Evolutionary implications of pyrrolizidine alkaloid assimilation by danaine and ithomiine larvae (Lepidoptera: Nymphalidae)

Abstract

Summary. Larvae of danaine and ithomiine butterflies assimilate pyrrolizidine alkaloids painted on their larval host plants. This finding supports the theory of the common ancestral use of these compounds by Ithomiinae and Danainae. Key words. Pyrrolizidine alkaloids; Ithomiinae; Danainae; phylogenetic relationships; assimilation of host-plant defensive chemicals.Larvae of more than 95 % of the species of Ithomiinae butterflies feed on plants of the family Solanaceae 1. However, four primitive genera (Tellervo, Tithorea, Elzunia and Aeria) feed on Apocynaceae (tribe Parsonsieae), whose leaves may contain pyrrolizidine alkaloids (PAs) 2-5. In some Ithomiinae, these alkaloids function as male pheromone precursors 6-1~ and as a chemical defense against predation by the spider Nephila clavipes al -13. Larvae of Tellervo and Tithorea sequester PAs from their host plants 4, 5, while Aeria probably uses host plant compounds as precursors for PA biosynthesis s. The adults of Solanaceae-feeding Ithomiinae assimilate PAs from their food sources (nectar of Boraginaceae and Asteraceae) and decomposing leaves of Boraginaceae (mainly Heliotropium), since Solanaceae do not contain PAs 11-t3. It has been suggested that the ancestral host plant of the closely related Danainae and Ithomiinae 14, 15 contained PAs, leading to a dependence of these bufferflies on these alkaloids which has been retained up to the present 6, 7. Danaus plexippus larvae assimilated PAs from a PA-free host plant which was treated with these alkaloids, suggesting that this danaine maintains the capacity for PA sequestration and storage probably used by its ancestors to obtain PAs from their host plants 16 In this work we show that Ithomiinae larvae which feed on PA-free plants also retain the capacity for PA sequestration and storage. On the basis of this finding we discuss the possible common ancestry of Ithomiinae and Danainae, and of their larval host plants. Material and methodsEggs and larvae of species of Ithomiinae, Danainae, Pieridae, and their host plants (table 1) were obtained in the regions of Campinas and Jundiai, Silo Paulo, Brazil. The Danainae were included as a closely related group (sistergroup of Ithomiinae is) and the Pieridae as a control, since they do not utilize plants with PAs in their life cycle. Larvae were reared at room temperature (about 25 ~ on leaves of their respective food plants. The leaves were changed daily. The third instar larvae were fed daily with PA ascorbate painted on the host-plant leaves, until pupation. The PA ascorbate salt was prepared with the free bases of PAs from Eupatorium laevigatum (echinatine and three other non-identified alkaloids 5) plus ascorbic acid (15:8 w/w). The PA ascorbate was utilized because it is water soluble (free bases are poorly miscible with water and soluble in organic solvents). PA N-oxides, which are soluble in water, could also be utilized, but the data on transformation from free bases to N-oxides would be lost. Controls were included for each butterfly species; they were given...

Storage and metabolism of radioactively labeled pyrrolizidine alkaloids by butterflies and larvae of Mechanitis polymnia (Lepidoptera: Nymphalidae, Ithomiinae)

“…This indicates a host plant shift of the more advanced ithomiines from PA containing species (most likely Apocynaceae) to the Solanaceae which do not have PAs. A mechanistic argument favoring this host-switch hypothesis is the observation that larvae of advanced ithomiine easily take up alkaloids from a PA mixture painted on their host leaves (Trigo & Motta 1990). The present study confirms and extends these results and shows that M. polymnia larvae possess the ability to N-oxidize sequestered PAs.…”

Brain composition in Godyris zavaleta, a diurnal butterfly, Reflects an increased reliance on olfactory information

“…This suggests that the signal is distributed over larger spatial scales than typical for butterflies. Most species of Danainae also utilize PA‐derived pheromones in sexual communication (Pliske et al, ; Trigo and Motta, ; Honda et al, ). Danainae have hair‐pencils located at the tip of the abdomen that are displayed during courtship and persistently brought into contact with the hind‐wing, to aid dissemination of chemical secretions (Müller, ; Boppré et al, ; Brower and Jones, ).…”

“…A greater role for olfaction in G. zavaleta ecology is further suggested by their derived mating behavior. Ithomiines use pyrrolizidine alkaloids (PA) both as precursors for pheromone synthesis and for chemical protection (Pliske et al, ; Trigo and Motta, ). The majority of ithomiines obtain these PAs pharmacophagously as adults, by males feeding on the nectar of Boraginaceae and Asteraceae, or decomposing Boraginaceae leaves, in particular the genus Heliotropium (Brown, ; Trigo and Motta, ), to which males show a strong olfactory attraction (Pliske et al, ).…”

“…Ithomiines use pyrrolizidine alkaloids (PA) both as precursors for pheromone synthesis and for chemical protection (Pliske et al, ; Trigo and Motta, ). The majority of ithomiines obtain these PAs pharmacophagously as adults, by males feeding on the nectar of Boraginaceae and Asteraceae, or decomposing Boraginaceae leaves, in particular the genus Heliotropium (Brown, ; Trigo and Motta, ), to which males show a strong olfactory attraction (Pliske et al, ). Females obtain the derived defense compounds from males through the spermatophore (Brown, ), as part of a “nuptial gift”, potentially meaning pheromone production serves as an honest indicator of a male's ability to collect PAs (Rutowski, ).…”

Evolution of pyrrolizidine alkaloid biosynthesis in Apocynaceae: revisiting the defence de‐escalation hypothesis

“…Only a few species sequester PAs via larval feeding that are retained through metamorphosis: Idea leuconoe ( Fig. 1c,d), proposed as a model of plesiomorphic Danainae (Honda et al, 1997), Tellervo zoilus (Orr et al, 1996) and Tithorea harmonia (Trigo & Motta, 1990). However, larvae of danaine species that have PA-free host plants (e.g.…”