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Abstract In contrast to the typified view of genome cycling only between haploidy and diploidy, there is evidence from across the tree of life of genome dynamics that alter both copy number (i.e. ploidy) and chromosome complements. Here, we highlight examples of such processes, including endoreplication, aneuploidy, inheritance of extrachromosomal DNA, and chromatin extrusion. Synthesizing data on eukaryotic genome dynamics in diverse extant lineages suggests the possibility that such processes were present before the last eukaryotic common ancestor. While present in some prokaryotes, these features appear exaggerated in eukaryotes where they are regulated by eukaryote-specific innovations including the nucleus, complex cytoskeleton, and synaptonemal complex. Based on these observations, we propose a model by which genome conflict drove the transformation of genomes during eukaryogenesis: from the origin of eukaryotes (i.e. first eukaryotic common ancestor) through the evolution of last eukaryotic common ancestor. 

The evolution of lineage-specific gene families remains poorly studied across the eukaryotic tree of life, with most analyses focusing on the recent evolution ofde novogenes in model species. Here we explore the origins of lineage-specific genes in ciliates, a ~1 billion year old clade of microeukaryotes that are defined by their division of somatic and germline functions into distinct nuclei. Previous analyses on conserved gene families have shown the effect of ciliates’ unusual genome architecture on gene family evolution: extensive genome processing–the generation of thousands of gene-sized somatic chromosomes from canonical germline chromosomes–is associated with larger and more diverse gene families. To further study the relationship between ciliate genome architecture and gene family evolution, we analyzed lineage specific gene families from a set of 46 transcriptomes and 12 genomes representing x species from eight ciliate classes. We assess how the evolution lineage-specific gene families occurs among four groups of ciliates: extensive fragmenters with gene-size somatic chromosomes, non-extensive fragmenters with “large’’ multi-gene somatic chromosomes, Heterotrichea with highly polyploid somatic genomes and Karyorelictea with ‘paradiploid’ somatic genomes. Our analyses demonstrate that: 1) most lineage-specific gene families are found at shallow taxonomic scales; 2) extensive genome processing (i.e., gene unscrambling) during development likely influences the size and number of young lineage-specific gene families; and 3) the influence of somatic genome architecture on molecular evolution is increasingly apparent in older gene families. Altogether, these data highlight the influences of genome architecture on the evolution of lineage-specific gene families in eukaryotes. 

Abstract The enormous population sizes and wide biogeographical distribution of many microbial eukaryotes set the expectation of high levels of intraspecific genetic variation. However, studies investigating protist populations remain scarce, mostly due to limited ‘omics data. Instead, most genetics studies of microeukaryotes have thus far relied on single loci, which can be misleading and do not easily allow for detection of recombination, a hallmark of sexual reproduction. Here, we analyze >40 genes from 72 single-cell transcriptomes from two morphospecies—Hyalosphenia papilio and Hyalosphenia elegans—of testate amoebae (Arcellinida, Amoebozoa) to assess genetic diversity in samples collected over four years from New England bogs. We confirm the existence of cryptic species based on our multilocus dataset, which provides evidence of recombination within and high levels of divergence between the cryptic species. At the same time, total levels of genetic diversity within cryptic species are low, suggesting that these abundant organisms have small effective population sizes, perhaps due to extinction and repopulation events coupled with efficient modes of dispersal. This study is one of the first to investigate population genetics in uncultivable heterotrophic protists using transcriptomics data and contributes towards understanding cryptic species of nonmodel microeukaryotes.