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Inter-individual gene expression variability implies stable regulation of brain-biased genes across organs
<div> <div> <h2>Abstract</h2> <a href="https://github.com/christabel-bucao/fish-variability-across-organs/#abstract"></a></div> <p>Phenotypic variation among individuals plays a key role in evolution, since variation provides the material on which natural selection can act. One important link between genetic and phenotypic variation is gene expression. As for other phenotypes, the range of accessible expression variation is limited and biased by different evolutionary and developmental constraints. Gene expression variability broadly refers to the tendency of a gene to vary in expression (i.e., between individuals or cells) due to stochastic fluctuations or differences in genetic, epigenetic, or environmental factors, separately from the differences between e.g. organs. Variability due to biomolecular stochasticity (transcriptional ‘noise’) and cell-to-cell heterogeneity has been well-studied in isogenic populations of unicellular organisms such as bacteria and yeasts. However, for more complex organisms with multiple cells, tissues, and organs sharing the same genetic background, the interplay between inter-individual expression variability, gene and organ function, and gene regulation remains an open question. In this study, we used highly multiplexed 3’-end Bulk RNA Barcoding and sequencing (BRB-seq) to generate transcriptome profiles spanning at least nine organs in outbred individuals of three ray-finned fish species: zebrafish, Northern pike, and spotted gar. For each condition, we measured expression variation per gene independent of mean expression level. We observed that lowly variable genes are enriched in cellular housekeeping functions whereas highly variable genes are enriched in stimulus-response functions. Furthermore, genes with highly variable expression between individuals evolve under weaker purifying selection at the coding sequence level, indicating that intra-species gene expression variability predicts inter-species protein sequence divergence. Genes that are broadly expressed across organs tend to be both highly expressed and lowly variable between individuals, whereas organ-biased genes are typically highly variable within their top organ of expression. For genes with organ-biased expression profiles, we inferred differences in selective pressure on gene regulation depending on their top organ. We found that genes with peak expression in the brain have low inter-individual expression variability across non-nervous organs, suggesting stabilizing selection on regulatory evolution of brain-biased genes. Conversely, liver-biased genes have highly variable expression across organs, implying weaker regulatory constraints. These patterns show that gene regulatory mechanisms evolved differently based on constraints on the primary organ.</p> <h2>Directory Structure</h2> </div> <ul> <li> <p><code>config/</code>: Contains YAML file indicating package versions for conda environment</p> </li> <li> <p><code>data/</code>: Contains input data</p> <ul> <li><code>counts/</code>: Contains counts and UMI-deduplicated counts. Currently under embargo and will be made available upon acceptance for publication.</li> <li><code>gene_metadata/</code>: Contains gene biotype information from Ensembl</li> <li><code>sample_metadata/</code>: Contains sample metadata files for each species</li> <li><code>selectome/</code>: Contains selection statistics from the <a href="https://selectome.org/" rel="nofollow">Selectome</a> database<br><br></li> </ul> </li> <li> <p><code>results/</code>: Contains output files sorted by subfolders labeled after each step of the analysis pipeline. Only R notebook HTML files are available on the Git repository, please check Zenodo for R data files.</p> <ul> <li><code>run_pipeline.Rdata</code>: Contains all parameters used for each step of the analysis pipeline<br><br></li> </ul> </li> <li> <p><code>workflow/</code>: Contains scripts used for the analysis pipeline</p> <ul> <li><code>analysis/</code>: Contains all steps of the analysis pipeline, available as .Rmd files</li> <li><code>functions/</code>: Contains all functions used for analysis/</li> <li><code>renv/</code>: Used for package management in R</li> <li><code>run_pipeline.R</code>: Runs all the steps under analysis/</li> <li><code>run_go_figure.sh</code>: Runs <a href="https://gitlab.com/evogenlab/GO-Figure" rel="nofollow">GO-Figure!</a> 1.0.0 (downloaded separately)</li> <li><code>demultiplex_brbseq_fastq.sh</code>: Used for demultiplexing BRB-seq fastq files using <a href="https://github.com/DeplanckeLab/BRB-seqTools">BRB-seqTools</a> 1.6.1 (downloaded separately) for uploading to NCBI SRA</li> <li><code>rename_fastq_files.sh</code>: Used for renaming demultiplexed fastq files by mapping each barcode to their corresponding sample name</li> <li><code>renv.lock</code>: Lockfile for managing R package versions. Run <code>renv::restore()</code> to set up the R environment based on packages specified in the lockfile. All package versions used are also specified in the output HTML files under results/.</li> </ul> </li> </ul> <div> <h2>Species Codes</h2> </div> <ul> <li><strong>LOC</strong>: <em>Lepisosteus oculatus</em> (spotted gar)</li> <li><strong>ELU</strong>: <em>Esox lucius</em> (Northern pike)</li> <li><strong>DRE</strong>: <em>Danio rerio</em> (zebrafish)</li> </ul>
Data from: Number of neighbors instead of group size significantly affects individual vigilance levels in large animal aggregations
The group size effect states that animals living in groups gain anti-predator benefits through reducing vigilance levels as group size increases. A basic assumption of group size effect is that all individuals are equally important for a focal individual, who may adjust its vigilance levels according to social information acquired from them. However, some studies have indicated that neighbors pose greater influences on an individual's vigilance decisions than other group members, especially in large aggregations. Vigilance has also been found to be directed to both predators (anti-predation vigilance) and conspecifics (social vigilance). Central individuals might rely more on social vigilance than peripheral individuals. To test these hypotheses, we examined the effects of flock size, number of neighbors and position within a flock on vigilance and competition of greater white-fronted goose (Anser albifrons) that form large foraging flocks in winter, controlling the effects of other variables (group identity, winter period, and site). We found that individual vigilance levels were significantly affected by number of neighbors and position within a flock, whereas flock size showed no effect. Individuals devoted a large component of vigilance to nearby flock mates. Central individuals directed a relatively larger proportion of vigilance to monitor neighbors than peripheral ones, indicating that central individuals more relied on social information acquired from neighbors, possibly caused by the more blocked visual field of central individuals. Moreover, some social vigilance may function as conducting or preventing agonistic interactions since competition intensity was positively correlated with number of neighbors. Our study therefore demonstrate that the number of neighbors is more important than group size in determining individual vigilance in large animal groups. Further studies are still needed to unravel which neighbors pose greater influence on individual vigilance, and the factors that influence individuals to acquire information from their neighbors to adjust vigilance behaviors.
Data from: Natural selection on gall size: variable contributions of individual host plants to population-wide patterns
Studies that provide estimates of the form and magnitude of selection on herbivore traits at the level of individual plants in natural populations represent a vital step in understanding the interaction of selection and gene flow among host-affiliated insect populations when individual plants equate to differing selective regimes. We analyzed phenotypic selection on the trait gall size for a host-specific gall former at both the individual host plant and population level (across host plants) in each of two years. Linear and nonlinear selection and the fitness function relating gall size to the probability of survivorship in the absence of natural enemies were estimated for each level and year. Selection imposed by the host plant was observed in 19 of the 22 subpopulations monitored. At the population level, linear and nonlinear selection were evident each year. However, population-level estimates masked the significant heterogeneity in the form and direction of selection evident among plants each year. Heterogeneity among gall-former subpopulations is emphasized by our findings that selection varied from directional to stabilizing among plants and the majority of selection gradients estimated for individual plants did not fall within the 95% CIs of the population-level estimates.
Data from: Genomic analysis reveals depression due to both individual and maternal inbreeding in a free-living mammal population
There is ample evidence for inbreeding depression manifested as a reduction in fitness or fitness-related traits in the focal individual. In many organisms, fitness is not only affected by genes carried by the individual, but also by genes carried by their parents, for example if receiving parental care. While maternal effects have been described in many systems, the extent to which inbreeding affects fitness directly through the focal individual, or indirectly through the inbreeding coefficients of its parents, has rarely been examined jointly. The Soay sheep study population is an excellent system in which to test for both effects, as lambs receive extended maternal care. Here, we tested for both maternal and individual inbreeding depression in three fitness-related traits (birthweight and weight and hindleg length at 4 months of age) and three fitness components (first-year survival, adult annual survival and annual breeding success), using either pedigree-derived inbreeding or genomic estimators calculated using ~37 000 SNP markers. We found evidence for inbreeding depression in 4-month hindleg and weight, first-year survival in males, and annual survival and breeding success in adults. Maternal inbreeding was found to depress both birthweight and 4-month weight. We detected more instances of significant inbreeding depression using genomic estimators than the pedigree, which is partly explained through the increased sample sizes available. In conclusion, our results highlight that cross-generational inbreeding effects warrant further exploration in species with parental care and that modern genomic tools can be used successfully instead of, or alongside, pedigrees in natural populations.
Data from: Individual quality and age but not environmental or social conditions modulate costs of reproduction in a capital breeder
Costs associated with reproduction are widely known to play a role in the evolution of reproductive tactics with consequences to population and eco-evolutionary dynamics. Evaluating these costs as they pertain to species in the wild remains an important goal of evolutionary ecology. Individual heterogeneity, including differences in individual quality (i.e., among-individual differences in traits associated with survival and reproduction) or state, and variation in environmental and social conditions can modulate the costs of reproduction; however, few studies have considered effects of these factors simultaneously. Taking advantage of a detailed, long-term dataset for a population of feral horses (Sable Island, Nova-Scotia, Canada), we address the question of how intrinsic (quality, age), environmental (winter severity, location), and social conditions (group size, composition, sex ratio, density) influence the costs of reproduction on subsequent reproduction. Individual quality was measured using a multivariate analysis on a combination of four static and dynamic traits expected to depict heterogeneity in individual performance. Female quality and age interacted with reproductive status of the previous year to determine current reproductive effort, while no effect of social or environmental covariates was found. High quality females showed higher probabilities of giving birth and weaning their foal regardless of their reproductive status the previous year, while those of lower quality showed lower probabilities of producing foals in successive years. Middle-aged (prime) females had the highest probability of giving birth when they had not reproduced the year before but no such relationship with age was found among females that had reproduced the previous year, indicating that prime-aged females bear higher costs of reproduction. We show that individual quality and age were key factors modulating the costs of reproduction in a capital breeder but that environmental or social conditions were not, highlighting the importance of considering multiple factors when studying costs of reproduction.
Data from: Seasonal contrasts in individual consistency of oriental honey buzzards' migration
Individual consistency in migration can shine light on the mechanisms of migration. Most studies reported that birds are more consistent in the timing than in the routes or stopover sites during migration, but some specialist species showed the opposite patterns, being more consistent in spatial than temporal aspects of migration. One possible explanation for this contrast is that specialists rely on particular food or habitat resources, which restrict the migratory routes they can take, leading to high spatial consistency. If this is the case, the effect of specialist foraging should become apparent only when birds forage, instead of fasting and flying continuously. To test this effect, we analysed individual consistency in migration of the oriental honey buzzard (Pernis ptilorhynchus), a specialist raptor that feeds on honeybees and wasps, using a long-term tracking data set. As honey buzzards make extended stopovers during which they forage in spring but not in autumn, the spatial consistency should be higher in spring than in autumn. Honey buzzards were highly consistent in both their migratory routes and stopover sites in Southeast Asia, but only during spring migration. Our results highlight an important link between species' migratory consistency and foraging ecology.
From individuals to populations: How intraspecific competition shapes thermal reaction norms
1. Most ectotherms follow the temperature-size rule (TSR): in cold environments individuals grow slowly but reach a large asymptotic length. Intraspecific competition can induce plastic changes of growth rate and asymptotic length and competition may itself be modulated by temperature. 2. Our aim is to disentangle the joint effects of temperature and intraspecific competition on growth rate and asymptotic length. 3. We used two distinct clonal lineages of the Collembola Folsomia candida, to describe thermal reaction norms of growth rate, asymptotic length and reproduction over 6 temperatures between 6°C and 29°C. In parallel, we measured the long-term size-structure and dynamics of populations reared under the same temperatures to measure growth rates and asymptotic lengths in populations and to quantify the joint effects of competition and temperature on these traits. 4. We show that intraspecific competition modulates the temperature-size rule. In dense populations there is a direct negative effect of temperature on asymptotic length, but there is no temperature dependence of the growth rate, the dominant factor regulating growth being competition. The two lineages responded differently to the joint effects of temperature and competition on growth and asymptotic size and these genetic differences have marked effects on population structure along our temperature gradient. 5. Our results reinforce the idea that the TSR response of ectotherms can be modulated by biotic and abiotic stressors when studied in non-optimal laboratory experiments. Untangling complex interactions between environment and demography will help to understand how size will respond to environmental change and how climate change may influence population size structure.
Data from: Individual and temporal variation in habitat association of an alien carnivore at its invasion front
Gathering information on how invasive species utilize the habitat is important, in order to better aim actions to reduce their negative impact. We studied habitat use and selection of 55 GPS-marked raccoon dogs (30 males, 25 females) at their invasion front in Northern Sweden, with particular focus on differences between males and females, between movement states, and between seasons and times of the day. Daily movement pattern was used to classify GPS-locations into dispersing and settled. We focused on both anthropogenic and natural landscape characteristics. Since we did not have any a priori knowledge about the spatial scale of raccoon dog habitat selection, we first assessed how landscape characteristics of random points changed with distance from the GPS-location they were paired to. Because changes in habitat use became less pronounced at approximately 5 km for all variables, we focused on habitat use at two spatial scales: fine (500 m) and coarse (5 km). Habitat selection was strongest at the coarse scale, and reflected the results found for habitat use. Raccoon dogs selected agricultural areas and wetlands, lower altitudes, and shallow slopes, and avoided forests, open natural areas, and areas close to water and roads. There were no differences in habitat selection between males and females, or between movement states. This lack of sexual segregation increases the probability of encountering potential mates during dispersal, and therefore the likelihood for reproduction in new areas. The seasonal and diurnal pattern of habitat use may provide guidance for where and when to aim management efforts.
Data from: Resource preferences and the emergence of individual niche specialization within populations
<p>Growing evidence that individuals of many generalist animals behave as resource specialists has attracted substantial research interest for its ecological and evolutionary implications. Variation in resource preferences is considered to be critical for developing a general theory of individual specialization. However, it remains to be shown whether diverging preferences can arise among individuals sharing a similar environment, and whether these preferences are sufficiently stable over time to be ecologically relevant. We addressed these issues by means of common garden experiments in feral pigeons (<i>Columba livia</i>), a species known to exhibit among-individual resource specialization in the wild. Food-choice experiments on wild-caught pigeons and their captive-bred cross-fostered descendants showed that short-term variation in food preferences can easily arise within a population, and that this variation may represent a substantial fraction of the population foraging niche. However, the experiments also showed that, rather than being limited by genetic or vertical cultural inheritance, food preferences exhibited high plasticity and tended to converge in the long-term. Although our results challenge the notion that variation in food preferences is a major driver of resource specialization, early differences in preferences could pave the way to specializations when combined with neophobic responses and/or positive feedbacks that reinforce niche conservation.</p>
Data from: Dissimilarity of individual microsatellite profiles under different mutation models: empirical approach
Microsatellites (simple sequence repeats, SSRs) still remain popular molecular markers for studying neutral genetic variation. Two alternative models outline how new microsatellite alleles evolve. Infinite alleles model (IAM) assumes that all possible alleles are equally likely to result from a mutation, while stepwise mutation model (SMM) describes microsatellite evolution as stepwise adding or subtracting single repeat units. Genetic relationships between individuals can be analyzed in higher precision when assuming the SMM scenario with allele size differences as a proxy of genetic distance. If population structure is not predetermined in advance, an empirical data analysis usually includes (a) estimating proximity between individual SSR profiles with a selected dissimilarity measure and (b) determining putative genetic structure of a given set of individuals using methods of clustering and/or ordination for the obtained dissimilarity matrix. We developed new dissimilarity indices between SSR profiles of haploid, diploid, or polyploid organisms assuming different mutation models and compared the performance of these indices for determining genetic structure with population data and with simulations. More specifically, we compared SMM with a constant or variable mutation rate at different SSR loci to IAM using data from natural populations of a freshwater bryozoan Cristatella mucedo (diploid), wheat leaf rust Puccinia triticina (dikaryon), and wheat powdery mildew Blumeria graminis (monokaryon). We show that inferences about population genetic structure are sensitive to the assumed mutation model. With simulations, we found that Bruvo's distance performs generally poorly, while the new metrics are capturing the differences in the genetic structure of the populations.
Data from: Keystone individuals alter ecological and evolutionary consumer-resource dynamics
Intraspecific variation is central to our understanding of evolution and ecology, but these fields generally consider either the mean trait value or its variance. Alternatively, the keystone individual concept from behavioral ecology posits that a single individual with an extreme phenotype can have disproportionate and irreplaceable effects on group dynamics. Here, I generalize this concept to include non-behavioral traits and broader ecological and evolutionary dynamics. I test for the effects of individuals with extreme phenotypes on the ecology and evolution or a gall-forming fly and its natural enemies that select for opposite gall sizes. Specifically I introduce a putatively keystone predator-attracting individual gall-maker, hypothesizing that the presence of such an individual should (i) increase gall-maker population-level mortality, (ii) cause consumer communities to be dominated by species that are most attracted to the keystone individual, (iii) increase selection for traits conferring defense against the most common consumer, and (iv) weaken patterns of stabilizing selection. I find support for both the ecological and evolutionary consequences of single individuals with extreme phenotypes, suggesting that they can be considered keystone individuals. I discuss the generality of the keystone individual concept, suggesting likely consequences for ecology and evolution.
FIGURE 2. Vochysia microphylla. A. Population showing the cespitose growth habit. B. Well-branched individual from Vellozia gigantea trail. C. Flowering branch with flower buds. D. Flowering branch with open flowers. A. Photo L.C. Rodrigues. B–D. Photos G.H in Vochysia microphylla (Vochysiaceae), a new species from Serra do Cipó, Minas Gerais, Brazil
FIGURE 2. Vochysia microphylla. A. Population showing the cespitose growth habit. B. Well-branched individual from Vellozia gigantea trail. C. Flowering branch with flower buds. D. Flowering branch with open flowers. A. Photo L.C. Rodrigues. B–D. Photos G.H. Shimizu.
Data from: The challenges of recognising individuals with few distinguishing features: identifying red foxes Vulpes vulpes from camera-trap photos
Over the last two decades, camera traps have revolutionised the ability of biologists to undertake faunal surveys and estimate population densities, although identifying individuals of species with subtle markings remains challenging. We conducted a two-year camera-trapping study as part of a long-term study of urban foxes: our objectives were to determine whether red foxes could be identified individually from camera-trap photos, and highlight camera-trapping protocols and techniques to facilitate photo identification of species with few or subtle natural markings. We collected circa 800,000 camera-trap photos over 4945 camera days in suburban gardens in the city of Bristol, UK: 152,134 (19 %) included foxes, of which 13,888 (9 %) contained more than one fox. These provided 174,063 timestamped capture records of individual foxes; 170,923 were of foxes ≥ 3 months old. Younger foxes were excluded because they have few distinguishing features. We identified the individual (192 different foxes: 110 males, 49 females, 33 of unknown sex) in 168,417 (99 %) of these capture records; the remainder could not be identified due to poor image quality or because key identifying feature(s) were not visible. We show that carefully designed survey techniques facilitate individual identification of subtly-marked species. Accuracy is enhanced by camera-trapping techniques that yield large numbers of high resolution, colour images from multiple angles taken under varying environmental conditions. While identifying foxes manually was labour-intensive, currently available automated identification systems are unlikely to achieve the same levels of accuracy, especially since different features were used to identify each fox, the features were often inconspicuous, and their appearance varied with environmental conditions. We discuss how studies based on low numbers of photos, or which fail to identify the individual in a significant proportion of photos, risk losing important biological information, and may come to erroneous conclusions.
FIGURE 2. Individual tracks, g through n in Track analysis of the Neotropical genus Sepedonea Steyskal (Diptera: Sciomyzidae): a proposal based on the phylogenetic analysis of its species
FIGURE 2. Individual tracks, g through n: g — S. lindneri; h — S. guatemalana; i — S. giovana; j — S. guianica; l — S. telson; m — S. incipiens; n — S. trichotypa.
FIGURES 84–87 in Facial affect recognition in individuals at clinical high risk for psychosis
FIGURES 84–87. Mesoceration, aedeagi of holotypes. —84. M. brevigranum. —85. M. granulovestum. —86. M. truncatum. —87. M. umbrosum.
FIGURES 78–81 in Facial affect recognition in individuals at clinical high risk for psychosis
FIGURES 78–81. Mesoceration, aedeagi of holotypes. —78. M. concessum. —79. M. tabulare. —80. M. littlekarroo. —81. M. piceum.
FIGURES 71–74 in Facial affect recognition in individuals at clinical high risk for psychosis
FIGURES 71–74. Mesoceration, aedeagi of holotypes. —71. M. bispinum. —72. M. curvosum. —73. M. longipennis. —74. M. natalensis.
FIGURES 55–58 in Facial affect recognition in individuals at clinical high risk for psychosis
FIGURES 55–58. Mesoceration, aedeagi of holotypes. —55. M. barriotum. —56. M. incarinum. —57. M. semicarinulum. —58. M. compressum.
FIGURES 47–50 in Facial affect recognition in individuals at clinical high risk for psychosis
FIGURES 47–50. Mesoceration, aedeagi of holotypes. —47. M. periscopum. —48. M. splendorum. —49. M. maluti. —50. M. rapidensis.
FIGURES 32–35 in Facial affect recognition in individuals at clinical high risk for psychosis
FIGURES 32–35. Parasthetops, aedeagi of holotypes. —32. P. benefossus. —33. P. parallelus. —34. P. camurus. —35. P. reflexus.
ScienceDex guides
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These curated guides explain access requirements, typical timelines, costs, and reuse considerations for widely used research datasets.
Allen Brain Atlas
Allen Brain Atlas is an Allen Institute collection of brain map atlases, datasets, APIs, and analysis tools covering mouse, human, and non-human primate brain resources.
Annotated Behaviour and Observability Dataset (ABODe)
ABODe is a University of Edinburgh DataShare dataset for behavior classification in group-housed mice using home-cage video, identities, bounding boxes, ground-plate positions, and annotator labels.
DANDI Archive for NWB datasets
DANDI is a BRAIN Initiative archive for publishing and sharing neurophysiology data, including electrophysiology, optophysiology, and behavioral data packaged as NWB and related standards.
International Brain Laboratory public data
The International Brain Laboratory public data releases expose standardized mouse decision-making experiments, including Neuropixels recordings, widefield calcium imaging, behavior, and session metadata accessed through the ONE API.
OpenNeuro
OpenNeuro is a free, open platform for sharing neuroimaging datasets, with public search, dataset pages, and download paths for web, S3, DataLad, and the OpenNeuro CLI.