Biology subjects

Miller, S. F.

Publications and source records attributed to Miller, S. F..

5 recordsLinked to original sources

bioRxiv2026

Evolutionary Dynamics of Paramecium Mitochondrial Genomes

Ciliates are a diverse group of single-celled eukaryotes that can exhibit a wide range of genetic diversity within morphologically indistinguishable species. However, they are still not well studied as their mechanisms of speciation and the extent of diversification remain unknown. Mitochondrial genomes offer an effective framework for resolving species relationships and evolutionary changes. Here, we analyzed a globally sampled dataset of Paramecium to understand the evolution of mitochondrial genomes in ciliates. Phylogenetic analysis of linear mitochondrial genomes shows the presence of cryptic diversity beyond the P. aurelia complex, with P. bursaria lineage appearing as a deeply diverging out-group. Protein-coding genes are largely conserved, with limited rearrangements, and some ciliate-specific genes appear to be missing in P. bursaria. Population genetic analysis show little to no evidence of recombination along with substantial differences in effective population size across species. Patterns of molecular evolution also indicate purifying selection as the predominant force, the strength of which is at least as strong as in the nucleus and consistent with mitochondrial effective population sizes that are similar or larger than those of the nucleus. Across the functional groups, the electron transport chain and ribosomal genes are highly constrained, while ciliate-specific ymf genes show reduced efficacy of selection compared to the others. These findings offer a basis for connecting mitochondrial variation to evolutionary divergence, functional constraint, and speciation in microbial eukaryotes.

genomics↗

bioRxiv2026

Shifts in the population-genetic landscape of the ciliate genus Paramecium

Ciliates are one of the most ecologically diverse and morphologically intricate unicellular organisms. Despite their evolutionary significance and their prominence in cell-biological research, the population-genetic processes governing their diversification have received remarkably little attention. A fundamental unresolved problem is the existence of geographic isolation among free-living protists and its consequences for species richness. We addressed this issue in the model ciliate Paramecium by sequencing genomes of hundreds of isolates collected worldwide, capturing multiple morphological and cryptic species, with multiple populations each. Contrary to previous reports, we found evidence of geographic differentiation in the majority of species. In a few cases, geographic structure became evident when deeply diverging clades in a species were treated separately. This suggests that the biogeographical patterns of Paramecium have been shaped by periods of genetic isolation leading to speciation, with rare events of global dispersal realized over its long evolutionary history. Despite being largely isolated, populations were remarkably similar in their effective population size, recombination rate, and efficacy of natural selection. Across species, selection appears to be least effective in Paramecium aurelia lineages, and most effective in P. bursaria, presumably due to differences in their breeding characteristics. Despite differences among species in the population-genetic environment, patterns of variation across the genome remained consistent. Selective constraints on a core set of genes seemed to have gradually diverged across the species phylogeny. Genes with multiple copies retained from whole-genome duplication events in P. aurelia were found to be under relatively relaxed purifying selection. Moving forward, this dataset will serve to test hypotheses on the ecological and cellular complexity of Paramecium and beyond.

evolutionary biology↗

bioRxiv2023

Trade-offs, trade-ups, and high mutational parallelism underlie microbial adaptation to extreme feast/famine

Microbes are robust organisms capable of rapidly adapting to complex stress, enabling the colonization of harsh environments. In nature, microbes are regularly challenged by starvation, which is a particularly complex stress because resource limitation often co-occurs with changes in pH, osmolarity, and toxin accumulation created by metabolic waste. Often overlooked are the additional complications introduced by eventual resource replenishment as successful microbes must withstand rapid environmental shifts before swiftly capitalizing on replenished resources to avoid invasion by competing species. To understand how microbes navigate trade-offs between growth and survival, ultimately adapting to thrive in environments with extreme fluctuations, we experimentally evolved 16 Escherichia coli populations for 900 days to repeated feast/famine cycles of 100-day starvation before resource replenishment. Using longitudinal population-genomic analysis, we found that evolution in response to extreme feast/famine is characterized by narrow adaptive trajectories with high mutational parallelism and notable mutational order. Genetic reconstructions reveal that early mutations result in trade-offs for biofilm and motility but trade-ups for growth and survival, as these mutations conferred correlated advantages during both short-term and long-term culture. Our results demonstrate how microbes can navigate the adaptive landscapes of regularly fluctuating conditions and ultimately follow mutational trajectories that confer benefits across diverse environments.

evolutionary biology↗

bioRxiv2021

Evolutionary dynamics of asexual hypermutators adapting to a novel environment

How microbes adapt to a novel environment is a central question in evolutionary biology. While adaptive evolution must be fueled by beneficial mutations, whether higher mutation rates facilitate the rate of adaptive evolution remains unclear. To address this question, we cultured Escherichia coli hypermutating populations, in which a defective methyl-directed mismatch repair pathway causes a 140-fold increase in single-nucleotide mutation rates. In parallel with wild-type E. coli, populations were cultured in tubes containing Luria-Bertani broth, a complex medium known to promote the evolution of subpopulation structure. After 900 days of evolution, in three transfer schemes with different population-size bottlenecks, hypermutators always exhibited similar levels of improved fitness as controls. Fluctuation tests revealed that the mutation rates of hypermutator lines converged evolutionarily on those of wild-type populations, which may have contributed to the absence of fitness differences. Further genome-sequence analysis revealed that, although hypermutator populations have higher rates of genomic evolution, this largely reflects the effects of genetic draft under strong linkage. Despite these linkage effects, the evolved populations exhibit parallelism in fixed mutations, including those potentially related to biofilm formation, transcription regulation, and mutation-rate evolution. Together, these results generally negate the presumed relationship between high mutation rates and high adaptive speed of evolution, providing insight into how clonal adaptation occurs in novel environments. Significance statementWhile mutations are critical source for the adaptation in a new environment, whether or not the elevated mutation rates can empirically lead to the elevated adaptation rates remains unclear, especially when the environment is more heterogenous. To answer this question, we evolved E. coli populations with different starting mutation rates in a complex medium for 900 days and then examined their fitness and genome profiles. In the populations that have a higher starting mutation rate, despite faster genome evolution, their fitness improvement is not significantly faster. Our results reveal that the effect of elevated mutation rates is only very limited, and the mutations accumulated in hypermutators are largely due to linkage effect.

evolutionary biology↗

bioRxiv2019

Antagonism in Evolutionary Opportunities Results in Non-Monotonic Evolution Across an Environmental Gradient

Establishing reliable frameworks for predicting unknown outcomes from empirical observations is of great interest to ecologists and evolutionary biologists. Strong predictability in evolutionary responses has been previously demonstrated by the repeated observation of similar phenotypes or genotypes across multiple natural or experimental populations in analogous environments. However, the degree to which evolutionary outcomes can be predicted across environmental gradients, or in fluctuating environments, remains largely unexplored. Presumably, the phenotypic evolution in an intermediate environment could be interpolated from the evolved phenotypes observed in two extreme environments, but this assumption remains to be fully tested. Here, we report on the experimental evolution of Escherichia coli under three nutritional transfer periods: every day, every 10 days, and every 100 days, representing increasing severity in feast/famine cycles. After 900 days of experimental evolution, populations experiencing intermediate durations of starvation had evolved longer times to reach maximum growth rate, smaller colony sizes, higher biofilm formation, and higher mutation rates than populations evolving in the other environmental extremes. Because the intermediately starved populations exhibit significantly high molecular parallelism, these distinct phenotypes are likely due to non-monotonic deterministic forces instead of increased stochastic forces commonly associated with fluctuating environments. Our results demonstrate novel complexities associated with evolutionary predictability across environmental gradients and highlight the risk of using interpolation in evolutionary biology.

evolutionary biology↗