Na⁺/K⁺-ATPase resistance and cardenolide sequestration: basal adaptations to host plant toxins in the milkweed bugs (Hemiptera: Lygaeidae: Lygaeinae)

Abstract

Despite sequestration of toxins being a common coevolutionary response to plant defence in phytophagous insects, the macroevolution of the traits involved is largely unaddressed. Using a phylogenetic approach comprising species from four continents, we analysed the ability to sequester toxic cardenolides in the hemipteran subfamily Lygaeinae, which is widely associated with cardenolide-producing Apocynaceae. In addition, we analysed cardenolide resistance of their Na þ /K þ -ATPases, the molecular target of cardenolides. Our data indicate that cardenolide sequestration and cardenolide-resistant Na þ /K þ -ATPase are basal adaptations in the Lygaeinae. In two species that shifted to non-apocynaceous hosts, the ability to sequester was secondarily reduced, yet NaATPase resistance was maintained. We suggest that both traits evolved together and represent major coevolutionary adaptations responsible for the evolutionary success of lygaeine bugs. Moreover, specialization on cardenolides was not an evolutionary dead end, but enabled this insect lineage to host shift to cardenolide-producing plants from distantly related families.

Gene duplications circumvent trade-offs in enzyme function: Insect adaptation to toxic host plants

“…Our results, like those of Bramer et al. (), show that the nervous tissue of O. fasciatus is nevertheless highly insensitive to ouabain, an extent of insensitivity that we only reached with the construct mimicking the A copy of O. fasciatus . Similar to O. fasciatus nervous tissue this construct retained about 60% of Na,K‐ATPase activity at 10 −3 M ouabain.…”

“…The IC 50 value and overall ouabain sensitivity curve of D. melanogaster , on the other hand, are similar to the ones of Kleidoceris resedae (Hemiptera, Lygaeidae), the nonadapted outgroup comparison to O. fasciatus and the other Lygaeinae used by Bramer et al. ().…”

“…; Bramer et al. ). In addition, O. fasciatus and the other investigated Lygaeinae species express a Na,K‐ATPase in their nervous tissue that has the lowest binding affinity to cardenolides of all insects tested so far (Moore and Scudder ; Bramer et al.…”

“…In addition, O. fasciatus and the other investigated Lygaeinae species express a Na,K‐ATPase in their nervous tissue that has the lowest binding affinity to cardenolides of all insects tested so far (Moore and Scudder ; Bramer et al. ). Genetic analysis of the Na,K‐ATPase α‐subunit of O. fasciatus revealed that it not only bears the greatest number of amino acid exchanges in the target site for cardenolides observed so far (Dobler et al.…”

Cardenolide‐defended milkweed bugs do not evoke learning in Nephila senegalensis spiders

“…True bugs of the Lygaeinae (Heteroptera: Lygaeidae), commonly known as milkweed bugs, are seed predators and are mostly associated with milkweeds and other plants of the Apocynaceae (Ralph, ; Wheeler, ). These red and black colored species tolerate and take up deterrent plant chemicals (usually cardenolides) with the most famous example being the large milkweed bug Oncopeltus fasciatus (Dallas, 1852) (Bramer, Dobler, Deckert, Stemmer, & Petschenka, ; Duffey & Scudder, ; Scudder & Duffey, ; Scudder, Moore, & Isman, ; Von Euw, Reichstein, & Rothschild, ). Both the nymphs and adults of this brightly colored species obtain a variety of potentially toxic, plant produced cardenolides from Asclepias seeds, whereas species reared on sunflower seeds lack these chemicals (Duffey & Scudder, ; Lohr et al., ; Scudder et al., ).…”