Chemical convergence between a guild of facultative myrmecophilous caterpillars and host plants

Abstract

1. Ants exert strong selective pressure on herbivorous insects, although some caterpillars can live in symbiosis with them using chemical defensive strategies.2. We investigated the adaptive resemblance of cuticular hydrocarbons (CHCs) in multitrophic systems involving a guild of facultative myrmecophilous caterpillar species (Lepidoptera: Lycaenidae), tending ants (Hymenoptera: Formicidae), and host plants from three families. We hypothesised that the CHCs of the caterpillars would resemble those of their host plants (chemical camouflage).3. We analysed CHCs using gas chromatography/mass spectrometry. Morisita's similarity index (SI) was used to compare CHC profiles of caterpillar species with different types of ant associations (commensal or mutualistic), ants, and host plants.4. We found strong convergence between caterpillars' CHCs and plants, especially for commensal species that do not provide secretion rewards for ants. Moreover, we found unexpected chemical convergence among mutualistic (trophobiotic) caterpillar species that offer caloric reward secretions to ants.5. These results show that the studied caterpillars acquire CHCs through their diet and that they vary according to host plant species and type of ant association (commensalism or mutualism). This 'chemical camouflage' of myrmecophilous caterpillars may have arisen as a defensive strategy allowing coexistence with ants on plants, whereas 'chemical conspicuousness' may have evolved in the context of honest signalling between mutualistic partners.6. We suggest the existence of chemical mimicry among myrmecophilous species, especially between mutualistic caterpillars. Cuticular chemical mixtures can play a key adaptive role in decreasing ant attacks and increasing caterpillar survival in multimodal sensory systems.

On the adaptive meaning of chemically insignificant cues in multitrophic caterpillar-ant-plant symbioses

“…The caterpillars studied here are presumed to have mutualistic interactions with ants, so our initial hypothesis that caterpillars would have informative CHC profiles, as reported for other trophobiotic species (e.g. [6,[18][19][20]), was not confirmed. The strategies of chemical mimicry and chemical camouflage were discarded due to the low concentrations and number of compounds and incongruence with the CHC profiles of the ants or host plants.…”

“…CC-BY-NC-ND 4.0 International license made available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is The cuticular chemical composition of the studied ants, caterpillars, and host plants was assessed by extracting the compounds following [6] by immersing the samples for 5 min in 5 ml of hexane (99%, SupraSolv, Merck, Germany), followed by removal from hexane with entomological tweezers that were previously cleaned with hexane. Pools of about 10 individuals (workers) per sample were used for tending ants, while for the caterpillars, one individual was used when it was in the last instar or a pool of up to five individuals when they were from first to the fourth instar.…”

“…Besides these strategies, ants can learn to recognise the CHC profiles of mutualistic partners, even when they are neither congruent with those of the ants nor the host plants, and thus avoid attacking them [18][19][20]. These non-congruent profiles may constitute conspicuousness strategy (sensu [6]).…”

“…Studies with the chemical profiles of myrmecophilous caterpillars with different kinds of interactions with ants (commensalism, mutualism, or parasitism), different degrees of specificity (facultative or obligate), and different feeding habits (herbivorous, omnivorous or carnivorous) have identified several kinds of chemical strategies (e.g. [6,17,28–29]). Thus, myrmecophilous caterpillars are excellent models for studying the ecology and evolution of different chemical strategies mediated by cuticular compounds [30].…”

“…Thus, the aim of this study was to perform chemical analyses and experiments in the field to identify the functional role of the CHC profiles of these caterpillars. Studies with species in the sister family Lycaenidae showed that trophobiotic caterpillars (that produce caloric rewards) generally have conspicuous CHCs that may appease ant aggressiveness or be associated with resource availability [6,20,33]. Based on this information, we hypothesised that the CHC profiles in the two caterpillar species would be informative to their respective tending ants and that, for this reason, they would be recognised as mutualistic partners and would not be attacked.…”