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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.