A switch to feeding on cycads generates parallel accelerated evolution of toxin tolerance in two clades ofEumaeuscaterpillars (Lepidoptera: Lycaenidae)

Abstract

We assembled a complete reference genome of Eumaeus atala, an aposematic cycad-eating hairstreak butterfly that suffered near extinction in the United States in the last century. Based on an analysis of genomic sequences of Eumaeus and 19 representative genera, the closest relatives of Eumaeus are Theorema and Mithras. We report natural history information for Eumaeus, Theorema, and Mithras. Using genomic sequences for each species of Eumaeus, Theorema, and Mithras (and three outgroups), we trace the evolution of cycad feeding, coloration, gregarious behavior, and other traits. The switch to feeding on cycads and to conspicuous coloration was accompanied by little genomic change. Soon after its origin, Eumaeus split into two fast evolving lineages, instead of forming a clump of close relatives in the phylogenetic tree. Significant overlap of the fast evolving proteins in both clades indicates parallel evolution. The functions of the fast evolving proteins suggest that the caterpillars developed tolerance to cycad toxins with a range of mechanisms including autophagy of damaged cells, removal of cell debris by macrophages, and more active cell proliferation.

Evolutionary trade-offs between male secondary sexual traits revealed by a phylogeny of the hyperdiverse tribe Eumaeini (Lepidoptera: Lycaenidae)

“…The tribe encompasses a staggering array of ecological and behavioural diversity, thriving in habitats from the Alaskan subarctic to temperate Chile, from sea level to the high Andes, and in environments as distinct as the Amazon rainforest and the Atacama Desert [5][6][7]. Species of Eumaeini possess a broad spectrum of adaptations to avoid predation, including complex larval interactions with ants, eyespots and tails that resemble a 'false head' at their posterior end, and aposematic coloration advertising toxins sequestered from their host plants [8][9][10][11][12].…”

Genomics‐based higher classification of the species‐rich hairstreaks (Lepidoptera: Lycaenidae: Eumaeini)

“…Semi‐hemispherical abdominal brush organs are unique to species of Eumaeus , Theorema and Mithras (Robbins et al, 2021). Piliform scales on the dorsal hindwing of male Eumaeus childrenae (Grey) are absent in females and may be androconia (Robbins et al, 2021).…”

“…Semi‐hemispherical abdominal brush organs are unique to species of Eumaeus , Theorema and Mithras (Robbins et al, 2021). Piliform scales on the dorsal hindwing of male Eumaeus childrenae (Grey) are absent in females and may be androconia (Robbins et al, 2021). A dorsal forewing scent pad occurs in all species of Mithras , Micandra and Brevianta , but in some species of the latter two, there are additional complex androconial structures that have not been detailed morphologically.…”

“…In contrast, the caterpillars of some genera specialize primarily on one plant family. Examples include Eumaeus Hübner on Zamiaceae (Robbins et al, 2021), Evenus Hübner on new leaves of Sapotaceae (Janzen & Hallwachs, 2021; Robbins, 2004a), a lineage of Strymon Hübner on Bromeliaceae (Robbins, 2010a), Arawacus Kaye on Solanaceae (Robbins, 2000) and Thereus Hübner on Loranthaceae (Heredia & Robbins, 2016). The concept that caterpillar food plant associations, such as specialization, generalization and the frequency of host shifts, shape diversification has been widely supported (e.g., Braga, Guimarães, Wheat, Nylin, & Janz, 2018; Fordyce, 2010; Hardy & Otto, 2014; Janz, 2011; Janz, Nylin, & Wahlberg, 2006; St Laurent, Carvalho, Earl, & Kawahara, 2021).…”

“…Sequencing complete genomes of Eumaeini butterflies using museum specimens provides a prodigious quantity of phylogenetic data (Cong et al, 2016, 2017; Robbins et al, 2021). In this paper, we infer phylogenetic relationships using three datasets of protein‐coding genes.…”