A phylogenomic analysis of lichen-feeding tiger moths uncovers evolutionary origins of host chemical sequestration

Abstract

Host species utilize a variety of defenses to deter feeding, including secondary chemicals. Some phytophagous insects have evolved tolerance to these chemical defenses, and can sequester secondary defense compounds for use against their own predators and parasitoids. While numerous studies have examined plant-insect interactions, little is known about lichen-insect interactions. Our study focused on reconstructing the evolution of lichen phenolic sequestration in the tiger moth tribe Lithosiini (Lepidoptera: Erebidae: Arctiinae), the most diverse lineage of lichen-feeding moths, with 3000 described species. We built an RNA-Seq dataset and examined the adult metabolome for the presence of lichen-derived phenolics. Using the transcriptomic dataset, we recover a well-resolved phylogeny of the Lithosiini, and determine that the metabolomes within species are more similar than those among species. Results from an initial ancestral state reconstruction suggest that the ability to sequester phenolics produced by a single chemical pathway preceded generalist sequestration of phenolics produced by multiple chemical pathways. We conclude that phenolics are consistently and selectively sequestered within Lithosiini. Furthermore, sequestration of compounds from a single chemical pathway may represent a synapomorphy of the tribe, and the ability to sequester phenolics produced by multiple pathways arose later. These findings expand on our understanding of the interactions between Lepidoptera and their lichen hosts.

A deeper meaning for shallow‐level phylogenomic studies: nested anchored hybrid enrichment offers great promise for resolving the tiger moth tree of life (Lepidoptera: Erebidae: Arctiinae)

“…Previous support for this finding has varied from weak (BS = 30% and 41%, respectively; Zenker et al, 2016;Posterior probability = 0.83 and 0.86, respectively;Simmons et al, 2012) to relatively strong (BS = 98% and 75%, respectively; Zaspel et al, 2014). Despite a somewhat different taxon sampling scheme (50% and 30% generic-level overlap, respectively), our results within Lithosiini are consistent with recent work based on traditional markers as well as transcriptome data, at least within subtribes (Zaspel et al, 2014;Scott Chialvo et al, 2018). The relationships among subtribes within the Lithosiini were markedly different, however, particularly compared to results based on transcriptomic evidence.…”

“…Our NOC1 probe set recovered results at deep taxonomic levels (e.g., tribal, subtribal) that are largely congruent with the results of previous molecular studies (Zahiri et al, 2011;Zahiri et al, 2012;Zaspel et al, 2014;Zenker et al, 2016;Scott Chialvo et al, 2018). However, we also recovered novel and well-supported relationships within the Arctiinae which have eluded previous studies utilizing traditional markers, placing arctiine taxonomy, particularly at the subtribal level, in a potential state of taxonomic flux (Zaspel et al, 2014;Rönkä et al, 2016;Zenker et al, 2016).…”

“…The relationships among subtribes within the Lithosiini were markedly different, however, particularly compared to results based on transcriptomic evidence. This transcriptomic data moderately supported (BS = 87%) the topology recovered in the sensitivity analysis utilizing the intermediately sized loci subsets (i.e., 175-375 loci) of the NOC1 probe set [i.e., (Nudariina, Cisthenina), (Lithosiina)], rather than the topology we recovered utilizing the full probe set {i.e., [Nudariina, (Cisthenina, Lithosiina)]} (Scott Chialvo et al, 2018). The transcriptome-based study sampled a greater diversity of Lithosiini, indicating that a denser sampling of taxa and/or more loci with more conserved sites or less gene tree discordance may be necessary to help clarify the relationships among subtribes within Lithosiini.…”

“…Among Lepidoptera, transcriptomic data have proven useful in reconstructing framework phylogenies for deep divergences at the level of order (Bazinet et al, 2013;Kawahara & Breinholt, 2014) and within (Scott Chialvo et al, 2018). A recent study by Breinholt et al (2018) combined transcriptomic data with data derived from an AHE probe set ('Lep1') to resolve relationships within Lepidoptera at both deep and shallow taxonomic levels.…”

Molecular phylogeny of the Lichen Tiger Moths (Lepidoptera: Erebidae: Arctiinae: Lithosiini) of the Western Hemisphere

“…Not only do lichens offer a food source generally free from competition, they possess a chemical arsenal that can be exploited. It has been demonstrated by many researchers that the larvae of lithosiines possess metabolic pathways to deal with lichen toxins and actually sequester modifications of these for their own protection in all life stages (Hesbacher et al 1995;Wagner et al 2008;Conner 2009;Scott et al 2014;Anderson et al 2017;Scott-Chailvo et al 2018). Adults of most lithosiines exhibit aposematic coloration, however the larvae are dull-colored, secretive nocturnal feeders (Wagner 2005, Conner 2009).…”