Abstract
Coevolutionary theory has long predicted that the arms race between plants and herbivores is a major driver of host selection and diversification. At a local scale, plant defenses contribute significantly to the structure of herbivore assemblages and the high alpha diversity of plants in tropical rain forests. However, the general importance of plant defenses in host associations and divergence at regional scales remains unclear. Here, we examine the role of plant defensive traits and phylogeny in the evolution of host range and species divergence in leaf-feeding sawflies of the family Argidae associated with Neotropical trees in the genus Inga throughout the Amazon, the Guiana Shield and Panama. Our analyses show that the phylogenies of both the sawfly herbivores and their Inga hosts are congruent, and that sawflies radiated at approximately the same time, or more recently than their Inga hosts. Analyses controlling for phylogenetic effects show that the evolution of host use in the sawflies associated with Inga is better correlated with Inga chemistry than with Inga phylogeny, suggesting a pattern of delayed host tracking closely tied to host chemistry. Finally, phylogenetic analyses show that sister species of Inga-sawflies are dispersed across the Neotropics, suggesting a role for allopatric divergence and vicariance in Inga diversification. These results are consistent with the idea that host defensive traits play a key role not only in structuring the herbivore assemblages at a single site, but also in the processes shaping host association and species divergence at a regional scale.
Highlights
Insect herbivores and their plant hosts dominate terrestrial biodiversity (Hunt et al, 2007), and the processes that drive their interaction and diversification remain an enduring focus of research in ecology and evolution (Futuyma and Agrawal, 2009; Janz, 2011; Hembry et al, 2014; Forbes et al, 2017; Nakadai, 2017)
Ehrlich and Raven (1964) observed that closely related plants are often attacked by closely related herbivores, a pattern they attributed to an ‘escape and radiate’ model, in which plant lineages diversify following evolutionary innovation of a key defense trait, and specialist herbivore lineages diversify across the plant radiation through evolution of a key countermeasure (Wheat et al, 2007)
Our cytochrome oxidase I (COI) barcoding approach identified 41 MOTUs for sawflies feeding on Inga and Zygia host plants (Supplementary Figure S1), differing by 7–10 bp (1–1.5% divergence)
Summary
Insect herbivores and their plant hosts dominate terrestrial biodiversity (Hunt et al, 2007), and the processes that drive their interaction and diversification remain an enduring focus of research in ecology and evolution (Futuyma and Agrawal, 2009; Janz, 2011; Hembry et al, 2014; Forbes et al, 2017; Nakadai, 2017). Ehrlich and Raven (1964) observed that closely related plants are often attacked by closely related herbivores, a pattern they attributed to an ‘escape and radiate’ model, in which plant lineages diversify following evolutionary innovation of a key defense trait, and specialist herbivore lineages diversify across the plant radiation through evolution of a key countermeasure (Wheat et al, 2007) Where these traits are phylogenetically conserved in each lineage, we expect some degree of phylogenetic concordance between plant and herbivore lineages, resulting either from simultaneous co-diversification (Cruaud et al, 2012), or delayed herbivore colonization of an existing plant radiation (tracking of host resources; Janz, 2011). Robust analyses require phylogenetic histories of both plants and herbivores, and data on ecologically important traits such as plant defenses
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