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  1. Free, publicly-accessible full text available November 6, 2024
  2. Abstract

    Apicomplexa are ancient and diverse organisms which have been poorly characterized by modern genomics. To better understand the evolution and diversity of these single-celled eukaryotes, we sequenced the genome ofOphryocystis elektroscirrha, a parasite of monarch butterflies,Danaus plexippus. We contextualize our newly generated resources within apicomplexan genomics before answering longstanding questions specific to this host-parasite system. To start, the genome is miniscule, totaling only 9 million bases and containing fewer than 3,000 genes, half the gene content of two other sequenced invertebrate-infecting apicomplexans,Porospora giganteaandGregarina niphandrodes. We found thatO. elektroscirrhashares different orthologs with each sequenced relative, suggesting the true set of universally conserved apicomplexan genes is very small indeed. Next, we show that sequencing data from other potential host butterflies can be used to diagnose infection status as well as to study diversity of parasite sequences. We recovered a similarly sized parasite genome from another butterfly,Danaus chrysippus, that was highly diverged from theO. elektroscirrhareference, possibly representing a distinct species. Using these two new genomes, we investigated potential evolutionary response by parasites to toxic phytochemicals their hosts ingest and sequester. Monarch butterflies are well-known to tolerate toxic cardenolides thanks to changes in the sequence of their Type II ATPase sodium pumps. We show thatOphryocystiscompletely lacks Type II or Type 4 sodium pumps, and related proteins PMCA calcium pumps show extreme sequence divergence compared to other Apicomplexa, demonstrating new avenues of research opened by genome sequencing of non-model Apicomplexa.

     
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  3. Abstract

    Few studies have described the effects of larval diet quality on adult insect flight performance. Flight muscle development and high‐powered flight in insects are associated with costly energetic demands. Because larval diet is the energy source that powers these mechanisms, we asked whether larval diet has an impact on flight performance and metabolism in the monarch butterfly (Danaus plexippusLinnaeus).

    Monarch caterpillars from the eastern North American and Puerto Rican populations were fed a diet of eitherAsclepias incarnataL. (native to the eastern North American population) orAsclepias curassavicaL. (native to the Puerto Rican population and uncommon in eastern North America). We flew the monarchs on a tethered flight mill to acquire flight performance metrics including velocity, distance, duration, power, and oxygen consumption rate.

    Monarchs reared on theA. incarnata L. milkweed showed slower, shorter, and less powerful flights than those fed onA. curassavicaL. However, eastern North American and Puerto Rican monarchs, which were reared under summer conditions, did not differ in flight metrics or post‐flight metabolic rates.

    The results suggest that flight in eastern North American and Puerto Rican monarchs is similar during the breeding season, yet the milkweed the caterpillars consume has important implications for flight performance.

     
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  4. null (Ed.)
  5. Abstract

    Insect–pathogen dynamics can show seasonal and inter‐annual variations that covary with fluctuations in insect abundance and climate. Long‐term analyses are especially needed to track parasite dynamics in migratory insects, in part because their vast habitat ranges and high mobility might dampen local effects of density and climate on infection prevalence.

    Monarch butterfliesDanaus plexippusare commonly infected with the protozoanOphryocystis elektroscirrha(OE). Because this parasite lowers monarch survival and flight performance, and because migratory monarchs have experienced declines in recent decades, it is important to understand the patterns and drivers of infection.

    Here we compiled data onOEinfection spanning 50 years, from wild monarchs sampled in the United States, Canada and Mexico during summer breeding, fall migrating and overwintering periods. We examined eastern versus western North American monarchs separately, to ask how abundance estimates, resource availability, climate and breeding season length impact infection trends. We further assessed the intensity of migratory culling, which occurs when infected individuals are removed from the population during migration.

    Average infection prevalence was four times higher in western compared to eastern subpopulations. In eastern North America, the proportion of infected monarchs increased threefold since the mid‐2000s. In the western region, the proportion of infected monarchs declined sharply from 2000 to 2015, and increased thereafter. For both eastern and western subpopulations, years with greater summer adult abundance predicted greater infection prevalence, indicating that transmission increases with host breeding density. Environmental variables (temperature and NDVI) were not associated with changes in the proportion of infected adults. We found evidence for migratory culling of infected butterflies, based on declines in parasitism during fall migration. We estimated that tens of millions fewer monarchs reach overwintering sites in Mexico as a result ofOE, highlighting the need to consider the parasite as a potential threat to the monarch population.

    Increases in infection among eastern North American monarchs post‐2002 suggest that changes to the host’s ecology or environment have intensified parasite transmission. Further work is needed to examine the degree to which human practices, such as mass caterpillar rearing and the widespread planting of exotic milkweed, have contributed to this trend.

     
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  6. null (Ed.)
    A core hypothesis in coevolutionary theory proposes that parasites adapt to specifically infect common host genotypes. Under this hypothesis, parasites function as agents of negative frequency-dependent selection, favouring rare host genotypes. This parasite-mediated advantage of rarity is key to the idea that parasites maintain genetic variation and select for outcrossing in host populations. Here, we report the results of an experimental test of parasite adaptation to common versus rare host genotypes. We selected the bacterial parasite Serratia marcescens to kill Caenorhabdiis elegans hosts in uneven mixtures of host genotypes. To examine the effect of commonness itself, independent of host identity, each of four host genotypes was represented as common or rare in experimental host mixtures. After experimental selection, we evaluated a parasite line's change in virulence—the selected fitness trait—on its rare and common host genotypes. Our results were consistent with a slight advantage for rare host genotypes: on average, parasites lost virulence against rare genotypes but not against common genotypes. The response varied substantially, however, with distinct patterns across host genotype mixtures. These findings support the potential for parasites to impose negative frequency-dependent selection, while emphasizing that the cost of being common may vary with host genotype. 
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