Population-specific patterns of toxin sequestration in monarch butterflies from around the world

Abstract

Monarch butterflies are one of the preeminent examples of a toxin-sequestering animal, gaining protection against predators via cardenolides obtained from their milkweed host plants. Although cardenolide sequestration by monarchs has been studied in ecological, physiological, and phylogenetic contexts, relatively little research has surveyed genetic variation in the ability to sequester, nor has monarch sequestration been studied in relation to divergent host plant assemblages or variation in exposure to predation. Here, we use the monarch's recent global range expansion to test hypotheses about how cardenolide sequestration evolves over relatively contemporary time scales. First, we test for whether sympatric monarch/milkweed combinations have a sequestration advantage by rearing six geographically disparate monarch populations on six associated milkweed host species and measuring levels of sequestered cardenolides in a set of 440 adult butterflies. Second, we use monarchs from Guam - an oceanic island where birds have been functionally extirpated for approximately 40 years - to test hypotheses about how exposure to avian predation affects cardenolide sequestration. We find little overall evidence for increased sequestration on sympatric hosts. However, one monarch population (Puerto Rico) shows strong support for cross-host tradeoffs in sequestration ability, primarily driven by limited sequestration of polar cardenolides from two temperate North American milkweeds (Asclepias syriaca and A. speciosa). Monarchs from Guam show some evidence for reduced cardenolide sequestration in both a cross-island comparison of wild-caught butterflies as well as population-level comparisons of greenhouse-reared butterflies. Our results suggest that there is substantial genetic variation in sequestration ability (both within and between monarch populations) and that evolutionary history and contemporary species interactions may influence patterns of cardenolide sequestration.

The price of defence: toxins, visual signals and oxidative state in an aposematic butterfly

“…Oxidative state likely depends on the combination of genetic, environmental and gene by environment (G × E) interactions that determine an individual's condition. Monarchs show patterns of local adaptation to their host plants (based on larval growth rate [37]), and also show G × E interactions in sequestration ability [23] which may reflect either a lack of evolutionary history with different species of Asclepias , or a physiological trade-off in sequestration ability. Our results suggest that populations of monarchs that are sympatric with high cardenolide milkweeds could be less subject to oxidative damage, either because they have evolved higher antioxidant efficiency, or because they are able to accumulate more antioxidants to provide enhanced antioxidant protection.…”

The price of defence: toxins, visual signals and oxidative state in an aposematic butterfly

“…It is likely that oxidative state depends on the combination of genetic, environmental and gene by environment (GxE) interactions that determine an individual’s condition. Monarchs show patterns of local adaptation to their hostplants (based on larval growth rate [29]), and also show GxE interactions in sequestration ability [23] which may reflect either a lack of evolutionary history with different species of Asclepias , or a physiological trade-off in sequestration ability. Our results suggest that populations of monarchs that are sympatric with high cardenolide milkweeds could be less subject to oxidative damage, either because they have evolved higher antioxidant efficiency, or because they are able to accumulate more antioxidants to provide enhanced antioxidant protection.…”

“…Because there is substantial genetic variation in sequestration ability, and because evolutionary history and contemporary species interactions may influence patterns of cardenolide sequestration [23] we used monarchs from a single population. We reared them on four milkweed species (see table 1) that show within-and between-species, and amongpopulation variation in cardenolide concentration, diversity, and polarity [22,[24][25][26].…”

Trends and progress in studying butterfly migration

“…Monarch butterfly larvae ingest cardenolides from their hostplant—milkweeds, which is a toxic group of chemicals. Many species of North American milkweeds possess different proportions of these toxins, which remain intact in adult individuals (Freedman, Choquette, et al, 2021; Tan et al, 2019). By extracting these from adult butterflies and visualising them on a thin layer chromatography plate, they determined the ‘cardiac glycoside fingerprint’.…”

“…About 90% of monarchs in Mexico had developed on Asclepias syriaca —once the most abundant milkweed host in the midwestern US (Malcolm et al, 1989). One limitation of this approach is that some hostplant species contain a similar range of cardiac glycosides and some have none (Brower, 1995; Freedman, Choquette, et al, 2021; Malcolm et al, 1989; Tan et al, 2019).…”