Dietary cardenolides enhance growth and change the direction of the fecundity‐longevity trade‐off in milkweed bugs (Heteroptera: Lygaeinae)

Pokharel, Prayan; Steppuhn, Anke; Petschenka, Georg

doi:10.1002/ece3.8402

Cited by 12 publications

(18 citation statements)

References 96 publications

(119 reference statements)

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“…Our results from feeding Oncopeltus diets with purified glycosylated aspecioside and labriformin support these past studies. Nonetheless, another recent study fed Oncopeltus prepared diets of pure cardenolides (a mix of ouabain and digitoxin), revealing some costs ( 46 ). Although Oncopeltus showed faster nymphal growth, increased body mass, and enhanced longevity when fed diets with cardenolides, fecundity was reduced by 50% when cardenolides were continued on their diets as adults (at a dose of 6 mg/g dry mass).…”

Section: Discussionmentioning

confidence: 99%

Functional evidence supports adaptive plant chemical defense along a geographical cline

Agrawal

Alba

López‐Goldar

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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Environmental clines in organismal defensive traits are usually attributed to stronger selection by enemies at lower latitudes or near the host’s range center. Nonetheless, little functional evidence has supported this hypothesis, especially for coevolving plants and herbivores. We quantified cardenolide toxins in seeds of 24 populations of common milkweed ( Asclepias syriaca ) across 13 degrees of latitude, revealing a pattern of increasing cardenolide concentrations toward the host's range center. The unusual nitrogen-containing cardenolide labriformin was an exception and peaked at higher latitudes. Milkweed seeds are eaten by specialist lygaeid bugs that are even more tolerant of cardenolides than the monarch butterfly, concentrating most cardenolides (but not labriformin) from seeds into their bodies. Accordingly, whether cardenolides defend seeds against these specialist bugs is unclear. We demonstrate that Oncopeltus fasciatus (Lygaeidae) metabolized two major compounds (glycosylated aspecioside and labriformin) into distinct products that were sequestered without impairing growth. We next tested several isolated cardenolides in vitro on the physiological target of cardenolides (Na + /K + -ATPase); there was little variation among compounds in inhibition of an unadapted Na + /K + -ATPase, but tremendous variation in impacts on that of monarchs and Oncopeltu s. Labriformin was the most inhibitive compound tested for both insects, but Oncopeltus had the greater advantage over monarchs in tolerating labriformin compared to other compounds. Three metabolized (and stored) cardenolides were less toxic than their parent compounds found in seeds. Our results suggest that a potent plant defense is evolving by natural selection along a geographical cline and targets specialist herbivores, but is met by insect tolerance, detoxification, and sequestration.

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Section: Discussionmentioning

confidence: 99%

Functional evidence supports adaptive plant chemical defense along a geographical cline

Agrawal

Alba

López‐Goldar

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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“…Handling/detoxifying of defensive compounds in its plant diet also comes at a cost to developmental traits and warning signal expression (Lindstedt et al, 2010 ; Reudler et al, 2015 ). Similarly, the fecundity of cardenolide‐sequestering Oncopeltus fasciatus milkweed bugs was reduced when constantly artificially maintained on cardenolide‐containing diet, although in general, cardenolide exposure was associated with positive fitness effects (Pokharel et al, 2021 ).In the gregarious social Diprion pini pine sawfly, increased allocation to defensive secretion incurs costs in growth, immunity, and survival (Björkman & Larsson, 1991 ; Lindstedt et al, 2018 ), and in the pipevine swallowtail ( Battus philenor ) butterfly, toxin content is negatively correlated with fat content (Fordyce & Nice, 2008 ). Most evidence of defense costs is from the very few studies on species that biosynthesize their own chemical defenses, in contrast to the more numerous studies on species which sequester the defensive compounds of their host plants and often show neutral or positive fitness consequences of increasing defense levels (reviewed by: Bowers, 1992 ; Ruxton et al, 2018 ; Zvereva & Kozlov, 2016 ).…”

Section: Discussionmentioning

confidence: 99%

Condition dependence in biosynthesized chemical defenses of an aposematic and mimetic Heliconius butterfly

Mattila

Jiggins

Saastamoinen

2022

Ecology and Evolution

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Aposematic animals advertise their toxicity or unpalatability with bright warning coloration. However, acquiring and maintaining chemical defenses can be energetically costly, and consequent associations with other important traits could shape chemical defense evolution. Here, we have tested whether chemical defenses are involved in energetic trade‐offs with other traits, or whether the levels of chemical defenses are condition dependent, by studying associations between biosynthesized cyanogenic toxicity and a suite of key life‐history and fitness traits in a Heliconius butterfly under a controlled laboratory setting. Heliconius butterflies are well known for the diversity of their warning color patterns and widespread mimicry and can both sequester the cyanogenic glucosides of their Passiflora host plants and biosynthesize these toxins de novo . We find energetically costly life‐history traits to be either unassociated or to show a general positive association with biosynthesized cyanogenic toxicity. More toxic individuals developed faster and had higher mass as adults and a tendency for increased lifespan and fecundity. These results thus indicate that toxicity level of adult butterflies may be dependent on individual condition, influenced by genetic background or earlier conditions, with maternal effects as one strong candidate mechanism. Additionally, toxicity was higher in older individuals, consistent with previous studies indicating accumulation of toxins with age. As toxicity level at death was independent of lifespan, cyanogenic glucoside compounds may have been recycled to release resources relevant for longevity in these long‐living butterflies. Understanding the origins and maintenance of variation in defenses is necessary in building a more complete picture of factors shaping the evolution of aposematic and mimetic systems.

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“…However, it is methodologically difficult to separate the costs of sequestration from other potential effects of plant allelochemicals [56]. Future work could focus on comparative phytochemical profiles to understand resource availability, and experiments that control nutritional content while manipulating toxin content [57].…”

Section: Discussionmentioning

confidence: 99%

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

Blount

Rowland

Mitchell

et al. 2021

Preprint

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In a variety of aposematic species, the conspicuousness of an individual's warning signal and the quantity of its chemical defence are positively correlated. This apparent honest signalling in aposematism is predicted by resource competition models which assume that the production and maintenance of aposematic defences compete for access to antioxidant molecules that have dual functions as pigments directly responsible for colouration and in protecting against oxidative lipid damage. Here we study a model aposematic system - the monarch butterfly (Danaus plexippus) and make use of the variable phytochemistry of its larval host-plant, milkweeds (Asclepiadaceae), to manipulate the concentration of sequestered cardenolides. We test two fundamental assumptions of resource competition models: that (1) the possession of secondary defences is associated with costs in the form of oxidative lipid damage and reduced antioxidant defences; and (2) that oxidative damage or decreases in antioxidant defences can reduce the capacity of individuals to produce aposematic displays. Monarch caterpillars that sequestered the highest concentrations of cardenolides exhibited higher levels of oxidative lipid damage as adults. The relationship between warning signals, cardenolide concentrations and oxidative damage differed between the sexes. In male monarchs conspicuousness was explained by an interaction between oxidative damage and sequestration: as males sequester more cardenolides, those with high levels of oxidative damage become less conspicuous, while those that sequester lower levels of cardenolides equally invest in conspicuous with increasing oxidative damage. There was no significant effect of oxidative damage or concentration of sequestered cardenolides on female conspicuousness. Our results demonstrate physiological linkage between the production of coloration and protection from autotoxicity, that warning signals can be honest indicators of defensive capability, and that the relationships are different between the sexes.

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Dietary cardenolides enhance growth and change the direction of the fecundity‐longevity trade‐off in milkweed bugs (Heteroptera: Lygaeinae)

Abstract: This is an open access article under the terms of the Creat ive Commo ns Attri bution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 12 publications

References 96 publications

Functional evidence supports adaptive plant chemical defense along a geographical cline

Functional evidence supports adaptive plant chemical defense along a geographical cline

Condition dependence in biosynthesized chemical defenses of an aposematic and mimetic Heliconius butterfly

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

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