Biology subjects

Humphrey, P. T.

Publications and source records attributed to Humphrey, P. T..

6 recordsLinked to original sources

bioRxiv2025

Parallel but distinct adaptive routes in the budding and fission yeasts after 10,000 generations of experimental evolution

Quantitative genetics approaches designed to understand the evolution of traits have helped improve our understanding of the genetic basis of adaptation. However, they often overlook crucial aspects of adaptation, including the long-term temporal evolutionary dynamics, the predictability of evolutionary outcomes, the influence of past evolution on future evolutionary trajectories (contingency), and the diversity of molecular mechanisms underlying adaptation. Experimental evolution has been a useful tool for answering these questions, but extracting fundamental principles and predictive features of evolutionary outcomes from these datasets remains challenging due to the large number of covariates and confounding effects, such as differences in experimental setup, species lifestyle, gene content, and evolution rate. Here, we sought to circumvent these challenges by comparing distant yeast species that share several evolutionary features but differ mainly in evolutionary history and genome architecture, i.e. Saccharomyces cerevisiae and Schizosaccharomyces pombe. Thus, we evolved 10 populations of the fission yeast for 10,000 generations in the same conditions as a pre-existing budding yeast dataset (i.e. high-sugar media and hypoxic conditions), allowing us to observe repeatable evolutionary outcomes within species but diverse molecular mechanisms and targets of adaptation across species. The most frequent adapting route in these conditions involved upregulating fermentation genes and downregulating the glycolysis gene pyk1, which has not previously been observed in S. cerevisiae evolved populations or in wild Kluyveromyces lactis, but similar evolutionary paths have been observed in Schizosaccharomyces japonicus and in clinically relevant populations, such as some cancer cells. This suggests that parallelism is pervasive in the tree of life and that mechanisms of adaptation can be shared among closely related or distant species. Despite similar gene content and identical environments, recurrent adaptation across S. pombe populations involved different genes than in S. cerevisiae and was mostly detectable at the transcriptomic level. This suggests that trans-regulatory effects may play an important role in adaptation on short evolutionary timescales and that differences in evolutionary outcomes between these species may be attributed to contingency.

evolutionary biology↗

bioRxiv2025

Sex decreases the pleiotropic costs of local adaptation

Understanding the evolutionary mechanisms that maintain sex throughout nature despite its substantial direct costs is a longstanding challenge in biology. Previous work has shown that sexual recombination provides a key advantage in speeding adaptation, in part by separating beneficial mutations from deleterious hitchhikers. However, these earlier studies have focused on the effects of sex in a constant environment. Here, we show that recombination also provides a key advantage in fluctuating conditions, promoting the evolution of generalist phenotypes by reducing the pleiotropic costs of local adaptation. Using laboratory evolution in S. cerevisiae as a model system, we show that hitchhiking genetic load leads to pleiotropic costs and hence specialization in response to local adaptation in asexual but not in sexual lineages. This provides the first direct evidence that sex can be maintained over longer evolutionary timescales because it enables lineages to persist in the face of environmental change.

evolutionary biology↗

bioRxiv2023

Far From Home: Evolution of haploid and diploid populations reveals common, strong, and variable pleiotropic effects in non-home environments

Adaptation is driven by the selection for beneficial mutations that provide a fitness advantage in the specific environment in which a population is evolving. However, environments are rarely constant or predictable. When an organism well adapted to one environment finds itself in another, pleiotropic effects of mutations that made it well adapted to its former environment will affect its success. To better understand such pleiotropic effects, we evolved both haploid and diploid barcoded budding yeast populations in multiple environments, isolated adaptive clones, and then determined the fitness effects of adaptive mutations in "non-home" environments in which they were not selected. We find that pleiotropy is common, with most adaptive evolved lineages showing fitness effects in non-home environments. Consistent with other studies, we find that these pleiotropic effects are unpredictable: they are beneficial in some environments and deleterious in others. However, we do find that lineages with adaptive mutations in the same genes tend to show similar pleiotropic effects. We also find that ploidy influences the observed adaptive mutational spectra in a condition-specific fashion. In some conditions, haploids and diploids are selected with adaptive mutations in identical genes, while in others they accumulate mutations in almost completely disjoint sets of genes.

evolutionary biology↗

bioRxiv2020

Phenotypic and molecular evolution across 10,000 generations in laboratory budding yeast populations

Laboratory experimental evolution provides a window into the details of the evolutionary process. To investigate the consequences of long-term adaptation, we evolved 205 S. cerevisiae populations (124 haploid and 81 diploid) for [~]10,000 generations in three environments. We measured the dynamics of fitness changes over time, finding repeatable patterns of declining adaptability. Sequencing revealed that this phenotypic adaptation is coupled with a steady accumulation of mutations, widespread genetic parallelism, and historical contingency. In contrast to long-term evolution in E. coli, we do not observe long-term coexistence or populations with highly elevated mutation rates. We find that evolution in diploid populations involves both fixation of heterozygous mutations and frequent loss-of-heterozygosity events. Together, these results help distinguish aspects of evolutionary dynamics that are likely to be general features of adaptation across many systems from those that are specific to individual organisms and environmental conditions.

evolutionary biology↗

bioRxiv2020

Competitive hierarchies, antibiosis, and the distribution of bacterial life history traits in a microbiome

Microbiome manipulation requires an understanding of how species interact within communities. Can outcomes of ecological interactions be predicted from microbial life history traits, the identity of the species, or both? We addressed these questions by studying the competitive interaction network in a community of 40 endophytic Pseudomonas spp. bacterial isolates from a native plant. Pairwise competition experiments revealed competitive dominance of P. fluorescens over P. syringae strains within this microbiome-derived community. P. syringae strains with higher growth rates won more contests, while P. fluorescens strains with shorter lag times and lower growth rates won more contests. Adding to their competitive dominance, P. fluorescens strains often produced antibiotics to which few P. syringae strains were resistant. Many competitive outcomes among P. syringae strains were predicted to be reversed by P. fluorescens inhibitors because indirect benefits accrued to less competitive strains. P. fluorescens strains frequently changed competitive outcomes, suggesting a critical role of strains within this bacterial clade in structuring plant microbiome communities. Microbial traits also may provide a handle for directing the outcome of colonization processes within microbiomes.

ecology↗

bioRxiv2019

Insect herbivory reshapes a native leaf microbiome

Insect herbivory is pervasive in plant communities, but its impact on microbial plant colonizers is not well-studied in natural systems. By calibrating sequencing-based bacterial detection to absolute bacterial load, we find that the within-host abundance of most leaf microbiome (phyllosphere) taxa colonizing a native forb is amplified within leaves impacted by insect herbivory. Herbivore-associated bacterial amplification reflects community-wide compositional shifts towards lower ecological diversity, but the extent and direction of such compositional shifts can be interpreted only by quantifying absolute abundance. Experimentally eliciting anti-herbivore defenses reshaped within-host fitness ranks among Pseudomonas spp. field isolates and amplified a subset of putative P. syringae phytopathogens in a manner causally consistent with observed field-scale patterns. Herbivore damage was inversely correlated with plant reproductive success and was highly clustered across plants, which predicts tight co-clustering with putative phytopathogens across hosts. Insect herbivory may thus drive the epidemiology of plant-infecting bacteria as well as the structure of a native plant microbiome by generating variation in within-host bacterial fitness at multiple phylogenetic and spatial scales. This study emphasizes that \"non-focal\" biotic interactions between hosts and other organisms in their ecological settings can be crucial drivers of the population and community dynamics of host-associated microbiomes.

ecology↗