Sequestration of Defenses against Predators Drives Specialized Host Plant Associations in Preadapted Milkweed Bugs (Heteroptera: Lygaeinae)

Abstract

Host plant specialization across herbivorous insects varies dramatically, but while the molecular mechanisms of host-plant adaptations are increasingly known, we often lack a comprehensive understanding of the selective forces that favor specialization. The milkweed bugs (Heteroptera: Lygaeinae) are engaged in ancestrally specialized associations with plants of the Apocynaceae from which they commonly sequester cardiac glycosides for defense, facilitated by resistant Na + /K + -ATPases and adaptations for transport, storage and discharge of toxins. Here, we show that three Lygaeinae species independently colonized four novel non-apocynaceous hosts that convergently produce cardiac glycosides. A fourth species shifted to a new source of toxins by tolerating and sequestering alkaloids from meadow saffron (Colchicum autumnale, Colchicaceae). Across three milkweed bug species tested, feeding on seeds containing toxins did not improve growth or speed of development, and even impaired growth and development in two species, but sequestration mediated protection of milkweed bugs against two natural predators: lacewing larvae and passerine birds. We conclude that physiological preadaptations and convergent phytochemistry facilitated novel specialized host associations. Since toxic seeds did not improve but either impaired growth or at most had neutral effects, selection by predators on sequestration of defenses, rather than the exploitation of additional profitable dietary resources, can lead to obligatory specialized host associations in otherwise generalist insects.

Antioxidant availability trades off with warning signals and toxin sequestration in the large milkweed bug (Oncopeltus fasciatus)

“…It is possible that the variance in the hue of the black hemelytra patches that correlated with sequestration would be difficult to detect because the Euclidian distance varies by ~2.5, and because of the geometry of Lab color space where the length of the b * axes is reduced for dark colors. Whether the resource‐dependent variation in warning signals and cardenolide concentrations are perceived by natural predators will be important to test in the future to understand how variation and correlations in primary and secondary defenses is maintained in aposematic species (Ottocento et al, 2023 ; Petschenka et al, 2022 ; Pokharel et al, 2020 ; White & Umbers, 2021 ).…”

“…O. fasciatus do experience oxidative damage in other contexts (López‐Muñoz et al, 2019 ), so the stable levels of damage we measured here could be related to their higher cardenolide resistance rather than a general resistance to oxidative stress. A comparative analysis of related milkweed bug responses to sequestration would be worthwhile, and aid in our understanding of host shifts that are known to occur in the Lygaeinae (Petschenka et al, 2022 ).…”

Metabolization and sequestration of plant specialized metabolites in insect herbivores: Current and emerging approaches

“…Further microbiological studies can be conducted to assess the contribution of associated organisms (microbes from the digestive system) to PSM resistance in insects ( Adams et al, 2013 ; Boone et al, 2013 ; Hammerbacher et al, 2013 ; Mason et al, 2014 ; Vilanova et al, 2016 ; Welte et al, 2016 ; Jing et al, 2020 ; Shukla and Beran, 2020 ). Finally, field trials and experimental selection assays can further elucidate the ecological and evolutive significance of PSM resistance in insects ( Erb and Robert, 2016 ; Zhang et al, 2019a ; Machado et al, 2020 ; Petschenka et al, 2022 ).…”

Metabolization and Sequestration of Plant Specialized Metabolites in Insect Herbivores: Current and Emerging Approaches

“…Further microbiological studies can be conducted to assess the contribution of associated organisms (microbes from the digestive system) to PSM resistance in insects (Adams et al, 2013;Boone et al, 2013;Hammerbacher et al, 2013;Mason et al, 2014;Vilanova et al, 2016;Welte et al, 2016;Jing et al, 2020;Shukla and Beran, 2020). Finally, field trials and experimental selection assays can further elucidate the ecological and evolutive significance of PSM resistance in insects (Erb and Robert, 2016;Zhang et al, 2019;Machado et al, 2020;Petschenka et al, 2022). (Barbehenn, 1999).…”