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Evolution of ecological dominance of yeast species in high-sugar environments

In budding yeasts, fermentation in the presence of oxygen evolved around the time of a whole genome duplication (WGD) and is thought to confer dominance in high-sugar environments because ethanol is toxic to many species. While there are many fermentative yeast species, only Saccharomyces cerevisiae consistently dominates wine fermentations. In this study, we use co-culture experiments and intrinsic growth rate assays to examine the relative fitness of non-WGD and WGD yeast species across environments to assess when S. cerevisiaes ability to dominate high-sugar environments arose. We show that S. cerevisiae dominates nearly all other non-WGD and WGD species except for its sibling species S. paradoxus in both grape juice and a high-sugar rich medium. Of the species we tested, S. cerevisiae and S. paradoxus have evolved the highest ethanol tolerance and intrinsic growth rate in grape juice. However, the ability of S. cerevisiae and S. paradoxus to dominate certain species depends on the temperature and the type of high-sugar environment. Our results indicate that dominance of high-sugar environments evolved much more recently than the WGD, most likely just prior to or during the differentiation of Saccharomyces species, and that evolution of multiple traits contributes to S. cerevisiaes ability to dominate wine fermentations.

Evolutionary Biology

Evolution of color phenotypes in two distantly related species of stick insect: different ecological regimes acting on similar genetic architectures

Recurrent (e.g. parallel or convergent) evolution is widely cited as evidence for natural selections central role in evolution but can also highlight constraints affecting evolution. Here we describe the evolution of green and melanistic color phenotypes in two species of stick insect: Timema podura and T. cristinae. We show that similar color phenotypes of these species (1) cluster in phenotypic space and (2) confer crypsis on different plant microhabitats. We then use genome-wide association mapping to determine the genetic architecture of color in T. podura, and compare this to previous results in T. cristinae. In both species, color is under simple genetic control, dominance relationships of melanistic and green alleles are the same, and SNPs associated with color phenotypes colocalize to the same genomic region. These results differ from those of typical parallel phenotypes because the form of selection acting on color differs between species: a balance of multiple sources of selection acting within host species maintains the color polymorphism in T. cristinae whereas T. podura color phenotypes are under divergent selection between hosts. Our results highlight how different adaptive landscapes can result in the evolution of similar phenotypic variation, and suggest the same genomic region is involved.

Evolutionary Biology

Revealing complex ecological dynamics via symbolic regression

Complex ecosystems, from food webs to our gut microbiota, are essential to human life. Understanding the dynamics of those ecosystems can help us better maintain or control them. Yet, reverse-engineering complex ecosystems (i.e., extracting their dynamic models) directly from measured temporal data has not been very successful so far. Here we propose to close this gap via symbolic regression. We validate our method using both synthetic and real data. We firstly show this method allows reverse engineering two-species ecosystems, inferring both the structure and the parameters of ordinary differential equation models that reveal the mechanisms behind the system dynamics. We find that as the size of the ecosystem increases or the complexity of the inter-species interactions grow, using a dictionary of known functional responses (either previously reported or reverse-engineered from small ecosystems using symbolic regression) opens the door to correctly reverse-engineer large ecosystems.

Bioinformatics

Bacterial but not protist gut microbiota align with ecological specialization in a set of lower termite species

The role of microbes in adaptation of higher organisms to the environment is becoming increasingly evident, but remains poorly understood. Protist and bacterial microbes facilitate that lower termites thrive on wood and are directly involved in substrate break down. During the course of evolution lower termites adapted to different diets and lifestyles. In order to test whether there are changes of the termite gut microbiota that co-occur and hence could be related to diet and lifestyle adaptation, we assessed the bacterial and protist communities in a multispecies framework profiling three wood-dwelling and two foraging lower termite species using 16S and 18S rRNA gene amplicon sequencing. Termites were kept under controlled conditions on the same diet to minimize environmental effects on their gut microbiota. We found that protist communities group according to host phylogeny while bacterial communities group according to lifestyle. The change from the ancestral wood-dwelling to a foraging lifestyle coincides with exposure to more diverse and higher concentrations of pathogens as well as a more diverse diet. Accordingly, we identified bacteria that are associated with foraging termites of the genus Reticulitermes and could function as probiotics or be metabolically important on a more diverse diet. Furthermore, protist and bacterial diversity are correlated, suggesting not only that many termite gut bacteria are associated with protists, but also suggesting a role of protist diversity in the evolution of bacterial diversity in the termite gut or vice versa.

evolutionary biology

Epidemiological and ecological determinants of Zika virus transmission in an urban setting.

Zika has emerged as a global public health concern. Although its rapid geographic expansion can be attributed to the success of its Aedes mosquito vectors, local epidemiological drivers are still poorly understood. The city of Feira de Santana played a pivotal role in the early phases of the Chikungunya and Zika epidemics in Brazil. Here, using a climate-driven transmission model, we show that low Zika observation rates and a high vectorial capacity in this region were responsible for a high attack rate during the 2015 outbreak and the subsequent decline in cases in 2016, when the epidemic was peaking in the rest of the country. Our projections indicate that the balance between the loss of herd-immunity and the frequency of viral re-importation will dictate the transmission potential of Zika in this region in the near future. Sporadic outbreaks are expected but unlikely to be detected under current surveillance systems.

epidemiology

Response to nitrogen addition reveals metabolic and ecological strategies of soil bacteria

The nitrogen (N) cycle represents one of the most well studied systems yet the taxonomic diversity of the organisms that contribute to it is mostly unknown, or linked to poorly characterized microbial groups. While progress has allowed functional groups to be refined, they still rely on a priori knowledge of enzymes involved, and the assumption of functional conservation, with little connection to the role the transformation plays for specific organisms. Here, we use soil microcosms to test the impact of N deposition on prokaryotic communities. By combining chemical, genomic and transcriptomic analysis we are able to identify and link changes in community structure to specific organisms catalyzing given chemical reactions. Urea deposition led to a decrease in prokaryotic richness, and a shift in community composition. This was driven by replacement of stable native populations, which utilize energy from N-linked redox reactions for physiological maintenance, with fast responding populations that use this energy for growth. This model can be used to predict response to N disturbances and allows us to identify putative life strategies of different functional, and taxonomic, groups thus providing insights into how they persist in ecosystems by niche differentiation.

microbiology

Ecological characterization and infection of Anophelines (Diptera: Culicidae) of the Atlantic Forest in the southeast of Brazil over a 10 year period: Has the behaviour of the autochthonous malaria vector changed?

In the south and southeast of Brazil, autochthonous malaria cases can be found near Atlantic Forest fragments. The transmission is not totally clarified; thus, the behaviour of the possible vectors in those regions must be observed. An entomological and natural infection study was performed on anophelines (Diptera: Culicidae) captured in the municipalities of the mountainous region of Espirito Santo state in 2004-2005. Similarly, between the years 2014 and 2015, 12 monthly collections were performed at the permanent trapping station of the study mentioned above (Valsugana Velha, Santa Teresa, ES). Light traps with CO2 (CO2-baited Center for Disease Control [CDC] traps) were set in open areas, at the edge of the forest (canopy and ground) and inside the forest (canopy and ground), whereas Shannon traps were set on the edge of the forest. A total of 1,414 anophelines were collected from 13 species. Anopheles (Kerteszia) cruzii Dyar and Knab remained the most captured species in the CO2-baited CDC traps set in the forest canopy and was also the vector with the highest prevalence of Plasmodium vivax infection according to molecular PCR techniques. Regarding mosquitoes of the subgenus Nyssorhynchus, P. vivax was found only in abdomens, weakening the hypothesis that this subgenus also plays a role in malaria transmission in this specific region.\n\nSponsorshipEspirito Santo Research Foundation (Fundacao de Amparo a Pesquisa e Inovacao do Espirito Santo - FAPES).

epidemiology

Recurring infection with ecologically distinct human papillomavirus (HPV) types explains high prevalence and diversity

The high prevalence of human papillomavirus (HPV), the most common sexually transmitted infection, arises from the coexistence of over 200 genetically distinct types. Accurately predicting the impact of vaccines that target multiple types requires understanding the factors that determine HPV diversity. The diversity of many pathogens is driven by type-specific or \"homologous\" immunity, which promotes the spread of variants to which hosts have little immunity. To test for homologous immunity and to identify mechanisms determining HPV transmission, we fitted nonlinear mechanistic models to longitudinal data on genital infections in unvaccinated men. Our results provide no evidence for homologous immunity, instead showing that infection with one HPV type strongly increases the risk of infection with that type for years afterwards. For HPV16, the type responsible for most HPV-related cancers, an initial infection increases the one-year probability of reinfection by 20-fold, and the probability of reinfection remains 14-fold higher two years later. This increased risk occurs in both sexually active and celibate men, suggesting that it arises from auto-inoculation, episodic reactivation of latent virus, or both. Overall our results show that high HPV prevalence and diversity can be explained by a combination of a lack of homologous immunity, frequent reinfections, weak competition between types, and variation in type fitness between host subpopulations. Due to the high risk of reinfection, vaccinating boys that have not yet been exposed may be crucial to reduce prevalence, but our results suggest that there may also be large benefits from vaccinating previously infected individuals.

epidemiology

Robustness encoded across essential and accessory replicons in an ecologically versatile bacterium

Bacterial genome evolution is characterized by gains, losses, and rearrangements of functional genetic segments. The extent to which genotype-phenotype relationships are influenced by large-scale genomic alterations has not been investigated in a high-throughput manner. In the symbiotic soil bacterium Sinorhizobium meliloti, the genome is composed of a chromosome and two large extrachromosomal replicons (pSymA and pSymB, which together constitute 45% of the genome). Massively parallel transposon insertion sequencing (Tn-seq) was employed to evaluate contributions of chromosomal genes to fitness in both the presence and absence of these extrachromosomal replicons. Ten percent of chromosomal genes from diverse functional categories are shown to genetically interact with pSymA and pSymB. These results demonstrate the pervasive robustness provided by the extrachromosomal replicons, which is further supported by constraint-based metabolic modelling. A comprehensive picture of core S. meliloti metabolism was generated through a Tn-seq-guided in silico metabolic network reconstruction, producing a core network encompassing 726 genes. This integrated approach facilitated functional assignments for previously uncharacterized genes, while also revealing that Tn-seq alone misses over a quarter of wild type metabolism. This work highlights the strong functional dependencies and epistatic relationships that may arise between bacterial replicons and across a genome, while also demonstrating how Tn-seq and metabolic modelling can be used together to yield insights not obtainable by either method alone.

systems biology

An endogenous amdoparvovirus in the genome of the Transcaucasian mole vole (Ellobius lutescens): implications for ecology and evolution of carnivore amdoparvoviruses.

Amdoparvoviruses (family Parvoviridae: genus Amdoparvovirus) infect carnivores, and are a major cause of morbidity and mortality in farmed animals. In this study, we systematically screened animal genomes to identify PVe disclosing a high degree of similarity to amdoparvoviruses, and investigated their genomic, phylogenetic and protein structural features. We report the first examples of full-length, amdoparvovirus-derived PVe in the genome of the Transcaucasian mole vole (Ellobius lutescens). Furthermore, we identify four further PVe in mammal and reptile genomes that are intermediate between amdoparvoviruses and their sister genus (Protoparvovirus) in terms of their phylogenetic placement and genomic features. In particular, we identify a genome-length PVe in the genome of a pit viper (Protobothrops mucrosquamatus) that is more like a protoparvovirus than an amdoparvovirus in terms of its phylogenetic placement and the structural features of its capsid protein (as revealed by homology modeling), yet exhibits characteristically amdoparvovirus-like genome features including: (i) a putative middle ORF gene; (ii) a capsid gene that lacks a phospholipase A2 (PLA2) domain; (iii) a genome structure consistent with an amdoparvovirus-like mechanism of capsid gene expression. Our findings indicate that amdoparvovirus host range has extended to rodents in the past, and that parvovirus lineages possessing a mixture of proto- and amdoparvovirus-like characteristics have circulated in the past. In addition, we show that PVe in the mole vole and pit viper encode intact, expressible replicase genes that have potentially been co-opted or exapted in these host species.

evolutionary biology

The genomic and ecological context of hybridization affect the probability that symmetrical incompatibilities drive hybrid speciation.

Despite examples of homoploid hybrid species, theoretical work describing when, where, and how we expect homoploid hybrid speciation to occur remains relatively rare. Here I explore the probability of homoploid hybrid speciation due to \"symmetrical incompatibilities\" under different selective and genetic scenarios. Through simulation, I test how genetic architecture and selection acting on traits that do not themselves generate incompatibilities interact to affect the probability that hybrids evolve symmetrical incompatibilities with their parent species. Unsurprisingly, selection against admixture at adaptive loci that are linked to loci that generate incompatibilities tends to reduce the probability of evolving symmetrical incompatibilities. By contrast, selection that favors admixed genotypes at adaptive loci can promote the evolution of symmetrical incompatibilities. The magnitude of these outcomes is affected by the strength of selection, aspects of genetic architecture such as linkage relationships and the linear arrangement of loci along a chromosome, and the amount of hybridization following the formation of a hybrid zone. These results highlight how understanding the nature of selection, aspects of the genetics of traits affecting fitness, and the strength of reproductive isolation between hybridizing taxa can all be used to inform when we expect to observe homoploid hybrid speciation due to symmetrical incompatibilities.

evolutionary biology

TAG.ME: Taxonomic Assignment of Genetic Markers for Ecology

1.BackgroundSequencing of amplified genetic markers, such as the 16S rRNA gene, have been extensively used to characterize microbial community composition. Recent studies suggested that Amplicon Sequences Variants (ASV) should replace the Operational Taxonomic Units (OTU), given the arbitrary definition of sequence identity thresholds used to define units. Alignment-free methods are an interesting alternative for the taxonomic classification of the ASVs, preventing the introduction of biases from sequence identity thresholds.\n\nResultsHere we present TAG.ME, a novel alignment-independent and amplicon-specific method for taxonomic assignment based on genetic markers. TAG.ME uses a multilevel supervised learning approach to create predictive models based on user-defined genetic marker genes. The predictive method can assign taxonomy to sequenced amplicons efficiently and effectively. We applied our method to assess gut and soil sample classification, and it outperformed alternative approaches, identifying a substantially larger proportion of species. Benchmark tests performed using the RDP database, and Mock communities reinforced the precise classification into deep taxonomic levels.\n\nConclusionTAG.ME presents a new approach to assign taxonomy to amplicon sequences accurately. Our classification model, trained with amplicon specific sequences, can address resolution issues not solved by other methods and approaches that use the whole 16S rRNA gene sequence. TAG.ME is implemented as an R package and is freely available at http://gabrielrfernandes.github.io/tagme/

bioinformatics

Expanded view of the ecological genomics of ant responses to climate change

Given the abundance, broad distribution, and diversity of roles that ants play in many ecosystems, they are an ideal group to serve as ecosystem indicators of climatic change. At present, only a few whole-genome sequences of ants are available (19 of > 16,000 species), mostly from tropical and sub-tropical species. To address this limited sampling, we sequenced genomes of temperate-latitude species from the genus Aphaenogaster, a genus with important seed dispersers. In total, we sampled seven colonies of six species: A. ashmeadi, A. floridana, A. fulva, A. miamiana, A. picea, and A. rudis. The geographic ranges of these species collectively span eastern North America from southern Florida to southern Canada, which encompasses a latitudinal gradient in which many climatic variables are changing rapidly. For the six genomes, we assembled an average of 271,039 contigs into 47,337 scaffolds. The mean genome size was 370.5 Mb, ranging from 310.3 to 429.7, which is comparable to that of other sequenced ant genomes (212.8 to 396.0 Mb) and flow cytometry estimates (210.7 to 690.4 Mb). In an analysis of currently sequenced ant genomes and the new Aphaenogaster sequences, we found that after controlling for both spatial autocorrelation and phylogenetics ant genome size was marginally correlated with sample site climate similarity. Of all examined climate variables, minimum temperature showed the strongest correlation with genome size, with ants from locations with colder minimum temperatures having larger genomes. These results suggest that temperature extremes could be a selective force acting on ant genomes and point to the need for more extensive sequencing of ant genomes.

genomics

Combining landscape genomics and ecological modelling to investigate local adaptation of indigenous Ugandan cattle to East Coast fever

East Coast fever (ECF) is a fatal sickness affecting cattle populations of eastern, central, and southern Africa. The disease is transmitted by the tick Rhipicephalus appendiculatus, and caused by the protozoan Theileria parva parva, which invades host lymphocytes and promotes their clonal expansion. Importantly, indigenous cattle show tolerance to infection in ECF-endemically stable areas. Here, the putative genetic bases underlying ECF-tolerance were investigated using molecular data and epidemiological information from 823 indigenous cattle from Uganda. Vector distribution and host infection risk were estimated over the study area and subsequently tested as triggers of local adaptation by means of landscape genomics analysis. We identified 41 and seven candidate adaptive loci for tick resistance and infection tolerance, respectively. Among the genes associated with the candidate adaptive loci are PRKG1 and SLA2. PRKG1 was already described as associated with tick resistance in indigenous South African cattle, due to its role into inflammatory response. SLA2 is part of the regulatory pathways involved into lymphocytes proliferation. Additionally, local ancestry analysis suggested the zebuine origin of the genomic region candidate for tick resistance.\n\nAuthor summaryThe tick-borne parasite Theileria parva parva infects cattle populations of eastern, central and southern Africa, by causing a highly fatal pathology called \"East Coast fever\". The disease is especially severe for the exotic breeds imported to Africa, as well as outside the endemic areas of East Africa. In these regions, indigenous cattle populations can survive to infection, and this tolerance might result from unique adaptations evolved to fight the disease. We investigated this hypothesis by using a method named \"landscape genomics\", with which we compared the genetic characteristics of indigenous Ugandan cattle coming from areas at different infection risk, and located genomic sites potentially attributable to tolerance. In particular, the method pinpointed two genes, one (PRKG1) involved into inflammatory response and potentially affecting East Coast fever vector attachment, the other (SLA2) involved into lymphocytes proliferation, a process activated by T. parva parva infection. Our findings can orientate future research on the genetic basis of East Coast fever-tolerance, and derive from a general method that can be applied to investigate adaptation in analogous host-vector-parasite systems. Characterization of the genetic factors underlying East Coast-fever-tolerance represents an essential step towards enhancing sustainability and productivity of local agroecosystems.

evolutionary biology

ZetaHunter: a reproducible taxonomic classification tool for tracking the ecology of the Zetaproteobacteria and other poorly-resolved taxa

Like many taxa, the Zetaproteobacteria lack well-defined taxonomic divisions, 32 making it difficult to compare between studies. We designed ZetaHunter to reproducibly 33 assign 16S rRNA gene sequences to previously-described OTUs based on a curated 34 database. While ZetaHunter can use any given database, we include a curated 35 classification of publically-available Zetaproteobacteria.

bioinformatics

Flow stimuli reveal ecologically-appropriate responses in mouse visual cortex

Assessments of the mouse visual system based on spatial frequency analysis imply that its visual capacity is low, with few neurons responding to spatial frequencies greater than 0.5 cycles/degree. However, visually-mediated behaviors, such as prey capture, suggest that the mouse visual system is more precise. We introduce a new stimulus class--visual flow patterns--that is more like what the mouse would encounter in the natural world than are sine-wave gratings but is more tractable for analysis than are natural images. We used 128-site silicon microelectrodes to measure the simultaneous responses of single neurons in the primary visual cortex (V1) of alert mice. While holding temporal-frequency content fixed, we explored a class of drifting patterns of black or white dots that have energy only at higher spatial frequencies. These flow stimuli evoke strong visually-mediated responses well beyond those predicted by spatial frequency analysis. Flow responses predominate in higher spatial-frequency ranges (0.15-1.6 cycles/degree); many are orientation- or direction-selective; and flow responses of many neurons depend strongly on sign of contrast. Many cells exhibit distributed responses across our stimulus ensemble. Together, these results challenge conventional linear approaches to visual processing and expand our understanding of the mouses visual capacity to behaviorally-relevant ranges.\n\nSignificance StatementThe visual system of the mouse is now widely studied as a model for development and disease in humans. Studies of its primary visual cortex (V1) using conventional grating stimuli to construct linear-nonlinear receptive fields suggest that the mouse must have very poor vision. Using novel stimuli resembling the flow of images across the retina as the mouse moves through the grass, we find that most V1 neurons respond reliably to very much finer details of the visual scene than previously believed. Our findings suggest that the conventional notion of a unique receptive field does not capture the operation of the neural network in mouse V1.

neuroscience

Ecological analyses of mycobacteria in showerhead biofilms and their relevance to human health

Bacteria within the genus Mycobacterium can be abundant in showerheads, and the inhalation of aerosolized mycobacteria while showering has been implicated as a mode of transmission in nontuberculous mycobacterial (NTM) lung infections. Despite their importance, the diversity, distributions, and environmental predictors of showerhead-associated mycobacteria remain largely unresolved. To address these knowledge gaps, we worked with citizen scientists to collect showerhead biofilm samples and associated water chemistry data from 656 households located across the U.S. and Europe. Our cultivation-independent analyses revealed that the genus Mycobacterium was consistently the most abundant genus of bacteria detected in residential showerheads, yet mycobacterial diversity and abundances were highly variable. Mycobacteria were far more abundant, on average, in showerheads receiving municipal versus well water, and in U.S. households as compared to European households, patterns that are likely driven by differences in the use of chlorine disinfectants. Moreover, we found that water source, water chemistry, and household location also influenced the prevalence of specific mycobacterial lineages detected in showerheads. We identified geographic regions within the U.S. where showerheads have particularly high abundances of potentially pathogenic lineages of mycobacteria and these hot spots generally overlapped with those regions where NTM lung disease is most prevalent. Together these results emphasize the public health relevance of mycobacteria in showerhead biofilms. They further demonstrate that mycobacterial distributions in showerhead biofilms are often predictable from household location and water chemistry, knowledge that advances our understanding of NTM transmission dynamics and the development of strategies to reduce exposures to these emerging pathogens.

microbiology

How symbiosis and ecological context influence the variable expression of transgenerational wing induction upon fungal infection of aphids

Aphids, like most animals, mount a diverse set of defenses against pathogens. For aphids, two of the best studied defenses are symbiont-conferred protection and transgenerational wing induction. Aphids can harbor bacterial symbionts that provide protection against pathogens, parasitoids and predators, as well as against other environmental stressors. In response to signals of danger, aphids also protect not themselves but their offspring by producing more winged than unwinged offspring as a way to ensure that their progeny may be able to escape deteriorating conditions. Such transgenerational wing induction has been studied most commonly as a response to overcrowding of host plants and presence of predators, but recent evidence suggests that pea aphids (Acyrthosiphon pisum) may also begin to produce a greater proportion of winged offspring when infected with fungal pathogens. Here, we explore this phenomenon further by asking how protective symbionts, pathogen dosage and environmental conditions influence this response. Overall, while we find some evidence that protective symbionts can modulate transgenerational wing induction in response to fungal pathogens, we observe that transgenerational wing induction in response to fungal infection is highly variable. That variability cannot be explained entirely by symbiont association, by pathogen load or by environmental stress, leaving the possibility that a complex interplay of genotypic and environmental factors may together influence this trait.

evolutionary biology