Monarch butterflies infected with parasites capable of infecting their offspring avoid transmission by selectively laying their eggs on plants containing therapeutic remedies.

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The parasitic protozoan, Ophryocystis elektroscirrha, is known to infect monarch butterflies and produce extremely deleterious symptoms. Caterpillars ingest parasitic spores inadvertently scattered on leaves by their mothers during egg laying. After the parasite enters the body of the caterpillar, it reproduces rapidly and consumes a significant portion of the host’s nutrient intake. During pupation, the parasites produce millions of spores that cover the nascent wing scales of the developing adult butterfly. These spores are shaken off onto leaves during egg laying, thereby starting the cycle over again. Infected adults have not been observed self-medicating their own parasitic infection, but they preferentially lay their eggs on a specific species of milkweed (Asclepias curassavica) that contains compounds capable of fighting infection when consumed by their caterpillars. The anti-parasitic properties of A. curassavica are thought to be due to their special suite of cardenolides including several non-polar varieties that interfere with parasite ATPase enzymes.

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“‘[S]elf’-medication, through which animals use third species or compounds to prevent infection of or reduce parasite growth in their own bodies…individuals can also increase their fitness by mitigating disease in their relatives…’trans-generational medication’…In the case of herbivorous insects, oviposition choices of adults crucially affect larval fitness.” (Lefèvre et al. 2010:1485)

“[A]dults, infected with vertically transmitted parasites, can mitigate disease in their offspring by preferentially laying eggs on anti-parasitic host plants…Monarch butterflies are commonly infected with the protozoan parasite Ophryocystis elektroscirrhaO. elektroscirrha has strong detrimental effects on its host. Parasite infections occur when caterpillars ingest spores that are passively scattered onto eggs or host plant leaves by female adult butterflies during oviposition. Parasites penetrate the gut wall and undergo replication in the hypoderm. Upon host pupation, the parasite forms spores around the scales of the developing butterfly, and infected butterflies emerge covered with dormant spores on the outsides of their bodies…parasite reproduction was strongly reduced on Asclepias curassavica as compared to Asclepias incarnata, resulting in a strong alleviation of fitness loss…infected monarch larvae do not have the ability to preferentially consume anti-parasitic milkweed species; but (ii) infected adult female monarchs do preferentially lay their eggs on anti-parasitic milkweeds.” (Lefèvre et al. 2010:1485-1486)

“(1) infected monarchs show an oviposition preference for A. curassavica, whereas uninfected monarchs do not; (2) monarch larvae that feed on A. curassavica experience lower parasite burdens, and hence experience an alleviation of the fitness costs induced by the parasite; (3) these anti-parasitic benefits come at a cost with reduced longevity of uninfected caterpillars fed on A. curassavica; (4) the parasite does not benefit from reduced spore production…infected adult butterflies have no known way to cure themselves and are also not able to prevent the transmission of their parasites to their offspring. However, our results demonstrate that they can increase their inclusive fitness by laying their eggs on plants that will alleviate disease in their offspring…This medicating behaviour thereby resembles the maternal transfer of antibodies to offspring in mammals and birds…the fitness costs of parasite infection strongly outweigh any costs associated with locating preferred host plants…total cardenolide concentrations were much higher in A. curassavica than in A. incarnata. Moreover, A. curassavica plants contained many non-polar cardenolides, whose concentrations correlate with parasite spore load. Cardenolides usually act on Na+, K+-ATPases…Infection may induce changes in receptors involved in milkweed-seeking behaviour and preference, including the olfactory and contact chemoreceptor sensilla on the legs and antennae of the butterfly.” (Lefèvre et al. 2010:1491)

Journal article
Evidence for trans-generational medication in natureEcology LettersOctober 7, 2010
Thierry Lefèvre, Lindsay Oliver, Mark D. Hunter, Jacobus C. De Roode

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Living System/s

Organism
Tropical MilkweedAsclepias curassavicaSpecies

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