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The social and spatial ecology of dengue presence and burden during an outbreak in Guayaquil, Ecuador, 2012

Dengue fever, a mosquito-borne viral disease, is an ongoing public health problem in Ecuador and throughout the tropics, yet we have a limited understanding of the disease transmission dynamics in these regions. The objective of this study was to characterize the spatial dynamics and social-ecological risk factors associated with a recent dengue outbreak in Guayaquil, Ecuador. We examined georeferenced dengue cases (n = 4,248) and block-level census data variables to identify potential social-ecological variables associated with the presence and burden of dengue fever in Guayaquil in 2012. We applied LISA and Morans I tests to analyze hotspots of dengue cases and used multimodel selection in R computing language to identify covariates associated with dengue incidence at the census zone level. Significant hotspots of dengue transmission were found near the North Central and Southern portions of Guayaquil. Significant risk factors for presence of dengue included poor housing conditions (e.g., poor condition of ceiling, floors, and walls), access to paved roads, and receipt of remittances. Counterintuitive positive correlations with dengue presence were observed with several municipal services such as garbage collection and access to piped water. Risk factors for the increased burden of dengue included poor housing conditions, garbage collection, receipt of remittances, and sharing a property with more than one household. Social factors such as education and household demographics were negatively correlated with increased dengue burden. Our findings elucidate underlying differences with dengue presence and burden and indicate the potential to develop dengue vulnerability and risk maps to inform disease prevention and control - information that is also relevant for emerging epidemics of chikungunya and zika.\n\nHighlightsO_LIIn 2012, Guayaquil, Ecuador had a large outbreak of dengue cases\nC_LIO_LIDengue case presence and burden exhibited spatial heterogeneity at the census block level\nC_LIO_LISocial-ecological drivers of case presence and burden differed in this outbreak, highlighting the need to model both types of epidemiological data\nC_LIO_LIAccess to municipal resources such as garbage collection and piped water had counterintuitive relationships with dengue presence, but poor housing, garbage collection and remittances correlated to dengue burden.\nC_LIO_LIOur findings inform risk mapping and vector control and surveillance allocation, relevant to this and other concurrent emergent epidemics such as chikungunya and zika\nC_LI

epidemiology

Ecological Insights from the Evolutionary History of Microbial Innovations

Bacteria and Archaea represent the base of the evolutionary tree of life and contain the vast majority of phylogenetic and functional diversity. Because these organisms and their traits directly impact ecosystems and human health, a focus on functional traits has become increasingly common in microbial ecology. These trait-based approaches have the potential to link microbial communities and their ecological function. But an open question is how, why, and in what order microorganisms acquired the traits we observe in the present day. To address this, we reconstructed the evolutionary history of microbial traits using genomic data to understand the evolution, selective advantage, and similarity of traits in extant organisms and provide insights into the composition of genomes and communities. We used the geological timeline and physiological expectations to provide independent evidence in support of this evolutionary history. Using this reconstructed evolutionary history, we explored hypotheses related to the composition of genomes. We showed that gene transition rates can be used to make predictions about the size and type of genes in a genome: generalist genomes comprise many evolutionarily labile genes while specialist genomes comprise more highly conserved functional genes. These findings suggest that generalist organisms do not build up and hoard an array of functions, but rather tend to experiment with functions related to environmental sensing, transport, and complex resource degradation. Our results provide a framework for understanding the evolutionary history of extant microorganisms, the origin and maintenanceof traits, and linking evolutionary relatedness and ecological function.

microbiology

Leaps and bounds: geographical and ecological distance constrained the colonisation of the Afrotemperate by Erica

AO_SCPCAPBSTRACTC_SCPCAPThe coincidence of long distance dispersal and biome shift is assumed to be the result of a multifaceted interplay between geographical distance and ecological suitability of source and sink areas. Here, we test the influence of these factors on the dispersal history of the flowering plant genus Erica (Ericaceae) across the Afrotemperate. We quantify similarity of Erica climate niches per biogeographic area using direct observations of species, and test various colonisation scenarios while estimating ancestral areas for the Erica clade using parametric biogeographic model testing. We infer that the overall dispersal history of Erica across the Afrotemperate is the result of infrequent colonisation limited by geographic proximity and niche similarity. However, the Drakensberg Mountains represent a colonisation sink, rather than acting as a \"stepping stone\" between more distant and ecologically dissimilar Cape and Tropical African regions. Strikingly, the most dramatic examples of species radiations in Erica were the result of single unique dispersals over longer distances between ecologically dissimilar areas, contradicting the rule of phylogenetic biome conservatism. These results highlight the importance of rare biome shifts, in which a unique dispersal event fuels evolutionary radiation.\n\nThis article has been peer-reviewed and recommended by: Peer Community in Evolutionary Biology (DOI: 10.24072/pci.evolbiol.100065)

evolutionary biology

Synthetic methanogenic communities reveal differential impact of ecological perturbations on aceto- and hydrogeno-trophic methanogens

Synthetic microbial communities provide reduced microbial ecologies that can be studied under defined conditions. Here, we use this approach to study the interactions underpinning anaerobic digestion communities and involving the key microbial populations of a sulfate reducer (Desulfovibrio vulgaris), and aceto-(Methanosarcina barkeri) and hydrogenotrophic (Methanococcus maripaludis) methanogens. We create all possible mixed culture combinations of these species and analyse the stability and productivity of each system over multiple sub-culturings and under different sulfate levels, mimicking ecological perturbation in the form of strong electron acceptor availability. We find that all three species can co-exist in the absence of sulfate, and that system productivity (in form of methane production from lactate) increases by almost two-fold compared to co-cultures. With increasing sulfate availability, co-existence is perturbed and both methanogenic populations display a diminishing trend. Interestingly, we find that, despite the continued presence of acetate in the system, the acetotrophic methanogens are more readily disrupted by sulfate perturbation. We show that this is due to a shift in M. barkeri metabolism towards increased co-utilisation of hydrogen with acetate, which we verified through experiments on mono cultures and mass balance calculations in co-cultures. We conclude that hydrogen is a key factor for both hydrogeno- and aceto-trophic methanogenesis and can influence these populations differentially under the common ecological perturbation of strong electron acceptor availability. These findings will help engineering of larger synthetic communities for specific applications in biodegradation and understanding complex anaerobic digestion communities found in animal guts, sediments, and bioreactors.

synthetic biology

High impact journals in ecology cover proportionally more statistically significant findings

Unbiased scientific reporting is crucial for data and research synthesis. Previous studies suggest that statistically significant results are more likely to be published and more likely to be submitted to high impact journals. However, the most recent research on statistical significance in relation to journal impact factors in ecological research was published more than two decades ago or addressed a small subset of the literature. Here, we extract p-values from all articles published in 11 journals in 2012 and 2014 across a wide range of impact factors with six journals sampled in both years. Our results indicate that the proportion of statistically significant results increases with rising impact factor. Such a trend can have important consequences for syntheses of ecological data and it highlights the importance of covering a wide range of impact factors when identifying published studies for data syntheses. This trend can also lead to a biased understanding of the probability of true effects in ecology and conservation. We caution against the possible downplaying of non-significant results by either journals or authors.

scientific communication and education

Using molecular ecological network analysis to explore the effects of chemotherapy on intestinal microbial communities of colorectal cancer patients

Intestinal microbiota is now widely known to be key roles in the nutrition uptake, metabolism, and the regulation of human immune responses. However, we do not know how changes the intestinal microbiota in response to the chemotherapy. In this study, we used network-based analytical approaches to explore the effects of five stages of chemotherapy on the intestinal microbiota of colorectal cancer patients. The results showed that chemotherapy greatly reduced the alpha diversity and changed the specie-specie interaction networks of intestinal microbiota, proved by the network size, network connectivity and modularity. The OTU167 and OTU8 from the genus Fusobacterium and Bacteroides were identified as keystone taxa by molecular ecological networks in the first two stages of chemotherapy, and were significantly correlated with tumor makers (P < 0.05). Five stages of chemotherapy did not make the intestinal micro-ecosystem regain a steady state, because of the lower alpha diversity and more complicated ecological networks compared to the healthy individuals. Furthermore, combing the changes of ecological networks with the tumor markers, the intestinal microbiota was closely linked with clinical chemotherapeutic effects.\n\nImportanceA deeply understanding of the role of intestinal microbiota contributes to help us find path forward for improving the prognosis of colorectal cancer patients. In addition, diet or probiotics interventions will be a possible attempt to improve the clinical chemotherapeutic effects for colorectal cancer patients.

microbiology

Distinct Microbes, Metabolites, and Ecologies Define the Microbiome in Deficient and Proficient Mismatch Repair Colorectal Cancers

Background\n\nThe link between colorectal cancer (CRC) and the gut microbiome has been established, but the specific microbial species and their role in carcinogenesis remain controversial. Our understanding would be enhanced by better accounting for tumor subtype, microbial community interactions, metabolism, and ecology.\n\nMethods\n\nWe collected paired colon tumor and normal-adjacent tissue and mucosa samples from 83 individuals who underwent partial or total colectomies for CRC. Mismatch repair (MMR) status was determined in each tumor sample and classified as either deficient MMR (dMMR) or proficient MMR (pMMR) tumor subtypes. Samples underwent 16S rRNA gene sequencing and a subset of samples from 50 individuals were submitted for targeted metabolomic analysis to quantify amino acids and short-chain fatty acids. A PERMANOVA was used to identify the biological variables that explained variance within the microbial communities. dMMR and pMMR microbial communities were then analyzed separately using a generalized linear mixed effects model that accounted for MMR status, sample location, intra-subject sample correlation, and read depth. Genome-scale metabolic models were then used to generate microbial interaction networks for dMMR and pMMR microbial communities. We assessed global network properties as well as the metabolic influence of each microbe within the dMMR and pMMR networks.\n\nResults\n\nWe demonstrate distinct roles for microbes in dMMR and pMMR CRC. Sulfidogenic Fusobacterium nucleatum and hydrogen sulfide production were significantly enriched in dMMR CRC, but not pMMR CRC. We also surveyed the butyrate-producing microbial species, but did not find a significant difference in predicted or actual butyrate production between dMMR and pMMR microbial communities. Finally, we observed that dMMR microbial communities were predicted to be less stable than pMMR microbial communities. Community stability may play an important role in CRC development, progression, or immune activation within the respective MMR subtypes.\n\nConclusions\n\nIntegrating tumor biology and microbial ecology highlighted distinct microbial, metabolic, and ecological properties unique to dMMR and pMMR CRC. This approach could critically improve our ability to define, predict, prevent, and treat colorectal cancers.

cancer biology

The ecological cocktail party: Measuring brain activity during an auditory oddball task with background noise

Most experiments using EEG recordings take place in highly isolated and restricted environments, limiting their applicability to real-life scenarios. New technologies for mobile EEG are changing this by allowing EEG recording to take place outside of the laboratory. However, before results from experiments performed outside the laboratory can be fully understood, the effects of ecological stimuli on brain activity during cognitive tasks must be examined. In this experiment, participants performed an auditory oddball task while also listening to concurrent background noises of silence, white noise and outdoor ecological sounds, as well as a condition in which the tones themselves were at a low volume. We found a significantly increased N1 and decreased P2 when participants performed the task with outdoor sounds and white noise in the background, with the largest differences in the outdoor sound condition. This modulation in the N1 and P2 replicates what we have previously found outside while people ride bicycles (Scanlon et al., 2017). No behavioural differences were found in response to the target tones. We interpret these modulations in early ERPs as indicative of sensory filtering of background sounds, and that ecologically valid sounds require more filtering than synthetic sounds. Our results reveal that much of what we understand about the brain will need to be updated as we step outside the lab.

neuroscience

Molecular noise shapes bacteria-phage ecologies

Mathematical models have been used successfully at diverse scales of biological organization, ranging from ecology and population dynamics to stochastic reaction events occurring between individual molecules in single cells. Generally, many biological processes unfold across multiple scales, with mutations being the best studied example of how stochasticity at the molecular scale can influence outcomes at the population scale. In many other contexts, however, an analogous link between micro- and macro-scale remains elusive, primarily due to the challenges involved in setting up and analyzing multi-scale models. Here, we employ such a model to investigate how stochasticity propagates from individual biochemical reaction events in the bacterial innate immune system to the ecology of bacteria and bacterial viruses. We show analytically how the dynamics of bacterial populations are shaped by the activities of immunity-conferring enzymes in single cells and how the ecological consequences imply optimal bacterial defense strategies against viruses. Our results suggest that bacterial populations in the presence of viruses can either optimize their initial growth rate or their steady state population size, with the first strategy favoring simple and the second strategy favoring complex bacterial innate immunity.

biophysics

Emergence of social inequality in a spatial-ecological public goods game

Spatial ecological public goods, such as forests, grasslands, and fish stocks risk being overexploited by selfish consumers, a phenomenon called \"the tragedy of commons\". The spatial and ecological dimensions introduce new features absent in non spatio-ecological contexts, such as consumer mobility, incomplete information availability, and rapid evolution by social learning. It is unclear how these different processes interact to influence the harvesting and dispersal strategies of consumers. To answer these questions, we develop and analyze an individual-based, spatially-structured evolutionary model with explicit resource dynamics. We find that, 1) When harvesting efficiency is low, consumers evolve a sedentary harvesting strategy, with which resources are harvested sustainably, but harvesting rates remain far below their maximum sustainable value. 2) As harvesting efficiency increases, consumers adopt a mobile consume-and-disperse strategy, which is sustainable, equitable, and allows for maximum sustainable yield. 3) Further increase in harvesting efficiency leads to large-scale overexploitation. 4) If costs of dispersal are significant, increased harvesting efficiency also leads to social inequality between frugal sedentary consumers and overexploitative mobile consumers. Whereas overexploitation can occur without social inequality, social inequality always leads to overexploitation. Thus, we identify four conditions, which are characteristic (and as such positive) features of modern societies resulting from technological progress, but also risk promoting social inequality and unsustainable resource use: high harvesting efficiency, moderately low costs of dispersal, high consumer density, and consumers tendency to rapidly adopt new strategies. We also show that access to global information, which is also a feature of modern societies, may help mitigate these risks.

evolutionary biology

The ecology of sexual conflict: behaviorally plastic responses to temperature variation in the social environment can drastically modulate male harm to females.

Sexual conflict is a fundamental driver of male/female adaptations, an engine of biodiversity, and a crucial determinant of population viability. For example, sexual conflict frequently leads to behavioural adaptations that allow males to displace their rivals, but in doing so harm those same females they are competing to access. Sexual conflict via male harm hence not only deviates females from their fitness optimum, but can decrease population viability and facilitate extinction. Despite this prominent role, we are far from understanding what factors modulate the intensity of sexual conflict, and particularly the role of ecology in mediating underlying behavioural adaptations. In this study we show that, in Drosophila melanogaster, variations in environmental temperature of {+/-}4[Formula]C (within the natural range in the wild) decrease male harm impact on female fitness by between 45-73%. Rate-sensitive fitness estimates indicate that such modulation results in an average rescue of population productivity of 7% at colder temperatures and 23% at hotter temperatures. Our results: a) show that the thermal ecology of social interactions can drastically modulate male harm via behaviourally plasticity, b) identify a potentially crucial ecological factor to understand how sexual conflict operates in nature, and c) suggest that behaviourally plastic responses can lessen the negative effect of sexual conflict on population viability in the face of rapid environmental temperature changes.

evolutionary biology

Loci, genes, and gene networks associated with life history variation in a model ecological organism, Daphnia pulex (complex)

BackgroundIdentifying the molecular basis of heritable variation provides insight into the underlying mechanisms generating phenotypic variation and the evolutionary history of organismal traits. Life history trait variation is of central importance to ecological and evolutionary dynamics, and contemporary genomic tools permit studies of the basis of this variation in non-genetic model organisms. We used high density genotyping, RNA-Seq gene expression assays, and detailed phenotyping of fourteen ecologically important life history traits in a wild-caught panel of 32 Daphnia pulex clones to explore the molecular basis of trait variation in a model ecological species.\n\nResultsWe found extensive phenotypic and a range of heritable genetic variation (~0 < H2 < 0.44) in the panel, and accordingly identify 75-261 genes--organized in 3-6 coexpression modules--associated with genetic variation in each trait. The trait-related coexpression modules possess well-supported promoter motifs, and in conjunction with marker variation at trans- loci, suggest a relatively small number of important expression regulators. We further identify a candidate genetic network with SNPs in eight known transcriptional regulators, and dozens of differentially expressed genes, associated with life history variation. The gene-trait associations include numerous un-annotated genes, but also support several a priori hypotheses, including an ecdysone-induced protein and several Gene Ontology pathways.\n\nConclusionThe genetic and gene expression architecture of Daphnia life history traits is complex, and our results provide numerous candidate loci, genes, and coexpression modules to be tested as the molecular mechanisms that underlie Daphnia eco-evolutionary dynamics.

genomics

Parent-offspring conflict, ecology, and life history diversification of livebearing fishes

Shifts in life history evolution can potentiate sexual selection and speciation. However, we rarely understand the causative links between correlated patterns of diversification or the tipping points that initiate changes with cascading effects. We investigated livebearing fishes with repeated transitions from pre- (lecithotrophy) to post-fertilization maternal provisioning (matrotrophy) to identify the potential ecological drivers of evolutionary transitions in life history. Phylogenetic comparative analyses across 94 species revealed that bi-directional evolution along the lecithotrophy-matrotrophy continuum is correlated with ecology, supporting adaptive hypotheses of life history diversification. Consistent with theory, matrotrophy was associated with high resource availability and low competition. Our results suggest that ecological sources of selection contribute to the diversification of female provisioning strategies in livebearing fishes, which have been associated with macroevolutionary patterns of sexual selection and speciation.

evolutionary biology

Beyond species: why ecological interaction networks vary through space and time

Community ecology is tasked with the considerable challenge of predicting the structure, and properties, of emerging ecosystems. It requires the ability to understand how and why species interact, as this will allow the development of mechanism-based predictive models, and as such to better characterize how ecological mechanisms act locally on the existence of interspecific interactions. Here we argue that the current conceptualization of species interaction networks is ill-suited for this task. Instead, we propose that future research must start to account for the intrinsic variability of species interactions, then scale up from here onto complex networks. This can be accomplished simply by recognizing that there exists intra-specific variability, in traits or properties related to the establishment of species interactions. By shifting the scale towards population-based processes, we show that this new approach will improve our predictive ability and mechanistic understanding of how species interact over large spatial or temporal scales.

Ecology

Exploring the spatially explicit predictions of the Maximum Entropy Theory of Ecology

AimThe Maximum Entropy Theory of Ecology (METE) is a unified theory of biodiversity that attempts to simultaneously predict patterns of species abundance, size, and spatial structure. The spatial predictions of this theory have repeatedly performed well at predicting diversity patterns across scales. However, the theoretical development and evaluation of METE has focused on predicting patterns that ignore inter-site spatial correlations. As a result the theory has not been evaluated using one of the core components of spatial structure. We develop and test a semi-recursive version of METEs spatially explicit predictions for the distance decay relationship of community similarity and compare METEs performance to the classic random placement model of completely random species distributions. This provides a better understanding and stronger test of METEs spatial community predictions.\n\nLocationNew world tropical and temperate plant communities.\n\nMethodsWe analytically derived and simulated METEs spatially explicit expectations for the Sorensen index of community similarity. We then compared the distance decay of community similarity of 16 mapped plant communities to METE and the random placement model.\n\nResultsThe version of METE we examined was successful at capturing the general functional form of empirical distance decay relationships, a negative power function relationship between community similarity and distance. However, the semi-recursive approach consistently over-predicted the degree and rate of species turnover and yielded worse predictions than the random placement model.\n\nMain conclusionsOur results suggest that while METEs current spatial models accurately predict the spatial scaling of species occupancy, and therefore core ecological patterns like the species-area relationship, its semi-recursive form does not accurately characterize spatially-explicit patterns of correlation. More generally, this suggests that tests of spatial theories based only on the species-area relationship may appear to support the underlying theory despite significant deviations in important aspects of spatial structure.

Ecology

THE REGIME SHIFTS DATABASE: A FRAMEWORK FOR ANALYZING REGIME SHIFTS IN SOCIAL-ECOLOGICAL SYSTEMS

This paper presents the Regime Shifts Database (RSDB), a new online, open-access database that uses a novel consistent framework to systematically analyze regime shifts based on their impacts, key drivers, underlying feedbacks, and management options. The database currently contains 27 generic types of regime shifts, and over 300 specific case studies of a variety of regime shifts. These regime shifts occur across diverse types of systems and are driven by many different types of processes. Besides impacting provisioning and regulating services, our work shows that regime shifts substantially impact cultural and aesthetic ecosystem services. We found that social-ecological feedbacks are difficult to characterize and more work is needed to develop new tools and approaches to better understand social-ecological regime shifts. We hope that the database will stimulate further research on regime shifts and make available information that can be used in management, planning and assessment.

Ecology

Effect of Localization on the Stability of Mutualistic Ecological Networks

The relationships between the core-periphery architecture of the species interaction network and the mechanisms ensuring the stability in mutualistic ecological communities are still unclear. In particular, most studies have focused their attention on asymptotic resilience or persistence, neglecting how perturbations propagate through the system. Here we develop a theoretical framework to evaluate the relationship between architecture of the interaction networks and the impact of perturbations by studying localization, a measure describing the ability of the perturbation to propagate through the network. We show that mutualistic ecological communities are localized, and localization reduces perturbation propagation and attenuates its impact on species abundance. Localization depends on the topology of the interaction networks, and it positively correlates with the variance of the weighted degree distribution, a signature of the network topological hetereogenity. Our results provide a different perspective on the interplay between the architecture of interaction networks in mutualistic communities and their stability.

Ecology

Novel Covariance-Based Neutrality Test of Time-Series Data Reveals Asymmetries in Ecological and Economic Systems

Systems as diverse as the interacting species in a community, alleles at a genetic locus, and companies in a market are characterized by competition (over resources, space, capital, etc) and adaptation. Neutral theory, built around the hypothesis that individual performance is independent of group membership, has found utility across the disciplines of ecology, population genetics, and economics, both because of the success of the neutral hypothesis in predicting system properties and because deviations from these predictions provide information about the underlying dynamics. However, most tests of neutrality are weak, based on static system properties such as species-abundance distributions or the number of singletons in a sample. Time-series data provide a window onto a systems dynamics, and should furnish tests of the neutral hypothesis that are more powerful to detect deviations from neutrality and more informative about to the type of competitive asymmetry that drives the deviation.\n\nHere, we present a neutrality test for time-series data. We apply this test to several microbial time-series and financial time-series and find that most of these systems are not neutral. Our test isolates the covariance structure of neutral competition, thus facilitating further exploration of the nature of asymmetry in the covariance structure of competitive systems. Much like neutrality tests from population genetics that use relative abundance distributions have enabled researchers to scan entire genomes for genes under selection, we anticipate our time-series test will be useful for quick significance tests of neutrality across a range of ecological, economic, and sociological systems for which time-series data are available. Future work can use our test to categorize and compare the dynamic fingerprints of particular competitive asymmetries (frequency dependence, volatility smiles, etc) to improve forecasting and management of complex adaptive systems.\n\nAuthor SummaryFrom fisheries and forestries to game parks and gut microbes, managing a community of organisms is much like managing a portfolio. Managers care about diversity, and calculations of risk - for extinction or financial ruin - require accurate models of the covariance between the parts of the portfolio.\n\nTo model the covariances in portfolios or communities, it helps to start simple with a null model assuming the equivalence of species or companies relative to one another (termed \"neutrality\") and letting the data suggest otherwise. Researchers in biology and finance have independently entertained and tested neutral models, but the existing tests have used snapshots of communities or the variance of fluctuations of individual populations, whereas tests of the covariances between species can better inform the development of alternative models.\n\nWe develop a covariance-based neutrality test for time-series data and use it to show that the human microbiome, North American birds, and companies in the S&P 500 all have a similar deviation from neutrality. Understanding and incorporating this non-neutral covariance structure can yield more accurate alternative models of community dynamics which can improve our management of \"portfolios\" of multi-species systems.

Ecology