Variation of chemical compounds in wild Heliconiini reveals ecological factors involved in the evolution of chemical defenses in mimetic butterflies

Abstract

Evolutionary convergence of color pattern in mimetic species is tightly linked with the evolution of chemical defenses. Yet, the evolutionary forces involved in natural variations of chemical defenses in aposematic species are still understudied. Herein, we focus on the evolution of chemical defenses in the butterfly tribe Heliconiini. These neotropical butterflies contain large concentrations of cyanogenic glucosides, cyanide‐releasing compounds acting as predator deterrent. These compounds are either de novo synthesized or sequestered from their Passiflora host plant, so that their concentrations may depend on host plant specialization and host plant availability. We sampled 375 wild Heliconiini butterflies across Central and South America, covering 43% species of this clade, and quantify individual variations in the different CGs using liquid chromatography coupled with tandem mass spectrometry. We detected new compounds and important variations in chemical defenses both within and among species. Based on the most recent and well‐studied phylogeny of Heliconiini, we show that ecological factors such as mimetic interactions and host plant specialization have a significant association with chemical profiles, but these effects are largely explained by phylogenetic relationships. Our results therefore suggest that shared ancestries largely contribute to chemical defense variation, pointing out at the interaction between historical and ecological factors in the evolution of Müllerian mimicry.

Evolutionary and ecological processes influencing chemical defense variation in an aposematic and mimeticHeliconiusbutterfly

“…By altering the nature of mimetic relationships or selection for increased defense levels on a new warning signal form, evolvability of defense traits could drive the evolution and spread of new color patterns and the reproductive isolation that may follow, potentially even leading to the formation of new species (Jiggins et al, 2001;Mallet et al, 1998). A phylogenetic signal in the cyanogenic glucoside chemical profile in the Heliconiini tribe supports this idea (de Castro et al, 2019;Sculfort et al, 2020) and underscores the potential for adaptive evolution in chemical defense traits to influence evolutionary trajectories in mimicry systems. However, more empirical data is called for in future studies to estimate levels of evolutionary potential and patterns of selective responses in defensive traits in aposematic and mimetic species.…”

“…These populations could have specialized on a particular Passiflora host, selecting for a major decrease in biosynthesis, and leading to local adaptation in the biosynthesized toxicity level, in line with the demonstrated high evolutionary potential of this trait. Cases of zero levels of biosynthesized cyanogens in Heliconius are rare, but previous observations of such species provide evidence for their high levels of host plant specialization and plant defense compound sequestration 3,62 . Such adaptive radiations of Heliconius driven by host plant niche use could also have been facilitated by the high evolutionary potential in biosynthesized cyanogenic toxicity leading to local adaptations in the sequestrationbiosynthesis balance.…”

“…Although biosynthesis is not uncommon in chemically defended animals (Bowers, 1992;Ruxton et al, 2018), it is uncommon among chemically defended Lepidoptera (Nishida, 2002). There is substantial variation in the amounts and types of cyanogens among different Heliconius species (Arias et al, 2016;Cardoso & Gilbert, 2013;de Castro et al, 2019;Engler-Chaouat & Gilbert, 2007;Sculfort et al, 2020).…”

Heliconiusbutterflies host characteristic and phylogenetically structured adult-stage microbiomes

“…Within Heliconiini, the genus Heliconius exhibits unique feeding and life history traits relative to other genera: larvae feed on young passion-vine shoots and leaves as opposed to old foliage, adults of most species (besides H. aoede) feed on pollen as well as nectar, and they have distinctive defensive chemistry and a greatly extended adult-stage lifespan of several months (18,24). These traits could influence and be influenced by microbiomes in many ways.…”

Assessing the Role of Developmental and Environmental Factors in Chemical Defence Variation in Heliconiini Butterflies

“…Finally, regardless of how defensive compounds are obtained, chemical defences can also vary according to sex (Jeckel et al 2015a, b;Kissner et al 2000;Nahrstedt and Davis 1983), developmental stage (Columbus-Shenkar et al, 2018;Dossey et al, 2008), and age (Jeckel et al 2015a, b;Hayes et al 2009;Zagrobelny et al 2007a, b). Such variation can stem from physiological and/or ecological differences, such as differences in diet, and as a result, large qualitative and quantitative variation in chemical defences can occur between individuals, even within a given population or species (Alape-Girón et al 2008;María Arenas et al 2015;McGugan et al 2016;Sculfort et al 2020).…”