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

Abstract

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 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 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 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 to phylogenies for the major lepidopteran clades. We found that closely related herbivores fed on 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 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.

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

“…The strong phylogenetic signal for tyrosine overexpression differs from the patterns seen for Inga secondary metabolites (Endara et al, , ; Kursar et al, ). Previously we have argued that herbivores have selected for divergent defences, such that close relatives are not more similar in secondary metabolites (Coley et al, ).…”

“…In contrast, Noctuidae tend to avoid hosts that contain tyrosine, but are overrepresented on Inga with tyrosine‐ and tyramine‐gallates (Figure ). Our previous studies on Inga in Peru showed that the presence of tyrosine derivatives was among the most important factors for host selection by Noctuidae (Endara et al, ). In the present study, with a larger dataset, we show that this pattern extends to their entire regional distribution (Panama, Guiana Shield and Amazonia).…”

“…Unlike traits associated with resource acquisition (Endara et al, ; Sedio et al, ), secondary metabolites show no or only a weak phylogenetic signal across closely related species, implying that selection by herbivores favours rapid evolutionary divergence among relatives (Becerra, ; Fine, Metz, et al, ; Fine, Zapata, et al, ; Salazar et al, , , ; Sedio, ). In contrast, related herbivores feed on host species with similar secondary metabolites, suggesting that counter‐adaptations to plant defences are evolutionarily conserved (Endara et al, ; Janz, ). Thus, secondary metabolites appear to play an instrumental role in both the maintenance and origin of diversity for tropical plants and herbivores.…”

Promises and challenges in insect–plant interactions

“…Similarity in herbivore communities among plant species is often correlated with similarity in defences rather than with plant phylogeny, so host selection by herbivores appears to be more evolutionarily constrained (Endara et al, 2017). For example, studies show that plant anti-herbivore traits are more or less independent of phylogeny and, thus, are evolutionarily labile, with frequent shifts in defence strategies as plants colonize new habitats.…”

“…The regulation of the adaptive response of the plant must be finely balanced between defence and acquisition of benefits (Giron et al, 2013;Endara et al, 2017). However, plants have to interact with multiple biotic partners ranging from parasites to mutualists.…”