Biology subjects

Scott, T. J.

Publications and source records attributed to Scott, T. J..

10 recordsLinked to original sources

bioRxiv2026

Changing abiotic and biotic environments affect the genetics of adaptation and speciation

Abiotic and biotic environments can change in different ways that affect how populations adapt, diverge, and speciate. However, many models of speciation only examine adaptation to constant environments. We used Fishers geometric model to study adaptation and speciation in different types of changing abiotic and biotic environments. We hypothesized that, when the magnitude of environmental change is equal, fitness would be lowered more by consistently directional abiotic change and by consistently antagonistic biotic conflict. As a result, directional changes and biotic conflict would cause a greater evolutionary response through fixation of adaptive mutations, greater divergence between populations, and lower migrant or hybrid fitnesses (higher speciation potential). Increasing the directionality of abiotic change did indeed have all these effects. However, populations evolving with conflict, despite showing the expected arms-race elevation of deleterious change and evolutionary response, did not result in decreased fitness of migrants and hybrids. Two factors seem to be involved. In tug-of-war conflict, high total phenotypic change does not lead to high phenotypic divergence because the phenotypic change churns around in the same general area of trait space. With victim-exploiter (trait matching) conflict, hybrids and migrants were frequently more fit than those with other kinds of change because of escape from locally adapted antagonists. In this case, foreign genes sometimes allowed populations in conflict to generate useful variation. These results show that different kinds of ecological change can affect adaptation and the formation of new species in distinct ways and that local divergence and incompatibility do not always go hand in hand. Significance StatementAdaptation and speciation are key processes in evolution. During the process of adapting, populations genetically diverge from each other and can become incompatible, leading to new species. The tendency for populations to diverge can be different in changing environments. Changes in the environment can consist of changes in the non-living parts like temperature or elevation (the abiotic environment) or changes in the species that a population interacts with (the biotic environment). Abiotic and biotic environments are thought to change in different ways because biotic environments are evolving but abiotic ones are not. In particular, antagonistic biotic evolution can lead to arms races. We modeled how abiotic change and biotic changes from antagonistic or mutualistic interactions affect adaptation and speciation. We found that, as expected, antagonistic biotic changes led to a large amount of evolutionary divergence but surprisingly this did not lead to correspondingly large reduction in migrant or hybrid fitness. In a tug-of- war antagonistic model, this was due evolutionary churn - high change did not lead to high divergence. In a victim-exploiter (trait matching) model, migrants and hybrids between diverging populations were often better off because antagonisms were broken up. As a result of migrants and hybrids having higher fitness, antagonistic biotic interactions may result in less speciation than expected from their evolutionary arm-races.

evolutionary biology↗

bioRxiv2026

Evolution of a core ribosomal innovation in octopus

Much of biology focuses on how genetic changes mediate new functions, but less attention is given to adaptations in other steps of the central dogma. Octopuses exhibit complex nervous systems and sophisticated behaviors that rival vertebrates, but via an entirely divergent evolutionary history. Here, we serendipitously discovered that octopus ribosomes contain a structural break in the core ribosomal RNA that is unique among all animals. This break site enhances translation fidelity to reduce miscoding and subsequent protein aggregation, even when engineered into evolutionarily distant bacterial ribosomes. Furthermore, high fidelity translation by octopus ribosomes supports proteomic stability during extensive RNA editing observed in cephalopods, suggesting synergy between distinct non-canonical modes of gene regulation. This adaptation emerged in recently derived octopuses with expanded nervous systems, thereby revealing a mechanism that could broadly support the evolution of novel organismal traits.

biochemistry↗

bioRxiv2024

Temporally discordant chromatin accessibility and DNA demethylation define short and long-term enhancer regulation during cell fate specification

Epigenetic mechanisms govern the transcriptional activity of lineage-specifying enhancers; but recent work challenges the dogma that joint chromatin accessibility and DNA demethylation are prerequisites for transcription. To understand this paradox, we established a highly-resolved timeline of DNA demethylation, chromatin accessibility, and transcription factor occupancy during neural progenitor cell differentiation. We show thousands of enhancers undergo rapid, transient accessibility changes associated with distinct periods of transcription factor expression. However, most DNA methylation changes are unidirectional and delayed relative to chromatin dynamics, creating transiently discordant epigenetic states. Genome-wide detection of 5-hydroxymethylcytosine further revealed active demethylation begins ahead of chromatin and transcription factor activity, while enhancer hypomethylation persists long after these activities have dissipated. We demonstrate that these timepoint specific methylation states predict past, present and future chromatin accessibility using machine learning models. Thus, chromatin and DNA methylation collaborate on different timescales to mediate short and long-term enhancer regulation during cell fate specification.

genomics↗

bioRxiv2024

Non-selected incompatibilities and their effects on aggregative multicellularity in the social amoeba Dictyostelium discoideum

Multicellular organisms that form by aggregation of cells arguably do not achieve high levels of complexity. Conflict among the cells is a widely accepted explanation for this, but an alternative hypothesis is that mixing cells of different genotypes leads to failures of coordination, which we call the coordination hypothesis. We empirically tested the coordination hypothesis in the social amoeba Dictyostelium discoideum. We mixed D. discoideum clones that had evolved in isolation for generations and accumulated mutations that have not been tested against each other by selection. To quantify the effect of incompatibilities, we measured performance in terms of the developmental traits of slug migration and spore production. Importantly, kin recognition incompatibilities were avoided by mixing lines evolved from the same ancestor under conditions that would not select for the evolution of de novo recognition. Our results show no evidence of incompatibilities in coordinated movement of slugs towards light in the social amoeba. Spore production was higher than expected in mixtures, in apparent contradiction to the coordination hypothesis. However, we found support for coordination incompatibilities in an interaction between migration and spore production: in mixtures, fewer cells succeeded at migrating and becoming spores.

evolutionary biology↗

bioRxiv2023

Unpredictable soil conditions affect the prevalence of a microbial symbiosis

The evolution of symbiotic interactions may be affected by unpredictable conditions. However, a link between prevalence of symbiosis and these conditions has not been widely demonstrated. We test for these associations using Dictyostelium discoideum social amoebae and their bacterial symbionts. D. discoideum are host to endosymbiotic bacteria from three taxa: Paraburkholderia, Amoebophilus and Chlamydiae. Three species of facultative Paraburkholderia symbionts are the best studied and give hosts the ability to carry food bacteria through the dispersal stage to new environments. Amoebophilus and Chlamydiae are obligate endosymbionts with no measurable impact on host fitness. We test whether the frequency of both single infections and coinfections of these symbionts are associated with the unpredictability of their soil environments by using symbiont presence-absence data from soil isolates from 21 locations across the eastern United States. We find that that Amoebophilus and Chlamydiae obligate endosymbionts and coinfections are not associated with any of our mean measures, but that unpredictable precipitation can promote or hinder symbiosis depending on the species of Paraburkholderia symbiont.

evolutionary biology↗

bioRxiv2023

Symbiotic bacteria, immune-like sentinel cells, and the response to pathogens in a social amoeba

Some endosymbionts living within a host must modulate their hosts immune systems in order to infect and persist. We studied the effect of a bacterial endosymbiont on a facultatively multicellular social amoeba host. Aggregates of the amoeba Dictyostelium discoideum contain a subpopulation of sentinel cells that function akin to the immune systems of more conventional multicellular organisms. Sentinel cells sequester and discard toxins from D. discoideum aggregates and may play a central role in defense against pathogens. We measured the number and functionality of sentinel cells in aggregates of D. discoideum infected by bacterial endosymbionts in the genus Paraburkholderia. Infected D. discoideum produced fewer and less functional sentinel cells, suggesting that Paraburkholderia may interfere with its hosts immune system. Despite impaired sentinel cells, however, infected D. discoideum were less sensitive to ethidium bromide toxicity, suggesting that Paraburkholderia may also have a protective effect on its host. By contrast, D. discoideum infected by Paraburkholderia did not show differences in their sensitivity to two non-symbiotic pathogens. Our results expand previous work on yet another aspect of the complicated relationship between D. discoideum and Paraburkholderia, which has considerable potential as a model for the study of symbiosis.

ecology↗

bioRxiv2022

Cross-tissue patterns of DNA hypomethylation reveal genetically distinct histories of cell development

Establishment of DNA methylation (DNAme) patterns is essential for balanced multi-lineage cellular differentiation, but exactly how these patterns drive cellular phenotypes is unclear. While >80% of CpG sites are stably methylated, tens of thousands of discrete CpG loci form hypomethylated regions (HMRs). Because they lack DNAme, HMRs are considered transcriptionally permissive, but not all HMRs actively regulate genes. Unlike promoter HMRs, a subset of non-coding HMRs is cell-type specific and enriched for tissue specific gene regulatory functions. Our data further argues not only that HMR establishment is an important step in enforcing cell identity, but also that complex HMR patterns are functionally instructive to gene regulation. To understand the significance of non-coding HMRs, we systematically dissected HMR patterns across diverse human cell types and developmental timepoints, including embryonic, fetal, and adult tissues. Unsupervised clustering of 102,390 distinct HMRs revealed that levels of HMR specificity reflects a developmental hierarchy supported by enrichment of stage-specific transcription factors and gene ontologies. Using a pseudo-time course of development from embryonic stem cells to adult stem and mature hematopoietic cells, we find that most HMRs observed in differentiated cells (~70-75%) are established at early developmental stages and accumulate as development progresses. HMRs that arise during differentiation frequently (~35%) establish near existing HMRs ([≤] 6kb away), leading to the formation of HMR clusters associated with stronger enhancer activity. Using SNP-based partitioned heritability from GWAS summary statistics across diverse traits and clinical lab values, we discovered that genetic contribution to trait heritability is enriched within HMRs. Moreover, the contribution of heritability to cell-relevant traits increases with both increasing developmental specificity and HMR clustering, supporting the role of distinct HMR subsets in regulating normal cell function. Altogether, our findings reveal that HMRs can predict cellular phenotypes by providing genetically distinct historical records of a cells journey through development. AUTHOR SUMMARYStudies aiming to understand the relationship between DNA methylation patterns and phenotypic outcomes have focused largely on individual differentially methylated regions without consideration of combinatorial changes that drive phenotypes. In non-disease contexts, most of the human genome is stably methylated, except for thousands of discrete DNA hypomethylated regions (HMRs) coinciding with gene regulatory elements. Here, we comprehensively characterize HMR relationships both within and between developmentally diverse cell types to understand the functional significance of complex HMR patterns. We show that levels of HMR specificity across cell-types captures time-point specific branchpoints of development. Our analysis further reveals that HMRs form clusters in proximity to cell identity genes and are associated with stronger gene enhancer activity. This is a wide-spread phenomenon and only a very small subset of HMR clusters is explained by overlapping super-enhancer annotations. Partitioned heritability revealed the functional significance of different HMR patterns linked to specific phenotypic outcomes and indicates a quantitative relationship between HMR patterns and complex trait heritability. Altogether, our findings reveal that HMRs can predict cellular phenotypes by providing genetically distinct historical records of a cells journey through development, ultimately providing novel insights into how DNA hypo-methylation mediates genome function.

genomics↗

bioRxiv2022

Third-party effects in the Dictyostelium-Paraburkholderia symbiosis: food bacteria that are eaten, carried, or left behind

AbstractSymbiotic interactions may change depending on the abundance of third parties like predators, prey, or pathogens. Third-party interactions with prey bacteria are central to the symbiosis between Dictyostelium discoideum social amoeba hosts and Paraburkholderia facultative bacterial symbionts. Symbiosis with inedible Paraburkholderia allows host D. discoideum to carry prey bacteria through the dispersal stage where host amoebae aggregate and develop into fruiting bodies that disperse spores. Carrying prey bacteria benefits hosts when prey bacteria are scarce but harms hosts when prey bacteria are plentiful. Symbiont-carrying hosts leave some bacteria behind; this could explain the harm to hosts if left-behind bacteria include uneaten prey bacteria. Thus, understanding both benefits and costs in this symbiosis requires measuring how many prey bacteria are eaten, carried, and left behind by infected hosts. We found that Paraburkholderia infection makes hosts leave behind both symbionts and prey bacteria. However, the number of prey bacteria left uneaten was small and did not explain why infected hosts produced fewer spores than uninfected hosts. Turning to the bacteria that are carried, we found that hosts carry more prey bacteria after developing in prey- poor environments than in prey-rich ones. This suggests that carriage is actively modified to ensure hosts have prey in the harshest conditions. Our results show that multifaceted interactions with third parties shape the evolution of symbioses in complex ways.

evolutionary biology↗

bioRxiv2022

Cooperation genes are more pleiotropic than private genes in the bacterium Pseudomonas aeruginosa

Pleiotropy may affect the evolution of cooperation by limiting cheater mutants if such mutants also lose other important traits. Because pleiotropy limits cheaters, selection may favor cooperation genes that are more pleiotropic. However, the same should not be true for private genes with functions unrelated to cooperation. Pleiotropy in cooperative genes has mostly been studied with single genes and has not been measured on a wide scale or compared to a suitable set of control genes with private functions. I remedy this gap by comparing genomic measures of pleiotropy in previously identified cooperative and private gene sets in Pseudomonas aeruginosa. I found that cooperative genes in P. aeruginosa tended to be more pleiotropic than private genes according to the number of protein-protein interactions, the number of gene ontology terms, and gene expression specificity. These results show that pleiotropy may be a general way to limit cheating and that cooperation may shape pleiotropy in the genome.

evolutionary biology↗

bioRxiv2021

Context, competition, and symbiont-induced bet-hedging between Dictyostelium discoideum and Paraburkholderia

Symbiotic interactions change with environmental context. Measuring these context-dependent effects in hosts and symbionts is critical to determining the nature of symbiotic interactions. We investigated context-dependence in the symbiosis between social amoeba hosts and their inedible Paraburkholderia bacterial symbionts, where the context is the abundance of host food bacteria. Paraburkholderia have been shown to harm hosts dispersed to food-rich environments, but aid hosts dispersed to food-poor environments by allowing hosts to carry food bacteria. Through measuring symbiont density and host spore production, we show that this food context matters in three other ways. First, it matters for symbionts, who suffer a greater cost from competition with food bacteria in the food-rich context. Second, it matters for host-symbiont conflict, changing how symbiont density negatively impacts host spore production. Third, data-based simulations show that symbiosis often provides a long-term fitness advantage for hosts after rounds of growth and dispersal in variable food-contexts, especially when conditions are harsh with little food. These results show how food context can have many consequences for the Dictyostelium-Paraburkholderia symbiosis and that both sides can frequently benefit. Impact StatementMany organisms form symbiotic relationships with other species. These symbioses often exhibit context-dependence, where the sign or magnitude of one partners effect on the other will change in different environments. Context-dependent effects make it difficult to assign interactions to categories like mutualisms or antagonisms because they involve both benefits and costs depending on the environment. However, in some cases, accounting for context-dependence can clarify an interaction so that it more easily fits a mutualism or antagonism. We investigated context-dependence using the symbiosis between Dictyostelium discoideum and two symbiotic Paraburkholderia species. In this symbiosis, Paraburkholderia bacteria allow hosts to carry food bacteria to food-poor contexts, where hosts rarely survive without food, but reduce host fitness in the more hospitable food-rich contexts. The effect of food context on Paraburkholderia symbionts is unknown. We show that Paraburkholderia symbionts are also affected by this context, through facing reduced competition after being dispersed by hosts to food-poor contexts. We also identify a new way that symbionts affect hosts, where symbiont density reduces host fitness, but less so in food-poor contexts. Finally, we use simulations to show that infected hosts benefit in the long-term across variable food contexts, especially in the harshest environments with little food. These results show that context-dependence in symbiosis can have many consequences for hosts and symbionts, though in general for D. discoideum and Paraburkholderia, both are likely to benefit.

ecology↗