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bioRxiv2017

Explorations of the polygenic genetic architecture of flowering time in the worldwide Arabidopsis thaliana population

As a locally adapted complex trait, flowering time in Arabidopsis thaliana has attracted much attention in genetics. Most studies have, however, focused on contributions by individual loci rather than the joint contributions by the large number of loci in the genetic architecture of flowering time to local and global adaptation. In an earlier study, we reported 46 loci associated with flowering time variation during growth at 10{degrees}C, 16{degrees}C or both in the 1,001-genomes collection of Arabidopsis thaliana accessions. Here, we explore how these loci together contribute to differences among genetically defined, and geographically divided, subpopulations across the native range of this species. Our approach was to define flowering time as a trait, and the measurements at 10 and 16 {degrees}C as two independent measurements of it. This facilitated explorations of the dynamics in the genetic architecture -which loci contribute and their effects- of flowering time across growth temperatures and their potential roles in local and global adaptation. The overall flowering time differences between populations could be explained by subtle changes in allele-frequencies and gradual changes in phenotype due to globally present alleles. More extreme local adaptations were on several occasions due to contributions by regional alleles with relatively large effects. About 2/3 of the 48 evaluated flowering time loci had similar effects on flowering time at 10{degrees}C and 16{degrees}C, while the remaining 1/3 had different effects in the two temperatures, suggesting an important contribution of gene by temperature interactions to this trait. There are also indications that co-evolution of functionally connected alleles in local populations has been important for local adaptation. Overall, this study provides deeper insights to the polygenic genetic basis of flowering time variation in Arabidopsis thaliana across a wide range of ecological habitats.\n\nAuthor SummaryMany genes can affect flowering time in Arabidopsis thaliana, but their contribution to natural flowering time variation in the worldwide population is largely unknown. We explored how 48 loci associated with flowering time, measured at 10{degrees}C and 16{degrees}C, or their difference, for the same wild collected 1,001-genomes Arabidopsis thaliana accessions together contribute to differences among the genetically defined and geographically divided subpopulations from the native species range. The overall flowering time differences among these subpopulations could be explained by the joint small effects of globally present alleles, suggesting an important contribution by polygenic adaptation for this trait. Most alleles with large effects on flowering were present only in some populations, facilitating more extreme local adaptations. Long-range LD was observed between genes in several biological pathways, indicating possible local adaptation via co-evolution of functionally connected polymorphisms. The genetic architecture of flowering time was also found to depend on the growth temperature. Most flowering time loci had similar effects on flowering time measured at 10{degrees}C and 16{degrees}C, but the effects of about 1/3 of them had effects that varied with temperature. Overall, new insights are provided to how the polygenic architecture of flowering time has facilitated its colonisation of a wide range of ecological habitats.

genetics↗

bioRxiv2017

Evolutionary dynamics of bacteria in the gut microbiome within and across hosts

Gut microbiota are shaped by a combination of ecological and evolutionary forces. While the ecological dynamics have been extensively studied, much less is known about how species of gut bacteria evolve over time. Here we introduce a model-based framework for quantifying evolutionary dynamics within and across hosts using a panel of metagenomic samples. We use this approach to study evolution in [~]30 prevalent species in the human gut. Although the patterns of between-host diversity are consistent with quasi-sexual evolution and purifying selection on long timescales, we identify new genealogical signatures that challenge standard population genetic models of these processes. Within hosts, we find that genetic differences that accumulate over [~]6 month timescales are only rarely attributable to replacement by distantly related strains. Instead, the resident strains more commonly acquire a smaller number of putative evolutionary changes, in which nucleotide variants or gene gains or losses rapidly sweep to high frequency. By comparing these mutations with the typical between-host differences, we find evidence that some sweeps are seeded by recombination, in addition to new mutations. However, comparisons of adult twins suggest that replacement eventually overwhelms evolution over multi-decade timescales, hinting at fundamental limits to the extent of local adaptation. Together, our results suggest that gut bacteria can evolve on human-relevant timescales, and they highlight the connections between these short-term evolutionary dynamics and longer-term evolution across hosts.

evolutionary biology↗

bioRxiv2017

Kombucha as a model system for multispecies microbial cooperation: theoretical promise, methodological challenges and new solutions ‘in solution’

Kombucha is a sweetened tea fermented by bacteria and yeast into a carbonated, acidic drink, producing a surface biofilm pellicle (colloquially called a SCOBY) during the process. Typically, liquid and a biofilm pellicle from a previously fermented culture is used as a starter for new cultures; however, there is no standard protocol for growing kombucha in the laboratory. In order to establish a standard protocol with low variability between replicates, we tested whether we could begin a kombucha culture with only well-mixed liquid stock. We found that viable kombucha cultures can be grown from low percentages of initial inoculum stock liquid, that new pellicles can form from liquid alone (with no starter pellicle), and that the variation in the pellicle characteristics is lower when only a liquid starter is used (p = 0.0004). We also found that blending the pellicle before including it significantly reduces the variation among replicates, though the final pellicle was abnormal. We conclude that growing kombucha from only liquid stock is viable and provides a greater degree of experimental control and reproducibility compared to alternatives. Standardizing methodologies for studying kombucha in the lab can facilitate the use of this system for exploring questions about the evolutionary, ecological and cooperative/competitive dynamics within this multi-species system including resource transfers, functional dependence, genetic divergence, collective defense, and ecological succession. A better understanding of kombucha and other fermented foods may eventually allow us to leverage their pathogen inhibitory properties to develop novel antibiotics and bacteriocins.

microbiology↗

bioRxiv2017

The kinetoplastid-infecting Bodo saltans virus (BsV), a window into the most abundant giant viruses in the sea

Giant viruses are ecologically important players in aquatic ecosystems that have challenged concepts of what constitutes a virus. Herein, we present the giant Bodo saltans virus (BsV), the first characterized representative of the most abundant giant viruses in the oceans, and the first klosneuvirus isolate, a subgroup of the Mimiviridae proposed from metagenomic data. BsV infects an ecologically important microzooplankton, the kinetoplastid Bodo saltans. Its 1.39 Mb genome is the largest described for the Mimiviridae and encodes 1227 predicted ORFs, including pathways for host-independent replication. Yet, much of its translational machinery has been lost, including all tRNAs. Essential genes are invaded by homing endonuclease-encoding self-splicing introns that may defend against competing viruses. Putative anti-host factors show extensive gene duplication via a genomic accordion indicating an ongoing evolutionary arms race and highlighting the rapid evolution and genomic plasticity that has led to genome gigantism and the enigma that is giant viruses.

genomics↗

bioRxiv2017

Dynamics of finely resolved, abundant symbiotic marine plankton and other interacting microbes via automated high-frequency sampling

Short time-scale observations are valuable for understanding microbial ecological processes. We assessed dynamics in relative abundance and potential activities by sequencing the small sub-unit ribosomal RNA gene (rRNA gene) and rRNA molecules (rRNA) of Bacteria, Archaea, and Eukaryota once to twice-daily between March 2014 and May 2014 from the surface ocean off Catalina Island, California. Typically Ostreococcus, Braarudosphaera, Teleaulax, and Synechococcus dominated phytoplankton sequences (including chloroplasts) while SAR11, Sulfitobacter, and Fluviicola dominated non-phytoplankton Bacteria and Archaea. We observed short-lived increases of diatoms, mostly Pseudo-nitzschia and Chaetoceros, with quickly responding Bacteria and Archaea including Flavobacteriaceae (Polaribacter & Formosa), Roseovarius, and Euryarchaeota (MGII), notably the exact amplicon sequence variants we observed responding similarly to another diatom bloom nearby, three years prior. We observed correlations representing known interactions among abundant phytoplankton rRNA sequences, demonstrating the biogeochemical and ecological relevance of such interactions: 1) The kleptochloroplastidic ciliate Mesodinium 18S rRNA gene sequences and a single Teleaulax taxon (via 16S rRNA gene sequences) were correlated (Spearman r =0.83) yet uncorrelated to a Teleaulax 18S rRNA gene OTU, or any other taxon (consistent with a kleptochloroplastidic or karyoklepty relationship) and 2) the photosynthetic prymnesiophyte Braarudosphaera bigelowii and two strains of diazotrophic cyanobacterium UCYN-A were correlated and each taxon was also correlated to other taxa, including B. bigelowii to a verrucomicrobium and a dictyochophyte phytoplankter (all r > 0.8). We also report strong correlations (r > 0.7) between various ciliates, bacteria, and phytoplankton, suggesting interactions via currently unknown mechanisms. These data reiterate the utility of high-frequency time-series to show rapid microbial reactions to stimuli, and provide new information about in-situ dynamics of previously recognized and hypothesized interactions.

microbiology↗

bioRxiv2017

Climatic influence on the anthrax niche in warming northern latitudes

Climate change is impacting ecosystem structure and function, with potentially drastic downstream effects on human and animal health. Emerging zoonotic diseases are expected to be particularly vulnerable to climate and biodiversity disturbance. Anthrax is an archetypal zoonosis that manifests its most significant burden on vulnerable pastoralist communities. The current study sought to investigate the influence of temperature increases on the landscape suitability of anthrax in the temperate, boreal, and arctic North, where observed climate impact has been rapid. This study also explored the influence of climate relative to more traditional factors, such as livestock distribution, ungulate biodiversity, and soil-water balance, in demarcating high risk landscapes. Machine learning was used to model landscape suitability as the ecological niche of anthrax in northern latitudes. The model identified climate, livestock density and wild ungulate species richness as the most influential landscape features in predicting suitability. These findings highlight the significance of warming temperatures for anthrax ecology in northern latitudes, and suggest potential mitigating effects of interventions targeting megafauna biodiversity conservation in grassland ecosystems, and animal health promotion among small to midsize livestock herds.\n\nSignificance StatementWe present evidence that a warming climate may be associated with the current distribution of anthrax risk in the temperate, boreal, and arctic North. Moreover, projected warming over the coming decades was associated with substantive expansion of this risk. In addition, livestock distribution, ungulate biodiversity, and soil-water balance were also influential to anthrax risk. While these results are sobering for the future health of livestock and pastoralist communities in the northern latitudes, the coincident modulating effect of ungulate biodiversity may suggest targeted ecosystem conservation as a possible buffer against a growing anthrax niche.

epidemiology↗

bioRxiv2017

Timing of host feeding drives rhythms in parasite replication

Circadian rhythms enable organisms to synchronise the processes underpinning survival and reproduction to anticipate daily changes in the external environment. Recent work shows that daily (circadian) rhythms also enable parasites to maximise fitness in the context of ecological interactions with their hosts. Because parasite rhythms matter for their fitness, understanding how they are regulated could lead to innovative ways to reduce the severity and spread of diseases. Here, we examine how host circadian rhythms influence rhythms in the asexual replication of malaria parasites. Asexual replication is responsible for the severity of malaria and fuels transmission of the disease, yet, how parasite rhythms are driven remains a mystery. We perturbed feeding rhythms of hosts by 12 hours (i.e. diurnal feeding in nocturnal mice) to desynchronise the hosts peripheral oscillators from the central, light-entrained oscillator in the brain and their rhythmic outputs. We demonstrate that the rhythms of rodent malaria parasites in day-fed hosts become inverted relative to the rhythms of parasites in night-fed hosts. Our results reveal that the hosts peripheral rhythms (associated with the timing of feeding and metabolism), but not rhythms driven by the central, light-entrained circadian oscillator in the brain, determine the timing (phase) of parasite rhythms. Further investigation reveals that parasite rhythms correlate closely with blood glucose rhythms. In addition, we show that parasite rhythms resynchronise to the altered host feeding rhythms when food availability is shifted, which is not mediated through rhythms in the host immune system. Our observations suggest that parasites actively control their developmental rhythms. Finally, counter to expectation, the severity of disease symptoms expressed by hosts was not affected by desynchronisation of their central and peripheral rhythms. Our study at the intersection of disease ecology and chronobiology opens up a new arena for studying host-parasite-vector coevolution and has broad implications for applied bioscience.\n\nAuthor summaryHow cycles of asexual replication by malaria parasites are coordinated to occur in synchrony with the circadian rhythms of the host is a long-standing mystery. We reveal that rhythms associated with the time-of-day that hosts feed are responsible for the timing of rhythms in parasite development. Specifically, we altered host feeding time to phase-shift peripheral rhythms, whilst leaving rhythms driven by the central circadian oscillator in the brain unchanged. We found that parasite developmental rhythms remained synchronous but changed their phase, by 12 hours, to follow the timing of host feeding. Furthermore, our results suggest that parasites themselves schedule rhythms in their replication to coordinate with rhythms in glucose in the hosts blood, rather than have rhythms imposed upon them by, for example, host immune responses. Our findings reveal a novel relationship between hosts and parasites that if disrupted, could reduce both the severity and transmission of malaria infection.

microbiology↗

bioRxiv2017

Speciation in sympatry with ongoing secondary gene flow and an olfactory trigger in a radiation of Cameroon cichlids

Whether speciation can happen in the absence of geographical barriers and if so, under which conditions, is a fundamental question in our understanding of the evolution of new species. Among candidates for sympatric speciation, Cameroon crater lake cichlid radiations have been considered the most compelling. However, it was recently shown that a more complex scenario than a single colonization followed by isolation underlies these radiations. Here, we perform a detailed investigation of the speciation history of a radiation of Coptodon cichlids from Lake Ejagham using whole-genome sequencing data. The existence of the Lake Ejagham Coptodon radiation is remarkable since this 0.5 km2 lake offers limited scope for divergence across a shallow depth gradient, disruptive selection is weak, the species are sexually monochromatic, yet assortative mating is strong. We infer that Lake Ejagham was colonized by Coptodon cichlids almost as soon as it came into existence 9,000 years ago, yet speciation events occurred only in the last 1,000-2,000 years. We show that secondary gene flow from a nearby riverine species has been ongoing, into ancestral as well as extant Lake Ejagham lineages, and we identify and date river-to-lake admixture blocks. One of these contains a cluster of olfactory receptor genes that introgressed close to the time of the first speciation event and coincides with a higher overall rate of admixture into the recipient lineages. Olfactory signaling is a key component of mate choice and species recognition in cichlids. A functional role for this introgression event is consistent with previous findings that assortative mating appears much stronger than ecological divergence in Ejagham Coptodon. We conclude that speciation in this radiation took place in sympatry, yet may have benefited from ongoing riverine gene flow.\n\nAuthor SummaryDespite an active search for empirical examples and much theoretical work, sympatric speciation remains one of the most controversial ideas in evolutionary biology. While a host of examples have been described in the last few decades, more recent results have shown that several of the most convincing systems have not evolved in complete isolation from allopatric populations after all. By itself, documenting the occurrence of secondary gene flow is not sufficient to reject the hypothesis of sympatric speciation, since speciation can still be considered sympatric if gene flow did not contribute significantly to the build-up of reproductive isolation. One way forward is to use genomic data to infer where, when and into which lineages gene flow occurred, and identify the regions of the genome that experienced admixture. In this study, we use whole-genome sequencing to examine one of the cichlid radiations from a small isolated Cameroon lake, which have long been the flagship example of sympatric speciation. We show that gene flow from a riverine species into the lake has been ongoing during the history of the radiation. In line with this, we infer that the lake was colonized very soon after it was formed, and argue that Lake Ejagham is not as isolated as previously assumed. The magnitude of secondary gene flow was relatively even across Lake Ejagham lineages, yet with some evidence for differential admixture, most notably before the first speciation event into the C. deckerti and C. ejagham lineage. Among the sequences that were introgressed into this lineage is a cluster of olfactory receptor genes, which may have facilitated speciation by promoting sexual isolation between incipient species, consistent with previous findings that sexual isolation appears to be stronger than ecological isolation in Ejagham Coptodon. We conclude that speciation in this radiation took place in sympatry, yet may have benefited from ongoing riverine gene flow.

evolutionary biology↗

bioRxiv2017

First genome-wide analysis of an endangered lichen reveals isolation by distance and strong population structure

Lichenized fungi are evolutionarily diverse and ecologically important, but little is known about the processes driving diversification and genetic differentiation in these lineages. Though few studies have examined population genetic patterns in lichens, their geographic distributions are often assumed to be wholly shaped by ecological requirements rather than dispersal limitations. Furthermore, while their reproductive structures are observable, the lack of information about recombination mechanisms and rates can make inferences about reproductive strategies difficult. Here we investigate the population genomics of Cetradonia linearis, an endangered lichen narrowly endemic to the southern Appalachians of eastern North America, to test the relative contributions of environmental factors and geographic distance in shaping genetic structure, and to gain insights into the demography and reproductive biology of range restricted fungi. Analysis of genome-wide SNP data indicated strong evidence for both low rates of recombination and for strong isolation by distance, but did not support isolation by environment. Hindcast species distribution models and the spatial distribution of genetic diversity also suggested that C. linearis had a larger range during the last glacial maximum, especially in the southern portion of its current extent, consistent with previous findings in other southern Appalachian taxa. These results contribute to our understanding of intrinsic and extrinsic factors shaping genetic diversity and biogeographic patterns in C. linearis, and more broadly, in rare and endangered fungi.

evolutionary biology↗

bioRxiv2018

Strong hybrid male incompatibilities impede the spread of a selfish chromosome between populations of a fly.

Meiotically driving sex chromosomes manipulate gametogenesis to increase their transmission at a cost to the rest of the genome. The intragenomic conflicts they produce have major impacts on the ecology and evolution of their host species. However their ecological dynamics remain poorly understood. Simple population genetic models predict meiotic drivers will rapidly reach fixation in a population and spread across a landscape. In contrast, natural populations commonly show spatial variation in the frequency of drivers, with drive present in clines or mosaics across species ranges. For example, Drosophila subobscura harbours a Sex Ratio distorting drive chromosome (\"SRs\") at 15-25% frequency in North Africa, present at less than 2% frequency in adjacent Southern Spain and absent in other European populations. Here, we investigate the forces preventing the spread of the driver northward. We show that SRs has remained at a constant frequency in North Africa, and failed to spread in Spain. We find strong evidence in favour of our first hypothesis, genetic incompatibility between SRs and Spanish autosomal background. When we cross SRs from North Africa onto Spanish genetic backgrounds we observe strong SRs specific incompatibilities in hybrids. The incompatibilities increase in severity in F2 male hybrids, leading to almost complete infertility. We find no evidence supporting a second hypothesis, that there is resistance to drive in Spanish populations. We conclude that the source of the stepped frequency variation is genetic incompatibility between the SRs chromosome and the genetic backgrounds of the adjacent population, preventing SRs spreading northward. The low frequency of SRs in South Spain is consistent with recurrent gene flow across the Strait of Gibraltar combined with selection against the SRs element through genetic incompatibility. This demonstrates that incompatibilities between drive chromosomes and naive populations can prevent the spread of drive between populations, at a continental scale.

evolutionary biology↗

bioRxiv2018

Shallow evolutionary divergence between two Andean hummingbirds: Speciation with gene flow?

Ecological speciation can proceed despite genetic interchange when selection counteracts homogeneizing effects of migration. We tested predictions of this divergence-with-gene-flow model in Coeligena helianthea and C. bonapartei, two parapatric Andean hummigbirds with marked plumage divergence. We sequenced neutral markers (mtDNA and nuclear ultra conserved elements) to examine genetic structure and gene flow, and a candidate gene (MC1R) to assess its role underlying divergence in coloration. We also tested the prediction of Glogers rule that darker forms occur in more humid environments, and compared ecomorphological variables to assess adaptive mechanisms potentially promoting divergence. Genetic differentiation between species was very low and coalescent estimates of migration were consistent with divergence with gene flow. MC1R variation was unrelated to phenotypic differences. Species did not differ in macroclimatic niches but were distinct in ecomorphology. Although we reject adaptation to variation in humidity as the cause of divergence, we hypothesize that speciation likely occurred in the face of gene flow, driven by other ecological pressures or by sexual selection. Marked phenotypic divergence with no neutral genetic differentiation is remarkable for Neotropical birds, and makes C. helianthea and C. bonapartei an appropriate system in which to search for the genetic basis of species differences employing genomics.

evolutionary biology↗

bioRxiv2018

Evolution at two time frames: polymorphisms from an ancient singular divergence event fuel contemporary parallel evolution

When species occur in repeated ecologically distinct habitats across their range, adaptation may proceed surprisingly fast and result in parallel evolution. There is increasing evidence that such cases of rapid parallel evolution are fueled by standing genetic variation, but the origin of this genetic variation remains poorly understood. In Pogonus chalceus beetles, short- and long-winged ecotypes have diverged in response to contrasting hydrological regimes and can be repeatedly found along the Atlantic European coast. By analyzing genomic variation across the beetles distribution, we reveal that genomically widespread short-wing selected alleles evolved during a singular divergence event, estimated at ~0.19 Mya. The ancient and differentially selected alleles are currently polymorphic in all populations across the range, allowing for the fast evolution of one ecotype from a small number of random individuals, as low as 5 to 15, of the populations of the other ecotype. Our results suggest that cases of fast parallel ecological divergence might be the result of evolution at two different time frames: divergence in the past, followed by repeated selection on the divergently evolved alleles after admixture. We suggest that this mechanism may be common and potentially further driven by periods of geographic isolation imposed by large-scale environmental changes such as glacial cycles.

evolutionary biology↗

bioRxiv2018

Decomposing parasite fitness in a two-host, two-parasite system reveals the underpinnings of parasite specialization

AO_SCPLOWBSTRACTC_SCPLOWThe ecological specialization of parasites - whether they can obtain high fitness on very few or very many different host species - is a determining feature of their ecology. In order to properly assess specialization, it is imperative to measure parasite fitness across host species; to understand its origins, fitness must be decomposed into the underlying traits. Despite the omnipresence of parasites with multiple hosts, very few studies assess and decompose their specialization in this way. To bridge this gap, we quantified the infectivity, virulence, and transmission rate of two parasites, the horizontally transmitted microsporidians Anostracospora rigaudi and Enterocytospora artemiae, in their natural hosts, the brine shrimp Artemia parthenogenetica and Artemia franciscana. Our results demonstrate that each parasite performs well on one of the two host species (A. rigaudi on A. parthenogenetica, and E. artemiae on A. franciscana), and poorly on the other. This partial specialization is driven by high infectivity and transmission rates in the preferred host, and is associated with maladaptive virulence and large costs of resistance in the other. Our study represents a rare empirical contribution to the study of parasite evolution in multi-host systems, highlighting the negative effects of under- and over-exploitation when adapting to multiple hosts.

evolutionary biology↗

bioRxiv2018

Disentangling eco-evolutionary effects on trait fixation

In population genetics, fixation of traits in a demographically changing population under frequency-independent selection has been extensively analysed. In evolutionary game theory, models of fixation have typically focused on fixed population sizes and frequency-dependent selection. A combination of demographic fluctuations with frequency-dependent interactions such as Lotka-Volterra dynamics has received comparatively little attention. We consider a stochastic, competitive Lotka-Volterra model with higher order interactions between two traits. The emerging individual based model allows for stochastic fluctuations in the frequencies of the two traits and the total population size. We calculate the fixation probability of a trait under differing competition coefficients. This fixation probability resembles qualitatively the deterministic evolutionary dynamics. Furthermore, we partially disentangle the selection effects into their ecological and evolutionary components. We find that changing the evolutionary selection strength also changes the population dynamics and vice versa. Thus, a clean separation of the ecological and evolutionary effects is not possible. The entangled eco-evolutionary processes thus cannot be ignored when determining fixation properties in a co-evolutionary system.

evolutionary biology↗

bioRxiv2018

In situ relationships between microbiota and potential pathobiota in Arabidopsis thaliana

A current challenge in microbial pathogenesis is to identify biological control agents that may prevent and/or limit host invasion by microbial pathogens. In natura, hosts are often infected by multiple pathogens. However, most of the current studies have been performed under laboratory controlled conditions and by taking into account the interaction between a single commensal species and a single pathogenic species. The next step is therefore to explore the relationships between host-microbial communities (microbiota) and microbial members with potential pathogenic behavior (pathobiota) in a realistic ecological context. In the present study, we investigated such relationships within root and leaf associated bacterial communities of 163 ecologically contrasted Arabidopsis thaliana populations sampled across two seasons in South-West of France. In agreement with the theory of the invasion paradox, we observed a significant humped-back relationship between microbiota and pathobiota -diversity that was robust between both seasons and plant organs. In most populations, we also observed a strong dynamics of microbiota composition between seasons. Accordingly, the potential pathobiota composition was explained by combinations of season-specific microbiota OTUs. This result suggests that the potential biomarkers controlling pathogens invasion are highly dynamic.

microbiology↗

bioRxiv2018

Stronger connectivity of the resident gut microbiome lends resistance to invading bacteria

Bacterial infection in the gut is often due to successful invasion of the host microbiome by an introduced pathogen. Ecological theory indicates that resident community members and their interactions should be strong determinants of whether an invading taxon can persist in a community. In the context of the gut microbiome, this suggests colonization resistance against newly introduced bacteria should depend on the instantaneous bacterial community composition within the gut and interactions between these constituent members. Here we develop a mathematical model of how metabolite-dependent biotic interactions between resident bacteria mediate invasion, and find that stronger biotic connectivity from metabolite cross-feeding and competition increases colonization resistance. We then introduce a statistical method for identifying invasive taxa in the human gut, and show empirically that greater connectivity of the resident gut microbiome is related to increased resistance to invading bacteria. Finally, we examined patient outcomes after fecal microbiota transplant (FMT) for recurring Clostridium difficile infection. Patients with lower connectivity of the gut microbiome after treatment were more likely to relapse, experiencing a later infection. Thus, simulation models and data from human subjects support the hypothesis that stronger interactions between bacteria in the gut repel invaders. These results demonstrate how ecological invasion theory can be applied to the gut microbiome, which might inform targeted microbiome manipulations and interventions. More broadly, this study provides evidence that low connectivity in gut microbial communities is a hallmark of community instability and susceptibility to invasion.

microbiology↗

bioRxiv2018

Downgrading disease transmission risk estimates using terminal importations

As emerging and re-emerging infectious diseases like dengue, Ebola, chikungunya, and Zika threaten new populations worldwide, officials scramble to assess local severity and transmissibility, with little to no epidemiological history to draw upon. Standard methods for assessing autochthonous (local) transmission risk make either indirect estimates based on ecological suitability or direct estimates only after local cases accumulate. However, an overlooked source of epidemiological data that can meaningfully inform risk assessments prior to outbreak emergence is the absence of transmission by imported cases. Here, we present a method for updating a priori ecological estimates of transmission risk using real-time importation data. We demonstrate our method using Zika importation and transmission data from Texas in 2016, a high-risk region in the southern United States. Our updated risk estimates are lower than previously reported, with only six counties in Texas likely to sustain a Zika epidemic, and consistent with the number of autochthonous cases detected in 2017. Importation events can thereby provide critical, early insight into local transmission risks as infectious diseases expand their global reach.

epidemiology↗

bioRxiv2018

Whole-genome sequencing of parvoviruses from wild and domestic animals in Brazil provides new insights into parvovirus distribution and diversity

AbstractParvoviruses (family Parvoviridae) are small, single-stranded DNA viruses. Many parvoviral pathogens of medical, veterinary and ecological importance have been identified. In this study, we used high-throughput sequencing (HTS) to investigate the diversity of parvoviruses infecting wild and domestic animals in Brazil. We identified 21 parvovirus sequences (including twelve nearly complete genomes and nine partial genomes) in samples derived from rodents, bats, opossums, birds and cattle in Pernambuco, Sao Paulo, Parana and Rio Grande do Sul states. These sequences were investigated using phylogenetic and distance-based approaches, and were thereby classified into eight parvovirus species (six of which have not been described previously), representing six distinct genera in the subfamily Parvovirinae. Our findings extend the known biogeographic range of previously characterized parvovirus species, and the known host range of three parvovirus genera (Dependovirus, Aveparvovirus, and Tetraparvovirus). Moreover, our investigation provides a window into the ecological dynamics of parvovirus infections in vertebrates, revealing that many parvovirus genera contain well-defined sub-lineages that circulate widely throughout the world within particular taxonomic groups of hosts.

microbiology↗