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My dissertation addresses two aspects of eukaryotic evolution, (1) the organization of eukaryotic diversity and (2) genomic variation in Foraminifera. The bulk of eukaryotic diversity is microbial with plants and animals representing just two of the estimated 75 lineages of eukaryotes. Among these microbial lineages, there are many examples of dynamic genome processes. Elucidating the origin and evolution of genome features requires a robust phylogenetic framework for eukaryotes. Taxon-rich molecular analyses provide a mechanism to test hypothesized evolutionary relationships and enable placement of diverse taxa on the tree of life. These analyses result in a well-resolved eukaryotic tree of life. Relaxed molecular clock analyses of this taxon-rich dataset place the origin on eukaryotes in the Paleoproterozoic, and suggest that all of the major lineages of eukaryotes diverged before the Neoproterozoic. This robust scaffold of the tree of eukaryotes is also used to elucidate common themes in genome evolution across eukaryotes. Mapping dynamic genome features onto this tree demonstrates that they are widespread in eukaryotes, and suggests that a common mechanism underlies genome plasticity. Foraminifera, a diverse lineage of marine amoebae, provide a good model system for investigating genome dynamics because they amplify portions of their genome and go through ploidy cycles during their life cycle. Assessment of nuclear dynamics in one species of Foraminifera, Allogromia laticollaris strain CSH, reveals that genome content varies according the life cycle stage and food source, which may differentially impact organismal fitness. The inclusion of diverse microbial eukaryotes enables better resolution of eukaryotic relationships and improves our understanding the dynamic nature of eukaryotic genomes.

Small bacterial genomes are believed to be evolutionarily derived from larger genomes through massive loss of genes and are usually associated with symbiotic or pathogenic lifestyles. It is therefore intriguing that a similar phenomenon of genome reduction has been reported within a group of free-living phototrophic marine cyanobacteria Prochlorococcus. Here I have investigated the roles of natural selection and mutation rate in the process of Prochlorococcus genome size reduction. Using a data set of complete cyanobacterial genomes including 12 Prochlorococcus and a sister group of 5 marine Synechococcus , I first reconstructed the steps leading to Prochlorococcus genome reduction in a phylogenetic context. The result reveals that small genome sizes within Prochlorococcus were largely determined by massive gene loss shortly after the split of Prochlorococcus and Synechococcus (a process we refer to as early genome reduction). A maximum likelihood approach was then used to estimate changes in both selection effect and mutation rate in the evolutionary history of Prochlorococcus. I also examined the effect of selection and functional importance of a subset of ancestor-derived genes those are lost in Prochlorococcus but are still retained in the genomes of its sister Synechococcus group. It appears that the effect of purifying selection was strongest when a large number of small effect genes were deleted from nearly all functional categories. And during this period, mutation rate also accelerated. Based on these results, I propose that shortly after Prochlorococcus diverged from its common ancestor with marine Synechococcus, its population size increased quickly and thus the efficacy of selection became very high. Due to limited nutrients and relatively constant environment, selection favored a streamlined genome for maximum economies in material and energy, causing subsequent reduction in genome size and possibly also contributing to the observed higher mutation rate.

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This work sequenced the placental microbiome of preterm and full-term pregnancies, and related preterm/full-term variations in placental microbiome composition and function to maternal inflammation in order to evaluate the proximate roles of the placental microbiome in responding to maternal immune stress and determining gestation length. These findings were situated in an evolutionary life history framework based on reproductive-immune trade-offs in order to develop an ultimate explanation for why natural selection has left us vulnerable to preterm birth, and why some populations are more affected than others. The preterm placental microbiome was found to be characterized by an inflammatory microbiome, dominated by bacteria that multiply in the context of energetic stress. The presence of such high numbers of these bacteria at the preterm placenta suggests that energetic and immune stresses are occurring in preterm birth, and that there may be a bidirectional relationship between stressful conditions and the microbiome. That is, inflammation or other stressors that contribute to energy imbalance may encourage shifts in the microbiome, which in turn creates more inflammation and energy imbalance. When that happens, pregnancy may become unsustainable before reaching term. Conversely, term pregnancies were characterized by greater numbers of beneficial, anti-inflammatory bacteria, hinting at possible roles for a healthy placental microbiome in nourishing and protecting the fetus. These findings underscore the need for a more holistic view of the role of microbes in pregnancy, as well as the need for health interventions that identify and address root sources of energetic and immune stress. / Anthropology