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ABSTRACT Shared polymorphisms, loci with identical alleles across species, are of unique interest in evolutionary biology as they may represent cases of selection maintaining ancient genetic variation post‐speciation, or contemporary selection promoting convergent evolution. In this study, we investigate the abundance of shared polymorphism between two members of theDaphnia pulexspecies complex. We test whether the presence of shared mutations is consistent with the action of balancing selection or alternative hypotheses such as hybridization, incomplete lineage sorting or convergent evolution. We analyzed over 2,000 genomes from six taxa in theD. pulexspecies group and examined the prevalence and distribution of shared alleles between the focal species pair, North American and EuropeanD. pulex. We show that North American and EuropeanD. pulexdiverged over 10 million years ago, yet retained tens of thousands of shared polymorphisms. We suggest that the number of shared polymorphisms between North American and EuropeanD. pulexcannot be fully explained by hybridization or incomplete lineage sorting alone. We show that most shared polymorphisms could be the product of convergent evolution, that a limited number appear to be old trans‐specific polymorphisms, and that balancing selection is affecting convergent and ancient mutations alike. Finally, we provide evidence that a blue wavelength opsin gene with trans‐specific polymorphisms has functional effects on behavior and fitness in the wild. 

Abstract The early evolution of eukaryotes and their adaptations to low-oxygen environments are fascinating open questions in biology. Genome-scale data from novel eukaryotes, and particularly from free-living lineages, are the key to answering these questions. The Parabasalia are a major group of anaerobic eukaryotes that form the most speciose lineage of Metamonada. The most well-studied are parasitic parabasalids, including Trichomonas vaginalis and Tritrichomonas foetus, but very little genome-scale data are available for free-living members of the group. Here, we sequenced the transcriptome of Pseudotrichomonas keilini, a free-living parabasalian. Comparative genomic analysis indicated that P. keilini possesses a metabolism and gene complement that are in many respects similar to its parasitic relative T. vaginalis and that in the time since their most recent common ancestor, it is the T. vaginalis lineage that has experienced more genomic change, likely due to the transition to a parasitic lifestyle. Features shared between P. keilini and T. vaginalis include a hydrogenosome (anaerobic mitochondrial homolog) that we predict to function much as in T. vaginalis and a complete glycolytic pathway that is likely to represent one of the primary means by which P. keilini obtains ATP. Phylogenomic analysis indicates that P. keilini branches within a clade of endobiotic parabasalids, consistent with the hypothesis that different parabasalid lineages evolved toward parasitic or free-living lifestyles from an endobiotic, anaerobic, or microaerophilic common ancestor.