Microbial determinants of folivory in insects

Aileen Berasategui and Hassan Salem


A centerpiece to ecosystem productivity, land plants are key drivers of energy conversion and carbon fixation (Zelitch 1975; Kroth 2015). As the primary photosynthetic organs of plants, the bulk of Earth's carbon reservoirs are fixed and stored by leaves (Vogelman, Nishio, and Smith 1996). Abundant in energy-rich sugars, and endowed with a steady supply of essential nutrients, peptides, lipids, and cofactors, leaves share many features of a nutritionally balanced diet. Obligate folivory, however, evolved a limited number of times throughout the metazoan tree of life (McNab 1988; Chivers 1989; Rand et al. 1990; Currano, Labandeira, and Wilf 2010).

Despite the extensive radiation of land plants across every major continent and the ubiquity of foliage as a seemingly accessible resource, most animals lack the metabolic and physiological adaptations necessary to subsist on leaves as a sole source of nutrition. First, and most prominently, animals largely lack the enzymatic circuitry necessary to maximize the dietary value of ingested foliage. The highly recalcitrant polysaccharides that define the fibrous features of leaves can only be hydrolyzed by a specific range of enzymes that are ancestrally encoded by plants and their specialized pathogens (Walton 1994; Kubicek, Starr, and Glass 2014). Towards accessing the nutritionally rich cytosol, folivores must first contend with the main structural polysaccharide components of the plant cell wall, despite generally lacking an endogenous repertoire of essential digestive enzymes. Second, leaves are typically enriched with a range of constitutive and induced plant secondary metabolites evolved to mitigate the incidence and impact of herbivory (Levin 1976; Stotz et al. 2000; Wittstock and Gershenzon 2002). Ranging from terpenoids to alkaloids, these defensive compounds disrupt the integrity of the digestive epithelial lining of animals and compromise the functionality of neuronal networks when ingested. Finally, foliage can be transient, as with deciduous trees and shrubs spanning Earth’s temperate and polar regions (Jackson 1967). The total abscission of leaves poses as a considerable hurdle for folivores during the winter season (Giron et al. 2007), necessitating the evolution of strategies to survive in the absence of a specialized diet for months on end. Towards mitigating these challenges, strikingly convergent adaptations arose in independent folivorous lineages, many of which are mediated through symbioses with metabolically dynamic microbial communities.

With the advent of sequencing technologies and metabolic modeling, coupled with the development of conceptual frameworks to study the functionality of the metaorganism (McFall-Ngai et al. 2013), microbes are increasingly recognized as an essential source of adaptations for animals (Douglas 2015; Chomicki et al. 2019). By contributing complementary metabolic profiles, symbioses can upgrade the phenotypic complexity of both partners (Moran 2007), spurring their radiation into novel ecological niches and triggering their diversification. Microbial symbionts are especially recognized for fueling their hosts’ specializations on nutritionally challenging diets (Douglas 2015). Sap-feeding invertebrates are consistently demonstrated to partner with symbionts that supplement the essential amino acids lacking in their diet (Hansen and Moran 2014; Baumann 2005). Haematophagous animals contend with the B-vitamin deficiency of their bloodmeals through nutritional partnerships with endosymbionts contributing these cofactors (Akman et al. 2002; Rio, Attardo, and Weiss 2016; Duron et al. 2018). Wood feeding is made possible through the digestive range of their lignocellulolytic symbionts across a number of metazoan taxa (Brune 2014; Brune and Dietrich 2015). Here, we argue that leaves constitute an equally specialized diet, necessitating innovations that extend well beyond the metabolic range of most animals. In outlining the convergent metabolic features of folivore microbiomes, we point towards the outsized role microbes play towards upgrading the dietary value of ingested leaves. Given the compositionally simple, experimentally tractable partnerships folivorous insects form with their microbial partners, we emphasize the unique suitability of these study systems to pursue hypothesis-driven research into the adaptive impact of symbiosis in its intersection with the evolution of leaf-feeding behavior (Figure 13.1).

< Prev   CONTENTS   Source   Next >