Tracking of Host Defenses and Phylogeny During the Radiation of Neotropical Inga-Feeding Sawflies (Hymenoptera; Argidae)

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.

Keywords: Inga; coevolution; defense traits; herbivores; host tracking; plant–insect interactions; sawflies; tropical rain forests.

FIGURE 1

Phylogenetic relationships for the gene PGD among the Inga-feeding sawfly MOTUs and a panel of voucher sequences for sawflies in the families Argidae, Pergidae (sister group to Argidae; Malm and Nyman, 2015) and Tenthredinidae. The tree shown is a majority-rule consensus tree constructed in MrBayes, using substitutions modeled as GTR+I+G for 1st and 2nd codon positions combined, and GTR+I+G for 3rd positions. We used a relaxed clock, with a birth-death speciation model. Numbers at nodes indicate posterior probability. Taxon labels are colored by sampling source: red MOTU numbers are larvae found feeding on Inga or Zygia, while other colors indicate reference sequences for adult Argidae, Pergidae, and Tenthredinidae.

FIGURE 2

Sawfly occurrence for each Inga host chemotype. Shown is the range and distribution of proportion of occurrence of sawfly MOTUs per Inga chemotype. Chemistry is represented by the main chemical classes found in Inga. AP, Amines + phenolics; AS, Amines + saponins; P, Phenolics; PS, Phenolics + saponins; S, Saponins. The box shows the median and the 25%- and 75% percentiles. The whiskers are the 1.5 × interquartile range; outliers are drawn as individual points.

FIGURE 3

Patterns of diversification in Argidae sawfly MOTUs, mapped against (A) the phylogeny of their Inga food plants, and (B) a phenogram of host chemical defenses (‘chemogram’). The match between topologies in each case was optimized using the cophylo command in the R Phytools package. The sawfly and Inga phylogenies are maximum clade credibility species trees produced from multilocus analyses in ^∗Beast, for four and ten loci respectively (A,B). Links and taxon names highlighted in bold are identified as individually significant in parafit analyses (see Supplementary Tables S4, S5), while links highlighted in red show additional examples of closely related sawflies feeding on geographically separated populations of the same host plant species. The remaining links are indicated as dashed lines. The geographic location of Inga populations is indicated in the taxon labels as follows: EC, Ecuador; FG, French Guiana; PAN, Panama; PE, Peru. Colored symbols at nodes on phylogenies indicate posterior probability (PP) support: red = PP from 0.9 to 1.0, blue = PP from 0.75 to 0.89. Inga species in (B) are color-coded by chemotype: black (phenolics), red (phenolics + amines), green (phenolics + saponins), blue (saponins) and purple (saponins + amines).

FIGURE 4

Principal coordinates analyses plots of sawfly MOTUS-Inga hosts associations in terms of Inga phylogeny. Each point in the figure represents an Inga species, including those on which sawflies were never found, colored red. Inga that are associated with sawflies are colored in black. Points that are close together in the phylogenetic ordination diagram indicate closely related Inga species. Lines connecting the points represent sawfly phylogenetic relationships. Inga species that are located at and below the coordinate −0.01 in the y axis represent basal branches in the Inga phylogeny.