insights as well as ecosystem services. The convergent evolution of “kettle‐trap” flowers in species‐rich plant lineages (Aristolochia and Ceropegia) reveals the surprising value of small flies as pollinators and the opportunity to develop biocontrol that leverages floral features attractive to agricultural pests and disease vectors. This article highlights coevolution as a source of ecosystem services and potential solutions to the emerging challenges of global change.