Macroevolutionary patterns in overexpression of tyrosine:An anti‐herbivore defence in a speciose tropical tree genus, Inga (Fabaceae)

This is the author accepted manuscript. The final version is available from Wiley via the DOI in this record.1.Plant secondary metabolites are a key defence against herbivores, and their evolutionary origin is likely from primary metabolites. Yet for this to occur, an intermediate step of overexpression of primary metabolites would need to confer some advantage to the plant. Here, we examine the evolution of overexpression of the essential amino acid, L‐tyrosine and its role as a defence against herbivores. 2.We examined overexpression of tyrosine in 97 species of Inga (Fabaceae), a genus of tropical trees, at five sites throughout the Neotropics. We predicted that tyrosine could act as an anti‐herbivore defence because concentrations of 4% tyrosine in artificial diets halved larval growth rates. We also collected insect herbivores to determine if tyrosine and its derivatives influenced host associations. 3.Overexpression of tyrosine was only present in a single lineage comprising 21 species, with concentrations ranging from 5% to 20% of the leaf dry weight. Overexpression was pronounced in expanding but not in mature leaves. Despite laboratory studies showing toxicity of L‐tyrosine, Inga species with tyrosine suffered higher levels of herbivory. We therefore hypothesize that overexpression is only favoured in species with less effective secondary metabolites. Some tyrosine‐producing species also contained secondary metabolites that are derived from tyrosine: tyrosine‐gallates, tyramine‐gallates and DOPA‐gallates. Elevated levels of transcripts of prephenate dehydrogenase, an enzyme in the tyrosine biosynthetic pathway that is insensitive to negative feedback from tyrosine, were found only in species that overexpress tyrosine or related gallates. Different lineages of herbivores showed contrasting responses to the overexpression of tyrosine and its derived secondary metabolites in their host plants. 4.Synthesis. We propose that overexpression of some primary metabolites can serve as a chemical defence against herbivores, and are most likely to be selected for in species suffering high herbivory due to less effective secondary metabolites. Overexpression may be the first evolutionary step in the transition to the production of more derived secondary metabolites. Presumably, derived compounds would be more effective and less costly than free tyrosine as anti‐herbivore defences.National Science Foundatio

Coevolutionary arms race versus host defense chase in a tropical herbivore-plant system

This is the author accepted manuscript. The final version is available from National Academy of Sciences via the DOI in this record.Coevolutionary models suggest that herbivores drive diversification and community composition in plants. For herbivores, many questions remain regarding how plant defenses shape host choice and community structure. We addressed these questions using the tree genus Inga and its lepidopteran herbivores in the Amazon. We constructed phylogenies for both plants and insects and quantified host associations and plant defenses. We found that similarity in herbivore assemblages between Inga species was correlated with similarity in defenses. There was no correlation with phylogeny, a result consistent with our observations that the expression of defenses in Inga is independent of phylogeny. Furthermore, host defensive traits explained 40% of herbivore community similarity. Analyses at finer taxonomic scales showed that different lepidopteran clades select hosts based on different defenses, suggesting taxon-specific histories of herbivore–host plant interactions. Finally, we compared the phylogeny and defenses of Inga to phylogenies for the major lepidopteran clades. We found that closely related herbivores fed on Inga with similar defenses rather than on closely related plants. Together, these results suggest that plant defenses might be more evolutionarily labile than the herbivore traits related to host association. Hence, there is an apparent asymmetry in the evolutionary interactions between Inga and its herbivores. Although plants may evolve under selection by herbivores, we hypothesize that herbivores may not show coevolutionary adaptations, but instead “chase” hosts based on the herbivore’s own traits at the time that they encounter a new host, a pattern more consistent with resource tracking than with the arms race model of coevolution.We thank the Ministry of Agriculture of Peru for granting the research and exportation permits. We gratefully acknowledge Los Amigos Biological Station for institutional and logistical support. Invaluable field assistance was provided by Wilder Hidalgo and Silvana Lozano. We thank Axel Haussman, Suzy Khachaturyan, and Eric Murakami for help in the barcode identification of the insect herbivores. Kyle Harms suggested the short title for the manuscript. This work was supported by the Secretaría Nacional de Educación Superior, Ciencia, Tecnología e Innovación del Ecuador (SENESCYT) and grants from Conservation, Research and Education Opportunities and from the University of Utah: The Global Change and Sustainability Center and the International Student Center from the University of Utah (to M.-J.E.) and National Science Foundation Grants DEB-0640630 and Dimensions of Biodiversity DEB-1135733 (to P.D.C. and T.A.K.

Annotation of Inga transcriptomes

Trinnotate annotation for transcriptomes assembled from RNASeq of wild collected expanding leave

Assembled transcriptomes

Trinity assemblies of Inga transcriptome

Salmon counts with I_sapindoides as reference

Salmon counts for each transcriptome. Generated using I. sapindoides BCI-97 as the reference transcriptom