Feeding specialization and host-derived chemical defense in Chrysomeline leaf beetles did not lead to an evolutionary dead end

Abstract

Combination of molecular phylogenetic analyses of Chrysomelina beetles and chemical data of their defensive secretions indicate that two lineages independently developed, from an ancestral autogenous metabolism, an energetically efficient strategy that made the insect tightly dependent on the chemistry of the host plant. However, a lineage (the interrupta group) escaped this subordination through the development of a yet more derived mixed metabolism potentially compatible with a large number of new host-plant associations. Hence, these analyses on leaf beetles document a mechanism that can explain why high levels of specialization do not necessarily lead to "evolutionary dead ends."

Figure 1

(a) Strict consensus among the 120 MP trees (TL = 1532) with bootstrap values/decay indices indicated above the branches. (b) ML phylogram (−ln L = 10381.998, Ti/Tv = 1.734, Pinv = 0.421, γ shape parameter =0.536) with quartet puzzling support values >50% indicated above the branches. Scale is in percent expected substitution per position.

Figure 2

ML phylogram of all species from the interrupta clade with a chosen subset of outgroup taxa. Numbers above the branches are bootstrap proportions >50% (400 replicates). Scale is in percent-expected substitution per position.

Figure 3

(a) MP reconstruction of chemical defense strategies on the MP strict consensus from Fig. 1a; red, autogenous monoterpene iridoids; green, salicylaldehyde derived from salicin (sequestered from Salicaceae); blue, mixed metabolism, i.e., butyric acids and esters of them originating from esterification of de novo-synthesized butyric acids by alcohols taken up from the food plant. Some taxa within the interrupta lineage have a dual defense combining the mixed and host-derived metabolisms. (b) MP reconstruction of host plant associations. Que, Queyras (France); MC, Massif Central (France); Cze, Czech Republic; Finl, Finland. Asterisks indicate North American species within the interrupta group. (c–e) Typical gas chromatograms characterizing, mixed-metabolism, dual, and host-derived defenses, respectively; blue peaks, butyric acids and esters of them; green peak, salicylaldehyde; rt, retention time. The low bootstrap support for the two nodes indicated by a diamond do not challenge the general pattern of chemical defense evolution uncovered here (see text for details).