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.
Highlights
One of the most intriguing features of plants is their production of complex mixtures of secondary metabolites; hundreds or even thousands can sometimes be detected in a single tissue sample (Wiggins et al 2016, Sedio et al 2018)
This hypothesis posits that most secondary metabolites are inactive, but selection acts on biochemical mechanisms that increase diversity because plants that make and ‘screen’ a large number of metabolites will benefit from the rare metabolites that have potent biological activity
Integrating frugivory and chemical ecology: a roadmap To better understand the extent to which fruit–frugivore interactions have shaped phytochemical diversification, we suggest three broad approaches: 1) comparative chemistry across plant organs that includes fruits; 2) ecological studies that address how intraspecific variation in fruit phytochemical composition and diversity affect fruit–frugivore interactions and plant fitness, and; 3) macroevolutionary studies that examine whether patterns of phytochemical composition and diversity at the whole-plant level reflect a signature of selection from fruit– frugivore interactions
Summary
One of the most intriguing features of plants is their production of complex mixtures of secondary metabolites; hundreds or even thousands can sometimes be detected in a single tissue sample (Wiggins et al 2016, Sedio et al 2018). Most of the structures and functions of these metabolites are undescribed, but there are numerous well-studied examples in which secondary metabolites play a key role in shaping plant interactions, and, the evolution of both plants and consumers (Hartmann 2007, Futuyma and Agrawal 2009). Perhaps the most well-supported is the interaction diversity hypothesis, which suggests that chemical diversity is an emergent consequence of diverse selective pressures from the many different antagonists and mutualists with whom the plant interacts (Whitehead et al 2021). In particular, are highly nutritious resources and face complex and highly variable selection pressures from different consumers over time As they develop on the parent plant, they must defend against complex communities of antagonistic herbivores, seed predators, and pathogens (Andersen 1988, Kolb et al 2007, Tiansawat et al 2017). An exception is the screening hypothesis, which provides a null alternative to that assumption
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