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bioRxiv2017

Metaviz: interactive statistical and visual analysis of metagenomic data

Along with the survey techniques of 16S rRNA amplicon and whole-metagenome shotgun sequencing, an array of tools exists for clustering, taxonomic annotation, normalization, and statistical analysis of microbiome sequencing results. Integrative and interactive visualization that enables researchers to perform exploratory analysis in this feature rich hierarchical data is an area of need. In this work, we present Metaviz, a web browser-based tool for interactive exploratory metagenomic data analysis. Metaviz can visualize abundance data served from an R session or a Python web service that queries a graph database. As metagenomic sequencing features have a hierarchy, we designed a novel navigation mechanism to explore this feature space. We visualize abundance counts with heatmaps and stacked bar plots that are dynamically updated as a user selects taxonomic features to inspect. Metaviz also supports common data exploration techniques, including PCA scatter plots to interpret variability in the dataset and alpha diversity boxplots for examining ecological community composition. The Metaviz application and documentation is hosted at http://www.metaviz.org.

bioinformatics↗

bioRxiv2017

Demographic variability and heterogeneity among individuals within and among clonal bacteria strains

Identifying what drives individual heterogeneity has been of long interest to ecologists, evolutionary biologists and biodemographers, because only such identification provides deeper understanding of ecological and evolutionary population dynamics. In natural populations one is challenged to accurately decompose the drivers of heterogeneity among individuals as genetically fixed or selectively neutral. Rather than working on wild populations we present here data from a simple bacterial system in the lab, Escherichia coli. Our system, based on cutting-edge microfluidic techniques, provides high control over the genotype and the environment. It therefore allows to unambiguously decompose and quantify fixed genetic variability and dynamic stochastic variability among individuals. We show that within clonal individual variability (dynamic heterogeneity) in lifespan and lifetime reproduction is dominating at about 82-88%, over the 12-18% genetically (adaptive fixed) driven differences. The genetic differences among the clonal strains still lead to substantial variability in population growth rates (fitness), but, as well understood based on foundational work in population genetics, the within strain neutral variability slows adaptive change, by enhancing genetic drift, and lowering overall population growth. We also revealed a surprising diversity in senescence patterns among the clonal strains, which indicates diverse underlying cell-intrinsic processes that shape these demographic patterns. Such diversity is surprising since all cells belong to the same bacteria species, E. coli, and still exhibit patterns such as classical senescence, non-senescence, or negative senescence. We end by discussing whether similar levels of non-genetic variability might be detected in other systems and close by stating the open questions how such heterogeneity is maintained, how it has evolved, and whether it is adaptive.\n\nData depositionThe processed image analysis data, R code, as well as the Leslie matrices will be archived at Dryad.org.

evolutionary biology↗

bioRxiv2017

Disease implications of animal social organization and network structure - a quantitative analysis

O_LIThe disease costs of sociality have largely been understood through the link between group size and transmission. However, infectious disease spread is driven primarily by the social organization of interactions in a group and not its size.\nC_LIO_LIWe used statistical models to review the social network organization of 47 species, including mammals, birds, reptiles, fish and insects by categorizing each species into one of three social systems, relatively solitary, gregarious and socially hierarchical. Additionally, using computational experiments of infection spread, we determined the disease costs of each social system.\nC_LIO_LIWe find that relatively solitary species have large variation in number of social partners, that socially hierarchical species are the least clustered in their interactions, and that social networks of gregarious species tend to be the most fragmented. However, these structural differences are primarily driven by weak connections, which suggests that different social systems have evolved unique strategies to organize weak ties.\nC_LIO_LIOur synthetic disease experiments reveal that social network organization can mitigate the disease costs of group living for socially hierarchical species when the pathogen is highly transmissible. In contrast, highly transmissible pathogens cause frequent and prolonged epidemic outbreaks in gregarious species.\nC_LIO_LIWe evaluate the implications of network organization across social systems despite methodological challenges, and our findings offer new perspective on the debate about the disease costs of group living. Additionally, our study demonstrates the potential of meta-analytic methods in social network analysis to test ecological and evolutionary hypotheses on cooperation, group living, communication, and resilience to extrinsic pressures.\nC_LI

epidemiology↗

bioRxiv2017

High-Throughput Metabolic Network Analysis and Metatranscriptomics of a Cosmopolitan and Streamlined Freshwater Lineage

An explosion in the number of available genome sequences obtained through metagenomics and single-cell genomics has enabled a new view of the diversity of microbial life, yet we know surprisingly little about how microbes interact with each other or their environment. In fact, the majority of microbial species remain uncultivated, while our perception of their ecological niches is based on reconstruction of their metabolic potential. In this work, we demonstrate how the \"seed set framework\", which computes the set of compounds that an organism must acquire from its environment (1), enables computational analysis of metabolic reconstructions, while providing new insights into a microbes metabolic capabilities, such as nutrient use and auxotrophies. We apply this framework to members of the ubiquitous freshwater Actinobacterial lineage acI, confirming and extending previous experimental and genomic observations implying that acI bacteria are heterotrophs reliant on peptides and saccharides. We also present the first metatranscriptomic study of the acI lineage, revealing high expression of transport proteins and the light-harvesting protein actinorhodopsin. Putative transport proteins complement predictions of nutrients and essential metabolites while providing additional support to the hypothesis that members of the acI are photoheterotrophs.\n\nImportanceThe metabolic activity of uncultivated microorganisms contributes to numerous ecosystem processes, ranging from nutrient cycling in the environment to influencing human health and disease. Advances in sequencing technology have enabled the assembly of genomes for these microorganisms, but our ability to generate reference genomes far outstrips our ability to analyze them. Common approaches to analyzing microbial metabolism require reconstructing the entirety of an organisms metabolic pathways, or performing targeted searches for genes involved in a specific process. This paper presents a third approach, in which draft metabolic reconstructions are used to identify compounds through which an organism may interact with its environment. These compounds can then guide more intensive metabolic reconstruction efforts, and also provide new hypotheses about the specific contributions microbes make to ecosystem-scale metabolic processes.

microbiology↗

bioRxiv2017

Habitat generalists or specialists, insights from comparative genomic analyses of Thermosipho lineages

Thermosipho species inhabit various extreme environments such as marine hydrothermal vents, petroleum reservoirs and terrestrial hot springs. A 16S rRNA phylogeny of available Thermosipho spp. sequences suggested habitat specialists adapted to living in hydrothermal vents only, and habitat generalists inhabiting oil reservoirs, hydrothermal vents and hotsprings. Comparative genomics and recombination analysis of the genomes of 15 Thermosipho isolates separated them into three species with different habitat distributions, the widely distributed T. africanus and the more specialized, T. melanesiensis and T. affectus. The three Thermosipho species can also be differentiated on the basis of genome content. For instance the T. africanus genomes had the largest repertoire of carbohydrate metabolism, which could explain why these isolates were obtained from ecologically more divergent habitats. The three species also show different capacities for defense against foreign DNA. T. melanesiensis and T. africanus both had a complete RM system, while this was missing in T. affectus. These observations also correlated with Pacbio sequencing, which revealed a methylated T. melanesiensis BI431 genome, while no methylation was detected among two T. affectus isolates. All the genomes carry CRISPR arrays accompanied by more or less complete CRISPR-cas systems. Interestingly, some isolates of both T. melanesiensis and T. africanus carry integrated prophage elements, with spacers matching these in their CRISPR arrays. Taken together, the comparative genomic analyses of Thermosipho spp. revealed genetic variation allowing habitat differentiation within the genus as well as differentiation with respect to invading mobile DNA that is present in subsurface ecosystems.

microbiology↗

bioRxiv2017

What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies.

The process by which species evolve can be illuminated by investigating barriers that limit gene flow between taxa. Recent radiations, such as Heliconius butterflies, offer the opportunity to compare isolation between pairs of taxa at different stages of ecological, geographic and phylogenetic divergence. We carry out a comparative analysis of existing and novel data in order to quantify the strength and direction of isolating barriers within a well-studied clade of Heliconius. Our results highlight that increased divergence is associated with the accumulation of stronger and more numerous barriers to gene flow. Wing pattern is both under natural selection for Mullerian mimicry and involved in mate choice, and therefore underlies several isolating barriers. However, pairs which share a similar wing pattern, also display strong reproductive isolation mediated by traits other than wing pattern. This suggests that, while wing pattern is a key factor for early stages of divergence, it is not essential at a higher level. Additional factors including habitat isolation, hybrid sterility and chemically-mediated mate choice are associated with complete speciation. Therefore, although most previous work has emphasised the role of wing pattern, our comparative results highlight that speciation is a multidimensional process, whose completion is stabilized by many factors.

evolutionary biology↗

bioRxiv2017

Functional Bias and Demographic History Obscure Patterns of Selection among Single-Copy Genes in a Fungal Species Complex

Many different evolutionary processes may be responsible for explaining natural variation within genomes, some of which include natural selection at the molecular level and changes in population size. Fungi are highly adaptable organisms, and their relatively small genomes and short generation times make them pliable for evolutionary genomic studies. However, adaptation in wild populations has been relatively less documented compared to experimental or clinical studies. Here, we analyzed DNA sequences from 502 putative single-copy orthologous genes in 63 samples that represent seven recently diverged North American Amanita (jacksonii-complex) lineages. For each gene and each species, we measured the genealogical sorting index (gsi) and infinite-site-based summary statistics, such as [Formula], [Formula] and DTaj in coding and intron regions. MKT-based approaches and likelihood-ratio-test Kn/Ks models were used to measure natural selection in all coding sequences. Multi-locus (Extended) Bayesian Skyline Plots (eBSP) were used to model intraspecific demographic changes through time based on unlinked, putative neutral regions (introns). Most genes show evidence of long-term purifying selection, likely reflecting a functional bias implicit in single-copy genes. We find that two species have strongly negatively skewed Tajimas D, while three other have a positive skew, corresponding well with patterns of demographic expansion and contraction. Standard MKT analyses resulted in a high incidence of near-zero with a tendency towards negative values. In contrast, estimates based on the distribution of fitness effects (DFE), which accounts for demographic effects and slightly deleterious mutations, suggest a higher proportion of sites fixed by positive selection. The difference was more notorious in species with expansion signatures or with historically low population sizes, evidencing the concealing effects of specific demographic histories. Finally, we attempt to mitigate Gene Ontology term overrepresentation, highlighting the potential adaptive or ecological roles of some genes under positive selection.

evolutionary biology↗

bioRxiv2017

Wild tobacco genomes reveal the evolution of nicotine biosynthesis

Nicotine, the signature alkaloid of Nicotiana species responsible for the addictive properties of human tobacco smoking, functions as a defensive neurotoxin against attacking herbivores. However, the evolution of the genetic features that contributed to the assembly of the nicotine biosynthetic pathway remains unknown. We sequenced and assembled genomes of two wild tobaccos, Nicotiana attenuata (2.5 Gb) and N. obtusifolia (1.5 Gb), two ecological models for investigating adaptive traits in nature. We show that after the Solanaceae whole genome triplication event, a repertoire of rapidly expanding transposable elements (TEs) bloated these Nicotiana genomes, promoted expression divergences among duplicated genes and contributed to the evolution of herbivory-induced signaling and defenses, including nicotine biosynthesis. The biosynthetic machinery that allows for nicotine synthesis in the roots evolved from the stepwise duplications of two ancient primary metabolic pathways: the polyamine and nicotinic acid dinucleotide (NAD) pathways. While the duplication of the former is shared among several Solanaceous genera which produce polyamine-derived tropane alkaloids, the innovation and efficient production of nicotine in the genus Nicotiana required lineage-specific duplications within the NAD pathway and the evolution of root-specific expression of the duplicated Solanaceae-specific ethylene response factor (ERF) that activates the expression of all nicotine biosynthetic genes. Furthermore, TE insertions that incorporated transcription factor binding motifs also likely contributed to the coordinated metabolic flux of the nicotine biosynthetic pathway. Together, these results provide evidence that TEs and gene duplications facilitated the emergence of a key metabolic innovation relevant to plant fitness.

genomics↗

bioRxiv2017

A generator of morphological clones for plant species

Detailed and realistic tree form generators have numerous applications in ecology and forestry. Here, we present an algorithm for generating morphological tree \"clones\" based on the detailed reconstruction of the laser scanning data, statistical measure of similarity, and a plant growth algorithm with simple stochastic rules. The algorithm is designed to produce tree forms, i.e. morphological clones, similar as a whole (coarse-grain scale), but varying in minute details of organization (fine-grain scale). We present a general procedure for obtaining these morphological clones. Although we opted for certain choices in our algorithm, its various parts may vary depending on the application. Namely, we have shown that specific multi-purpose procedural stochastic growth model can be algorithmically adjusted to produce the morphological clones replicated from the target experimentally measured tree. For this, we have developed a statistical measure of similarity (structural distance) between any given pair of trees, which allows for the comprehensive comparing of the tree morphologies in question by means of empirical distributions describing geometrical and topological features of a tree. Our algorithm can be used in variety of applications and contexts for exploration of the morphological potential of the growth models, arising in all sectors of plant science research.\n\nSummary StatementWe present an algorithmic framework, based on the Bayesian inference, for generating morphological tree clones using a combination of stochastic growth models and experimentally derived tree structures.

systems biology↗

bioRxiv2017

Foreground Enhancement and Background Suppression in Human Early Visual System During Passive Perception of Natural Images

One of the major challenges in visual neuroscience is represented by foreground-background segmentation. Data from nonhuman primates show that segmentation leads to two distinct, but associated processes: the enhancement of neural activity during figure processing (i.e., foreground enhancement) and the suppression of background-related activity (i.e., background suppression). To study foreground-background segmentation in ecological conditions, we introduce a novel method based on parametric modulation of low-level image properties followed by application of simple computational image-processing models. By correlating the outcome of this procedure with human fMRI activity measured during passive viewing of 334 natural images, we reconstruct easily interpretable \"neural images\" from seven visual areas: V1, V2, V3, V3A, V3B, V4 and LOC. Results show evidence of foreground enhancement for all tested regions, while background suppression specifically occurs in V4 and LOC. \"Neural images\" reconstructed from V4 and LOC revealed a preserved spatial resolution of foreground textures, indicating a richer representation of the salient part of natural images, rather than a simplistic model of object shape. Our results indicate that scene segmentation is an automatic process that occurs during natural viewing, even when individuals are not required to perform any particular task.

neuroscience↗

bioRxiv2017

Niche construction in evolutionary theory: the construction of an academic niche?

In recent years, fairly far-reaching claims have been repeatedly made about how niche construction, the modification by organisms of their environment, and that of other organisms, represents a vastly neglected phenomenon in ecological and evolutionary thought. The proponents of this view claim that the niche construction perspective greatly expands the scope of standard evolutionary theory and that niche construction deserves to be treated as a significant evolutionary process in its own right, almost at par with natural selection. Claims have also been advanced about how niche construction theory represents a substantial extension to, and re-orientation of, standard evolutionary theory, which is criticized as being narrowly gene-centric and ignoring the rich complexity and reciprocity of organism-environment interactions. We examine these claims in some detail and show that they do not stand up to scrutiny. We suggest that the manner in which niche construction theory is sought to be pushed in the literature is better viewed as an exercise in academic niche construction whereby, through incessant repetition of largely untenable claims, and the deployment of rhetorically appealing but logically dubious analogies, a receptive climate for a certain sub-discipline is sought to be manufactured within the scientific community. We see this as an unfortunate, but perhaps inevitable, nascent post-truth tendency within science.

evolutionary biology↗

bioRxiv2017

Environmental cholera (Vibrio cholerae) dynamics in an estuarine system in southern coastal Ecuador

Cholera emergence is strongly linked to local environmental and ecological context. The 1991-2004 pandemic emerged in Peru and spread north into Ecuadors El Oro province, making this a key site for potential re-emergence. Machala, El Oro, is a port city of 250,000, near the Peruvian border. Many livelihoods depend on the estuarine system, from fishing for subsistence and trade, to domestic water use. In 2014, we conducted biweekly sampling for 10 months in five estuarine locations, across a gradient of human use, and ranging from inland to ocean. We measured water characteristics implicated in V. cholerae growth and persistence: pH, temperature, salinity, and algal concentration, and evaluated samples in five months for pathogenic and non-pathogenic Vibrio cholerae, by polymerase chain reaction (PCR). We found environmental persistence of strains O1 and O139, but no evidence for toxigene presence. V. cholerae presence was coupled to algal and salinity concentration, and sites exhibited considerable seasonal and spatial heterogeneity. This study indicates that environmental conditions in Machala are optimal for human cholera re-emergence, with risk peaking during September, and higher risk near urban periphery low-income communities. This highlights a need for surveillance of this coupled cholera- estuarine system to anticipate potential future outbreaks.

epidemiology↗

bioRxiv2017

The evolution of queen control over worker reproduction in the social Hymenoptera

A trademark of eusocial insect species is reproductive division of labor, in which workers forego their own reproduction while the queen produces almost all offspring. The presence of the queen is key for maintaining social harmony, but the specific role of the queen in the evolution of eusociality remains unclear. A long-discussed scenario is that a queen either behaviorally or chemically sterilizes her workers. However, the demographic and ecological conditions that enable such manipulation are unknown. Accordingly, we propose a simple model of evolutionary dynamics that is based on haplodiploid genetics. We consider a mutation that acts in a queen, causing her to control the reproductive behavior of her workers. Our mathematical analysis yields precise conditions for the evolutionary emergence and stability of queen-induced worker sterility. These conditions do not depend on the queen's mating frequency. Moreover, we find that queen control is always established if it increases colony reproductive efficiency and can evolve even if it decreases colony efficiency. We further outline the conditions under which queen control is evolutionarily stable against invasion by mutant, reproductive workers.

evolutionary biology↗

bioRxiv2017

Costs and benefits of sub-lethal Drosophila C virus infection

Viruses are major evolutionary drivers of insect immune systems. Much of our knowledge of insect immune responses derives from experimental infections using the fruit fly Drosophila melanogaster. Most experiments, however, employ lethal pathogen doses through septic injury, frequently overwhelming host physiology. While this approach has revealed a number of immune mechanisms, it is less informative about the fitness costs hosts may experience during infection in the wild. Using both systemic and oral infection routes we find that even apparently benign, sub-lethal infections with the horizontally transmitted Drosophila C Virus (DCV) can cause significant physiological and behavioral morbidity that is relevant for host fitness. We describe DCV-induced effects on fly reproductive output, digestive health, and locomotor activity, and we find that viral morbidity varies according to the concentration of pathogen inoculum, host genetic background and sex. Notably, sub-lethal DCV infection resulted in a significant increase in fly reproduction, but this effect depended on host genotype. We discuss the relevance of sub-lethal morbidity for Drosophila ecology and evolution, and more broadly, we remark on the implications of deleterious and beneficial infections for the evolution of insect immunity.

evolutionary biology↗

bioRxiv2017

Allopatric divergence, local adaptation, and multiple Quaternary refugia in a long-lived tree (Quercus spinosa) from subtropical China

O_LIThe complex geography and climatic changes occurring in subtropical China during the Tertiary and Quaternary might have provided substantial opportunities for allopatric speciation. To gain further insight into these processes, we reconstruct the evolutionary history of Quercus spinosa, a common evergreen tree species mainly distributed in this area.\nC_LIO_LIForty-six populations were genotyped using four chloroplast DNA regions and 12 nuclear microsatellite loci to assess genetic structure and diversity, which was supplemented by divergence time and diversification rate analyses, environmental factor analysis, and ecological niche modeling of the species distributions in the past and at present.\nC_LIO_LIThe genetic data consistently identified two lineages: the western Eastern Himalaya-Hengduan Mountains lineage and the eastern Central-Eastern China lineage, mostly maintained by populations environmental adaptation. These lineages diverged through climate/orogeny-induced vicariance during the Neogene and remained separated thereafter. Genetic data strongly supported the multiple refugia (per se, interglacial refugia) or refugia within refugia hypotheses to explain Q. spinosa phylogeography in subtropical China.\nC_LIO_LIQ. spinosa population structure highlighted the importance of complex geography and climatic changes occurring in subtropical China during the Neogene in providing substantial opportunities for allopatric divergence.\nC_LI

evolutionary biology↗

bioRxiv2017

How to get the most bang for your buck: the evolution and physiology of nutrition-dependent resource allocation strategies

All organisms utilize resources to grow, survive, and reproduce. The supply of these resources varies widely across landscapes and time, imposing ultimate constraints on the maximal trait values for allocation-related traits. In this review, we address three key questions fundamental to our understanding of the evolution of allocation strategies and their underlying mechanisms. First, we ask: how diverse are flexible resource allocation strategies among different organisms? We find there are many, varied, examples of flexible strategies that depend on nutrition. However, this diversity is often ignored in some of the best-known cases of resource allocation shifts, such as the commonly observed pattern of lifespan extension under nutrient limitation. A greater appreciation of the wide variety of flexible allocation strategies leads directly to our second major question: what conditions select for different plastic allocation strategies? Here, we highlight the need for additional models that explicitly consider the evolution of phenotypically plastic allocation strategies and empirical tests of the predictions of those models in natural populations. Finally, we consider the question: what are the underlying mechanisms determining resource allocation strategies? Although evolutionary biologists assume differential allocation of resources is a major factor limiting trait evolution, few proximate mechanisms are known that specifically support the model. We argue that an integrated framework can reconcile evolutionary models with proximate mechanisms that appear at first glance to be in conflict with these models. Overall, we encourage future studies to 1) mimic ecological conditions in which those patterns evolve, and 2) take advantage of the omic opportunities to produce multi-level data and analytical models that effectively integrate across physiological and evolutionary theory.

evolutionary biology↗

bioRxiv2017

Dengue fever and Aedes aegypti risk in the Galapagos Islands, Ecuador

IntroductionDengue fever is an emerging infectious disease in the Galapagos Islands of Ecuador, with the first cases reported in 2002 and periodic outbreaks since then. Here we report the results of a pilot study conducted in two cities in 2014: Puerto Ayora (PA) on Santa Cruz Island, and Puerto Baquerizo Moreno (PB) on Santa Cristobal Island. The aims of this study were to assess the social-ecological risk factors associated with dengue and mosquito presence at the household-level.\n\nMethodsIn 2014 we conducted 100 household surveys (50 on each island) in neighborhoods with prior reported dengue. Adult mosquitoes were collected inside and outside the home, larval indices were determined through container surveys, and heads of households were interviewed to determine demographics, prior dengue infections, housing conditions, and knowledge, attitudes and practices regarding dengue. Multimodel selection methods were used to derive best-fit generalized linear regression (GLM) models of prior dengue infection, and the presence of Ae. aegypti in the home.\n\nResultsWe found that 24% of PB and 14% of PA respondents self-reported a prior dengue infection, and more PB homes than PA homes had Ae. aegypti. The top-ranked model for prior dengue infection included human movement - travel between neighborhoods, between islands, and to the mainland; demographics including salary level and education of the head of household, and increase with more people per room in a house, house condition, access to water quality issues, and dengue awareness. The top-ranked model for the presence of Ae. aegypti included housing conditions, including the presence of window screens and air conditioners, mosquito control actions, and dengue risk perception.\n\nDiscussion/conclusionTo our knowledge, this is the first study of dengue risk and Aedes aegypti in the Galapagos Islands. The findings that human movement within and between islands, and to and from the mainland, were important to reported dengue cases confirms concerns of this route of introduction and repeated transmission.

epidemiology↗

bioRxiv2017

Plasmid DNA analysis of pristine groundwater microbial communities reveal extensive presence of metal resistance genes

Native plasmids constitute a major category of extrachromosomal DNA elements responsible for harboring and transferring genes important in survival and fitness. A focused evaluation of plasmidomes can reveal unique adaptations required by microbial communities. We examined the plasmid DNA from two pristine wells at the Oak Ridge Field Research Center. Using a cultivation-free method that targets plasmid DNA, a total of 42,440 and 32,232 (including 67 and 548 complete circular units) scaffolds > 2 kb were obtained from the two wells. The taxonomic distribution of bacteria in the two wells showed greater similarity based on their plasmidome sequence, relative to 16S rRNA sequence comparison. This similarity is also evident in the plasmid encoded functional genes. Among functionally annotated genes, candidates providing resistance to copper, zinc, cadmium, arsenic, and mercury were particularly abundant and common to the plasmidome of both wells. The primary function encoded by the most abundant circularized plasmid, common to both wells, was mercury resistance, even though the current ground water does not contain detectable levels of mercury. This study reveals that the plasmidome can have a unique ecological role in maintaining the latent capacity of a microbiome enabling rapid adaptation to environmental stresses.

microbiology↗