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Abstract Diet profoundly influences the composition of an animal’s microbiome, especially in holometabolous insects, offering a valuable model to explore the impact of diet on gut microbiome dynamics throughout metamorphosis. Here, we use monarch butterflies (Danaus plexippus), specialist herbivores that feed as larvae on many species of chemically well-defined milkweed plants (Asclepias sp.), to investigate the impacts of development and diet on the composition of the gut microbial community. While a few microbial taxa are conserved across life stages of monarchs, the microbiome appears to be highly dynamic throughout the life cycle. Microbial diversity gradually diminishes throughout the larval instars, ultimately reaching its lowest point during the pupal stage and then recovering again in the adult stage. The microbial composition then undergoes a substantial shift upon the transition from pupa to adult, with female adults having significantly different microbial communities than the eggs that they lay, indicating limited evidence for vertical transmission of gut microbiota. While diet did not significantly impact overall microbial composition, our results suggest that fourth instar larvae exhibit higher microbial diversity when consuming milkweed with high concentrations of toxic cardenolide phytochemicals. This study underscores how diet and developmental stage collectively shape the monarch’s gut microbiota. 

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. 

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.