Biology subjects

Barraclough, T. G.

Publications and source records attributed to Barraclough, T. G..

13 recordsLinked to original sources

bioRxiv2025

Detecting and quantifying rare sex in natural populations

The distinction between sexual and asexual reproduction is fundamental to eukaryotic evolution. Testing theories about the evolution of reproductive modes first requires knowing whether sex is present or absent in a population. While this seems straightforward, the literature on asexuality reflects a history of shifting claims and uncertainty regarding reproductive mode, especially where sex is potentially rare or cryptic. Here, we develop a new framework to address the challenges in detecting and quantifying sexual reproduction from population genomic data. We first show that commonly calculated population genetic statistics do not reliably distinguish sexual and obligate asexual scenarios if asexuality is accompanied by sex-independent homologous recombination, as emerging evidence indicates is often the case. We then present a new method to quantify the relationship between evolutionary trees and mode of reproduction by classifying local trees for pairs of diploid individuals using ancestral recombination graphs (ARGs). This approach accurately discriminates signatures of genetic exchange and homologous recombination, though some uncertainty remains because of unavoidable biases in the steps needed to reconstruct trees from genome data. We introduce new statistics and simulation models to account for common reconstruction biases and demonstrate their utility by uncovering contrasting reproductive histories in the facultatively sexual budding yeast Saccharomyces cerevisiae. This approach offers the potential for improved quantitative inference of reproductive modes that can readily be extended to a broad range of eukaryotes. Significance StatementDetermining how often, if at all, organisms have sex has implications across biology. Studies often use population genomic data to interrogate the private life of putative asexuals, but the results prove surprisingly inconclusive. We develop a framework to address the challenges in detecting and quantifying rates of sex. New simulation models show how sex-independent recombination, which occurs widely across a range of asexual eukaryotes, causes genetic patterns to resemble sexual populations even when sex is absent. An approach based on ancestral recombination graphs (ARGs) and classification of local trees accounts for these problems and quantifies the remaining uncertainty due to inevitable reconstruction biases. Our framework will enable improved inferences of reproductive mode across a wide range of eukaryotes.

evolutionary biology↗

bioRxiv2024

Changes in flexibility but not in compactness underlie the thermal adaptation of prokaryotic adenylate kinases

Understanding the structural changes that enable enzymes to remain active in extreme thermal conditions is of broad scientific interest for both fundamental and applied biological research. Three key mechanisms that underlie the thermal adaptation of enzymes are modifications in structural flexibility, compactness, and the contacts formed among amino acids. However, most previous studies on these topics have been limited to small sample sizes or a narrow taxonomic focus, and the importance of these factors to thermal adaptation remains poorly understood. In this study, we combined molecular dynamics simulations and phylogenetic comparative analyses to thoroughly analyse the structural factors underlying thermal adaptation in adenylate kinase--a key enzyme involved in cellular energy balance and homeostasis--across 70 prokaryotic species. We detect systematic increases in the flexibility of the enzyme with temperature, both across and within species. In contrast, structural compactness appears to be almost completely independent of temperature. Finally, we uncover a remarkable diversity in the number and types of amino acid contacts observed in different adenylate kinases that cannot be explained solely by temperature. Our results suggest that there are multiple paths toward the adaptation of prokaryotic adenylate kinases to extreme thermal environments and that these paths are generally accessible through changes in flexibility. Lay summaryThe structure of a given enzyme can vary considerably among species, reflecting local environmental conditions to an extent. To this day, we do not have a clear picture of the impacts of the thermal environment on enzyme structure. To fill this gap, we performed a structural comparison of the enzyme adenylate kinase (ADK) from 70 species of bacteria and archaea. We find that rises in temperature tend to increase the flexibility of the enzyme. However, at any given temperature, ADKs from cold environments tend to be more flexible than those from hot environments. In contrast, the compactness of the enzyme did not vary consistently with temperature. Finally, we found that the pattern of amino acid contacts can vary dramatically across ADKs of different species, in a manner that cannot be predicted by temperature alone. Overall, our study shows that there are multiple ways to evolve an enzyme structure that can tolerate extreme temperatures, with a key constraint being maintaining sufficient flexibility at temperatures typically experienced by each species.

evolutionary biology↗

bioRxiv2023

Horizontal transfers between fungal Fusarium species contributed to successive outbreaks of coffee wilt disease

Outbreaks of fungal disease have devastated plants and animals throughout history. Over the past century, the repeated emergence of coffee wilt disease caused by the fungal pathogen Fusarium xylarioides severely impacted coffee production across sub-Saharan Africa. To improve the disease management of such pathogens, it is crucial to understand their genetic structure and evolutionary potential. We compared the genomes of 13 historic strains spanning six decades and multiple disease outbreaks to investigate population structure and host specialisation. We found F. xylarioides comprises at least four distinct lineages: one host-specific to Coffea arabica, one to C. canephora var. robusta, and two historic lineages isolated from various Coffea species. Mapping variation onto a new long-read reference genome showed that host-specificity appears to be acquired through horizontal transfer of effector genes from members of the F. oxysporum species complex. This species complex is known to cause wilt disease in over 100 plant species. Multiple transfers into the F. xylarioides populations matched to different parts of the F. oxysporum mobile pathogenicity chromosome and were enriched in effector genes and transposons. Effector genes in this region and other horizontally transferred carbohydrate-active enzymes important in the breakdown of plant cell walls were shown by transcriptomics to be highly expressed during infection of C. arabica by the fungal arabica strains. Widespread sharing of specific transposons between F. xylarioides and F. oxysporum, and the presence of large Starship elements, indicate that transposons were involved in horizontal transfers. Our results support the hypothesis that horizontal gene transfers contributed to the repeated emergence of this fungal disease.

evolutionary biology↗

bioRxiv2022

Public goods exploitation is reduced in species-rich microbial communities

Intraspecific public goods are commonly shared within microbial populations, where the benefits of public goods are largely limited to closely related conspecifics. One example is the production of iron-scavenging siderophores that deliver iron to cells via specific cell envelope receptor and transport systems. Intraspecific social exploitation of siderophore producers is common, since non-producers avoid the costs of production but retain the cell envelope machinery for siderophore uptake. However, little is known about how interactions between species (i.e. interspecific interactions) can shape intraspecific public goods exploitation. Here, we predicted that strong competition for iron between species in diverse communities will increase costs of siderophore cooperation, and hence select for increased intraspecific exploitation. We examined how increasing microbial community species diversity shapes intraspecific social dynamics by monitoring the growth of siderophore producers and non-producers of the plant-growth promoting bacterium Pseudomonas fluorescens, embedded within tree-hole microbial communities ranging from 2-15 species. We find, contrary to our prediction, that siderophore exploitation is reduced in high diversity communities, driven by increased likelihood of encountering key species that reduce the growth of siderophore non-producing (but not producing) strains of P. fluorescens. Our results suggest that maintaining a healthy soil microbiota could contribute to the maintenance of siderophore production in natural communities.

microbiology↗

bioRxiv2021

Bdelloid rotifers use hundreds of horizontally acquired genes against fungal pathogens

Obligately asexual lineages are typically rare and short-lived. According to one hypothesis, they adapt too slowly to withstand relentlessly coevolving pathogens. Bdelloid rotifers seem to have avoided this fate, by enduring millions of years without males or sex. We investigated whether bdelloids unusual capacity to acquire non-metazoan genes horizontally has enhanced their resistance to pathogens. We found that horizontally transferred genes are three times more likely than native genes to be upregulated in response to a natural fungal pathogen. This enrichment was twofold stronger than that elicited by a physical stressor (desiccation), and the genes showed little overlap. Among hundreds of upregulated non-metazoan genes were RNA ligases putatively involved in resisting fungal toxins and glucanases predicted to bind to fungal cell walls, acquired from bacteria. Our results provide evidence that bdelloids mitigate a predicted challenge of long-term asexuality in part through their ability to acquire and deploy so many foreign genes.

evolutionary biology↗

bioRxiv2021

CRISPRs are associated with bacterial expansion in the human gut during the first year of life

The dynamics of the gut microbiome in infancy have a profound impact on health in adulthood, but the ecological mechanism underlying the dynamics between bacteria and bacteriophages remains poorly understood. CRISPR is a bacterial adaptive immune system to resist bacteriophages; however, the role they play in the dynamics in infants gut microbiota is unknown. In this work, using large-scale metagenomic sequencing data from 82 Sweden infants gut microbiomes, 1882 candidate CRISPRs were identified and their dynamics were analyzed. The results showed CRISPRs were distributed in dominant bacteria and could target distinct bacteriophages at different time points with largely alternated spacers. In the putative identical CRISPRs, we found the CRISPRs could acquire new spacers and loss old spacers during the first year. In addition, it is the first time to report that gender was a major factor to determine the bacterial richness and the number of CRISPRs and host range of bacteriophages was narrow in silico. Therefore, we concluded that CRISPRs were associated with bacterial expansion. This work improves the understanding of the ecological mechanism behind dynamics in the early life of the human gut and substantially expands the repertoire of predicted CRISPRs providing a resource to study the function of bacterial unknown genes and to enhance the performance of these beneficial bacteria by CRISPR gene-editing technology.

microbiology↗

bioRxiv2020

Higher temperatures worsen the effects of mutations on protein stability

Understanding whether and how temperature increases alter the effects of mutations on protein stability is crucial for understanding the limits to thermal adaptation by organisms. Currently, it is generally assumed that the stability effects of mutations are independent of temperature. Yet, mutations should become increasingly destabilizing as temperature rises due to the increase in the energy of atoms. Here, by performing an extensive computational analysis on the essential enzyme adenylate kinase in prokaryotes, we show, for the first time, that mutations become more destabilizing with temperature both across and within species. Consistent with these findings, we find that substitution rates of prokaryotes decrease nonlinearly with temperature. Our results suggest that life on Earth likely originated in a moderately thermophilic and thermally fluctuating environment, and indicate that global warming should decrease the per-generation rate of molecular evolution of prokaryotes.

evolutionary biology↗

bioRxiv2020

Evolutionary dynamics of transposable elements in bdelloid rotifers

Transposable elements (TEs) are selfish genomic parasites whose ability to spread autonomously is facilitated by sexual reproduction in their hosts. If hosts become obligately asexual, TE frequencies and dynamics are predicted to change dramatically, but the long-term outcome is unclear. Here, we test current theory using whole-genome sequence data from eight species of bdelloid rotifers, a class of invertebrates where males are thus far unknown. Contrary to expectations, we find a diverse range of active TEs in bdelloid genomes, at an overall frequency within the range seen in sexual species. We find no evidence that TEs are spread by cryptic recombination or restrained by unusual DNA repair mechanisms, but we report that bdelloids share a large and unusual expansion of genes involved in RNAi-mediated TE suppression. This suggests that enhanced cellular defence mechanisms might mitigate the deleterious effects of active TEs and compensate for the consequences of long-term asexuality.

evolutionary biology↗

bioRxiv2019

Introgression in Brownea suggests that reticulate evolution contributes to Amazonian tree diversity

Hybridization has the potential to generate or homogenize biodiversity and is a particularly common phenomenon in plants, with an estimated 25% of species undergoing inter-specific gene flow. However, hybridization in Amazonias megadiverse tree flora was assumed to be extremely rare despite extensive sympatry between closely related species, and its role in diversification remains enigmatic because it has not yet been examined empirically. Using members of a dominant Amazonian tree family (Brownea, Fabaceae) as a model to address this knowledge gap, our study recovered extensive evidence of hybridization among multiple lineages across phylogenetic scales. More specifically, our results uncovered several historical introgression events between Brownea lineages and indicated that gene tree incongruence in Brownea is best explained by introgression, rather than solely by incomplete lineage sorting. Furthermore, investigation of recent hybridization using [~]19,000 ddRAD loci recovered a high degree of shared variation between two Brownea species which co-occur in the Ecuadorian Amazon. Our analyses also showed that these sympatric lineages exhibit homogeneous rates of introgression among loci relative to the genome-wide average, implying a lack of selection against hybrid genotypes and a persistence of hybridization over time. Our results demonstrate that gene flow between multiple Amazonian tree species has occurred across temporal scales, and contrasts with the prevailing view of hybridizations rarity in Amazonia. Overall, our results provide novel evidence that reticulate evolution influenced diversification in part of the Amazonian tree flora, which is the most diverse on Earth.

evolutionary biology↗

bioRxiv2019

Adaptive evolution explains the present-day distribution of the thermal sensitivity of population growth rate

Developing a thorough understanding of how ectotherm physiology adapts to different thermal environments is of crucial importance, especially in the face of global climate change. A key aspect of an organisms thermal performance curve--the relationship between fitness-related trait performance and temperature--is its thermal sensitivity, i.e., the rate at which trait values increase with temperature within its typically-experienced thermal range. For a given trait, the distribution of thermal sensitivities across species, often quantified as "activation energy" values, is typically right-skewed. Currently, the mechanisms that generate this distribution are unclear, with considerable debate about the role of thermodynamic constraints vs adaptive evolution. Here, using a phylogenetic comparative approach, we study the evolution of the thermal sensitivity of population growth rate across phytoplankton (Cyanobacteria and eukaryotic microalgae) and prokaryotes (bacteria and archaea), two microbial groups that play a major role in the global carbon cycle. We find that thermal sensitivity across these groups is moderately phylogenetically heritable, and that its distribution is shaped by repeated evolutionary convergence throughout its parameter space. More precisely, we detect bursts of adaptive evolution in thermal sensitivity, increasing the amount of overlap among its distributions in different clades. We obtain qualitatively similar results from evolutionary analyses of the thermal sensitivities of two physiological rates underlying growth rate: net photosynthesis and respiration of plants. Furthermore, we find that these episodes of evolutionary convergence are consistent with two opposing forces: decrease in thermal sensitivity due to environmental fluctuations and increase due to adaptation to stable environments. Overall, our results indicate that adaptation can lead to large and relatively rapid shifts in thermal sensitivity, especially in microbes where rapid evolution can occur at short time scales. Thus, more attention needs to be paid to elucidating the implications of rapid evolution in organismal thermal sensitivity for ecosystem functioning. Author summaryChanges in environmental temperature influence the performance of biological traits (e.g., respiration rate) in ectotherms, with the relationship between trait performance and temperature (the "thermal performance curve") being single-peaked. Understanding how thermal performance curves adapt to different environments is important for predicting how organisms will be impacted by climate change. One key aspect of the shape of these curves is the thermal sensitivity near temperatures typically experienced by the species. Whether and how thermal sensitivity responds to different environments is a topic of active debate. To shed light on this, here we perform an evolutionary analysis of the thermal sensitivity of three key traits of prokaryotes, phytoplankton, and plants. We show that thermal sensitivity does not evolve in a gradual manner, but can differ considerably even between closely related species. This suggests that thermal sensitivity undergoes rapid adaptive evolution, which is further supported by our finding that thermal sensitivity varies weakly with latitude. We conclude that variation in thermal sensitivity arises partly from adaptation to environmental factors and that this may need to be accounted for in ecophysiological models.

evolutionary biology↗

bioRxiv2018

Phytoplankton thermal responses adapt in the absence of hard thermodynamic constraints

To better predict how populations and communities respond to climatic temperature variation, it is necessary to understand how the shape of the response of fitness-related traits to temperature evolves (the thermal performance curve). Currently, there is disagreement about the extent to which the evolution of thermal performance curves is constrained. One school of thought has argued for the prevalence of thermodynamic constraints through enzyme kinetics, whereas another argues that adaptation can--at least partly--overcome such constraints. To shed further light on this debate, we perform a phylogenetic meta-analysis of the thermal performance curves of growth rate of phytoplankton--a globally important functional group--, controlling for environmental effects (habitat type and thermal regime). We find that thermodynamic constraints have a minor influence on the shape of the curve. In particular, we detect a very weak increase of maximum performance with the temperature at which the curve peaks, suggesting a weak "hotter-is-better" constraint. Also, instead of a constant thermal sensitivity of growth across species, as might be expected from strong constraints, we find that all aspects of the thermal performance curve evolve along the phylogeny. Our results suggest that phytoplankton thermal performance curves adapt to thermal environments largely in the absence of hard thermodynamic constraints.

evolutionary biology↗

bioRxiv2017

Comparative genomics of bdelloid rotifers: evaluating the effects of asexuality and desiccation tolerance on genome evolution

Bdelloid rotifers are microscopic invertebrates that have existed for millions of years apparently without sex or meiosis. They inhabit a variety of temporary and permanent freshwater habitats globally, and many species are remarkably tolerant of desiccation. Bdelloids offer an opportunity to better understand the evolution of sex and recombination, but previous work has emphasized desiccation as the cause of several unusual genomic features in this group. Here, we evaluate the relative effects of asexuality and desiccation tolerance on genome evolution by comparing whole genome sequences for three bdelloid species: Adineta ricciae (desiccation tolerant), Rotaria macrura and Rotaria magnacalcarata (both desiccation intolerant) to the only published bdelloid genome to date, that of Adineta vaga (also desiccation tolerant). We find that tetraploidy is conserved among all four bdelloid species, but homologous divergence in obligately aquatic Rotaria genomes is low, well within the range observed between alleles in obligately sexual, diploid animals. In addition, we find that homologous regions in A. ricciae are largely collinear and do not form palindromic repeats as observed in the published A. vaga assembly. These findings are contrary to current understanding of the role of desiccation in shaping the bdelloid genome, and indicate that various features interpreted as genomic evidence for long-term ameiotic evolution are not general to all bdelloid species, even within the same genus. Finally, we substantiate previous findings of high levels of horizontally transferred non-metazoan genes encoded in both desiccating and non-desiccating bdelloid species, and show that this is a unique feature of bdelloids among related animal phyla. Comparisons within bdelloids and to other desiccation-tolerant animals, however, again call into question the purported role of desiccation in horizontal transfer.

evolutionary biology↗

bioRxiv2017

Evidence for "inter- and intraspecific horizontal genetic transfers" between anciently asexual bdelloid rotifers is explained by cross-contamination

Bdelloid rotifers are microscopic invertebrates thought to have evolved for millions of years without sexual reproduction. They have attracted the attention of biologists puzzled by the maintenance of sex among nearly all other eukaryotes. Bdelloid genomes have an unusually high proportion of horizontally acquired non-metazoan genes. This well-substantiated finding has invited speculation that homologous horizontal transfer between rotifers also may occur, perhaps even 'replacing' sex. A 2016 study in Current Biology claimed to supply evidence for this hypothesis. The authors sampled rotifers of the genus Adineta from natural populations and sequenced one mitochondrial and four nuclear loci. For several samples, species assignments were incongruent among loci, which the authors interpreted as evidence of \"interspecific genetic exchanges\". Here, we use sequencing chromatograms supplied by the authors to demonstrate that samples treated as individuals actually contained two or more divergent mitochondrial and ribosomal sequences, indicating contamination with DNA from additional animals belonging to the supposed \"donor species\". We also show that \"exchanged\" molecules share only 75% sequence homology, a degree of divergence incompatible with established mechanisms of recombination and genomic features of Adineta. These findings are parsimoniously explained by cross-contamination of tubes with animals or DNA from different species. Given the proportion of tubes contaminated in this way, we show by calculation that evidence for \"intraspecific horizontal exchange\" in the same dataset is explained by contamination with conspecific DNA. On the clear evidence of these analyses, the 2016 study provides no reliable support for the hypothesis of horizontal genetic transfer between or within these bdelloid species.

evolutionary biology↗