Fruits, frugivores, and the evolution of phytochemical diversity

Abstract

Plants produce an enormous diversity of secondary metabolites, but the evolutionary mechanisms that maintain this diversity are still unclear. The interaction diversity hypothesis suggests that complex chemical phenotypes are maintained because different metabolites benefit plants in different pairwise interactions with a diversity of other organisms. In this synthesis, we extend the interaction diversity hypothesis to consider that fruits, as potential hotspots of interactions with both antagonists and mutualists, are likely important incubators of phytochemical diversity. We provide a case study focused on the Neotropical shrub Piper reticulatum that demonstrates: 1) secondary metabolites in fruits have complex and cascading effects for shaping the outcome of both mutualistic and antagonistic fruit-frugivore interactions, and; 2) fruits can harbor substantially higher levels of phytochemical diversity than leaves, even though leaves have been the primary focus of plant chemical ecology research for decades. We then suggest a number of research priorities for integrating chemical ecology with fruit-frugivore interaction research and make specific, testable predictions for patterns that should emerge if fruit interaction diversity has helped shape phytochemical diversity. Testing these predictions in a range of systems will provide new insight into the mechanisms driving frugivory and seed dispersal and shape an improved, whole-plant perspective on plant chemical trait evolution.

Comparative Metabolomics of Fruits and Leaves in a Hyperdiverse Lineage Suggests Fruits Are a Key Incubator of Phytochemical Diversification

“…These complex and contrasting selective pressures are distinct from those acting on leaves, and may lead to the occurrence of secondary metabolites not found in other organs. Indeed, given the complex and often contrasting nature of selective pressures to which fruits and seeds are exposed, fruits and seeds may serve as evolutionary incubators of novel secondary metabolites, and disproportionately contribute to the diversity of phytochemical traits (Whitehead et al, 2021). This is especially likely in systems involving animal-mediated seed dispersal (zoochory), in which plants face the ecological and physiological challenge of attracting and offering a nutritional reward to dispersal vectors while also repelling seed predators, pathogens, and non-target frugivores (Herrera, 1982;Tewksbury, 2002;Whitehead et al, 2016).…”

“…Our overall objective in this study is to test the hypothesis that fruits can act as incubators of phytochemical diversification in plants (Whitehead et al, 2021). First, we describe the occurrence patterns of secondary metabolites across leaves, fruit pulp, and seeds in 12 Piper species, providing baseline data for understanding Piper secondary metabolite function.…”

Quantifying chemodiversity considering biochemical and structural properties of compounds with the R packagechemodiv

“…Plants produce an astonishing diversity of phytochemical compounds (Kessler & Kalske, 2018; Wang et al ., 2019). With functions such as chemical defence, attractant or repellent signalling and protection against abiotic stressors, phytochemicals (also referred to as secondary metabolites) are crucial for mediating mutualistic and antagonistic interactions between plants and other organisms and the abiotic environment (Hartmann, 2007; Junker & Tholl, 2013; Kessler & Kalske, 2018; Whitehead et al ., 2021b). Understanding the evolutionary processes generating this phytochemical diversity, and the ecological functions of it are central goals in the field of chemical ecology (Fraenkel, 1959; Ehrlich & Raven, 1964; Hartmann, 2007; Raguso et al ., 2015).…”

Compartmentalization of specialized metabolites across vegetative and reproductive tissues in two sympatricPsychotria(Rubiaceae)

“…However, the development of the Interaction Diversity Hypothesis (IDH) with respect to ecologically disparate plant organs (e.g. animal-dispersed fruit vs. leaves; Whitehead et al, 2021) has established the efficacy of a plant-level perspective on specialized metabolite trait evolution, one which integrates organ-level patterns and processes. In brief, the IDH posits that the diversity of specialized metabolites in a given plant species is an emergent consequence of the diversity of biotic interactions amid which the species has evolved (Berenbaum and Zangerl, 1996; Iason et al, 2011; Whitehead et al, 2021).…”

“…animal-dispersed fruit vs. leaves; Whitehead et al, 2021) has established the efficacy of a plant-level perspective on specialized metabolite trait evolution, one which integrates organ-level patterns and processes. In brief, the IDH posits that the diversity of specialized metabolites in a given plant species is an emergent consequence of the diversity of biotic interactions amid which the species has evolved (Berenbaum and Zangerl, 1996; Iason et al, 2011; Whitehead et al, 2021). In such a scenario, the distinct selective pressures of each antagonistic or mutualistic interaction act independently from one another on the chemical deterrents and/or attractants in the pertinent plant tissue.…”