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Nurtured by nature: Considering the role of environmental and parental legacies in coral ecological performance

The persistence of reef building corals is threatened by human-induced environmental change. Maintaining coral reefs into the future requires not only the survival of adults, but also the influx of recruits to promote genetic diversity and retain cover following adult mortality. Few studies examine the linkages among multiple life stages of corals, despite a growing knowledge of carryover effects in other systems. We provide a novel test of coral parental preconditioning to ocean acidification (OA) to better understand impacts on the processes of offspring recruitment and growth. Coral planulation was tracked for three months following adult exposure to high pCO2 and offspring from the second month were reciprocally exposed to ambient and high pCO2. Offspring of parents exposed to high pCO2 had greater settlement and survivorship immediately following release, retained survivorship benefits during one and six months of continued exposure, and further displayed growth benefits to at least one month post release. Enhanced performance of offspring from parents exposed to high conditions was maintained despite the survivorship in both treatments declining in continued exposure to OA. Preconditioning of the adults while they brood their larvae may provide a form of hormetic conditioning, or environmental priming that elicits stimulatory effects. Defining mechanisms of positive carryover effects, or positive trans-generational plasticity, is critical to better understanding ecological and evolutionary dynamics of corals under regimes of increasing environmental disturbance. Considering parental and environmental legacies in ecological and evolutionary projections may better account for coral reef response to the chronic stress regimes characteristic of climate change.

physiology↗

Demographic inference in a spatially-explicit ecological model from genomic data: a proof of concept for the Mojave Desert Tortoise

In this paper, we study the general problem of extracting information from spatially explicit genomic data to inform inference of ecologically and geographically realistic population models. We describe methods and apply them to simulations motivated by the demography of the Mojave desert tortoise (Gopherus agassizii). The tortoise is an example of a long-lived, threatened species for which we have an excellent understanding of range, habitat preference, and certain aspects of demography, but inadequate information on other life history components that are important for conservation management. We use an individual-based model on a discretized geographic landscape with overlapping generations and age and sex-specific dispersal, fecundity, and mortality to develop and test a method that uses genomic data to infer demographic parameters. We do this by seeking parameters that best match a set of spatial statistics of genomes, which we introduce and discuss. We find that for inferring only overall population density and mean migration distance, a simple statistical learning method performs well using simulated training data, inferring parameters to within 10% accuracy. In the process, we introduce spatial analogues of common population genetics statistics, and discuss how and why they are expected to contain signal about the geography of population dynamics that are key for ecological modeling generally and conservation of endangered taxa.

genomics↗

Underlying mechanisms and ecological consequences of variation in exploratory behavior of the Argentine ant, Linepithema humile

Uncovering how and why animals explore their environment is fundamental for understanding population dynamics, the spread of invasive species, species interactions etc. In social animals, individuals within a group can vary in their exploratory behavior and the behavioral composition of the group can determine its collective success. Workers of the invasive Argentine ant (Linepithema humile) exhibit individual variation in exploratory behavior, which affects the colonys collective nest selection behavior. Here we examine the mechanisms underlying this behavioral variation in exploratory behavior and determine its implications for the ecology of this species. We first establish that individual variation in exploratory behavior is repeatable and consistent across situations. We then show a relationship between exploratory behavior and the expression of genes that have been previously linked with other behaviors in social insects. Specifically, we find a negative relationship between exploratory behavior and the expression of the FOR gene. Finally, we determine how colonies allocate exploratory individuals in natural conditions. We find that ants from inside the nest are the least exploratory individuals, while workers on newly formed foraging trails are the most exploratory individuals. Furthermore, workers in the spring, when new resources emerge, are more exploratory than workers in the winter, potentially allowing the colony to find and exploit new resources. These findings reveal the importance of individual variation in behavior for the ecology of social animals and provide mechanistic and functional explanations for how such behavioral variation can emerge.

animal behavior and cognition↗

Geographic shifts in Aedes aegypti habitat suitability in Ecuador using larval surveillance data and ecological niche modeling: implications of climate change for public health vector control

Arboviral disease transmission by Aedes mosquitoes poses a major challenge to public health systems in Ecuador, where constraints on health services and resource allocation call for spatially informed management decisions. Employing a unique dataset of larval occurrence records provided by the Ecuadorian Ministry of Health, we used ecological niche models (ENMs) to estimate the current geographic distribution of Aedes aegypti in Ecuador, using mosquito presence as a proxy for risk of disease transmission. ENMs built with the Genetic Algorithm for Rule-Set Production (GARP) algorithm and a suite of environmental variables were assessed for agreement and accuracy. The top model of larval mosquito presence was projected to the year 2050 under various combinations of greenhouse gas emissions scenarios and models of climate change. Under current climatic conditions, larval mosquitoes were not predicted in areas of high elevation in Ecuador, such as the Andes mountain range, as well as the eastern portion of the Amazon basin. However, all models projected to scenarios of future climate change demonstrated potential shifts in mosquito distribution, wherein range contractions were seen throughout most of eastern Ecuador, and areas of transitional elevation became suitable for mosquito presence. Encroachment of Ae. aegypti into mountainous terrain was estimated to affect up to 4,215 km2 under the most extreme scenario of climate change, an area which would put over 12,000 people currently living in transitional areas at risk. This distributional shift into communities at higher elevations indicates an area of concern for public health agencies, as targeted interventions may be needed to protect vulnerable populations with limited prior exposure to mosquito-borne diseases. Ultimately, the results of this study serve as a tool for informing public health policy and mosquito abatement strategies in Ecuador.\n\nAuthor summaryThe yellow fever mosquito (Aedes aegypti) is a medically important vector of arboviral diseases in Ecuador, such as dengue fever and chikungunya. Managing Ae. aegypti is a challenge to public health agencies in Latin America, where the use of limited resources must be planned in an efficient, targeted manner. The spatial distribution of Ae. aegypti can be used as a proxy for risk of disease exposure, guiding policy formation and decision-making. We used ecological niche models in this study to predict the range of Ae. aegypti in Ecuador, based on agency larval mosquito surveillance records and layers of environmental predictors (e.g. climate, altitude, and human population). The best models of current range were then projected to the year 2050 under a variety of greenhouse gas emissions scenarios and models of climate change. All modeled future scenarios predicted shifts in the range of Ae. aegypti, allowing us to assess human populations that may be at risk of becoming exposed to Aedes vectored diseases. As climate changes, we predict that communities living in areas of transitional elevation along the Andes mountain range are vulnerable to the expansion of Aedes aegypti.

epidemiology↗

Genomic architecture of parallel ecological divergence: beyond a single environmental contrast

The genetic basis of parallel ecological divergence provides important clues to the operation of natural selection and the predictability of evolution. Many examples exist where binary environmental contrasts seem to drive parallel divergence. However, this simplified view can conceal important components of parallel divergence because environmental variation is often more complex. Here, we disentangle the genetic basis of parallel divergence across two axes of environmental differentiation (crab-predation vs. wave-action and low-shore vs. high-shore habitat contrasts) in the marine snail Littorina saxatilis, a well established natural system of parallel ecological divergence. We used whole-genome resequencing across multiple instances of these two environmental axes, at local and regional scales from Spain to Sweden. Overall, sharing of genetic differentiation is generally low but it is highly heterogeneous across the genome and increases at smaller spatial scales. We identified genomic regions, both overlapping and non-overlapping with recently described candidate chromosomal inversions, that are differentially involved in adaptation to each of the environmental axis. Thus, the evolution of parallel divergence in L. saxatilis is largely determined by the joint action of geography, history, genomic architecture and congruence between environmental axes. We argue that the maintenance of standing variation, perhaps as balanced polymorphism, and/or the re-distribution of adaptive variants via gene flow can facilitate parallel divergence in multiple directions as an adaptive response to heterogeneous environments.

evolutionary biology↗

Taxonomy, ecology and distribution of Juniperus oxycedrus L. group in the Mediterranean Region using morphometric, phytochemical and bioclimatic approaches.

The ecology, taxonomy and distribution of the Juniperus oxycedrus L. group of taxa are studied. From an ecological aspect, this work proposes a new ombroedaphoxeric index to explain the presence of populations of Juniperus in ombrotypes that are not the optimum for these taxa. The controversy among various authors on the taxonomy of the oxycedrus group with regard to J. oxycedrus subsp. badia and J. oxycedrus subsp. lagunae is clarified. The phytochemical differences in essential oils are addressed, and their similarities analysed; greater similarities are observed between oxycedrus and badia (H. Gay) Debeaux, and between navicularis Grand. and macrocarpa (Sm.) Ball. The phytochemical, molecular and distribution differences allow J. macrocarpa and J. navicularis to be maintained as species.

plant biology↗

In situ estimation of genetic variation of functional and ecological traits in Quercus petraea and Q. robur

BackgroundPredicting the evolutionary potential of natural tree populations requires the estimation of heritability and genetic correlations among traits on which selection acts, as differences in evolutionary success between species may rely on differences for these genetic parameters. In situ estimates are expected to be more accurate than measures done under controlled conditions which do not reflect the natural environmental variance.\n\nAimsThe aim of the current study was to estimate three genetic parameters (i.e. heritability, evolvability and genetic correlations) in a natural mixed oak stand composed of Quercus petraea and Quercus robur about 100 years old, for 58 traits of ecological and functional relevance (growth, reproduction, phenology, physiology, resilience, structure, morphology and defence).\n\nMethodsFirst we estimated genetic parameters directly in situ using realized genomic relatedness of adult trees and parentage relationships over two generations to estimate the traits additive variance. Secondly, we benefited from existing ex situ experiments (progeny tests and conservation collection) installed with the same populations, thus allowing comparisons of in situ heritability estimates with more traditional methods.\n\nResultsHeritability and evolvability estimates obtained with different methods varied substantially and showed large confidence intervals, however we found that in situ were less precise than ex situ esti-mates, and assessments over two generations (with deeper relatedness) improved estimates of heritability while large sampling sizes are needed for accurate estimations. At the biological level, heritability values varied moderately across different ecological and functional categories of traits, and genetic correlations among traits were conserved over the two species.\n\nConclusionWe identified limits for using realized genomic relatedness in natural stands to estimate the genetic variance, given the overall low variance of genetic relatedness and the rather low sampling sizes of currently used long term genetic plots in forestry. These limits can be overcome if larger sample sizes are considered, or if the approach is extended over the next generation.

evolutionary biology↗

Ecological causes of uneven diversification and richness in the mammal tree of life

The uneven distributions of species over geography (e.g., tropical versus temperate regions) and phylogeny (e.g., rodents and bats versus the aardvark) are prominent biological patterns for which causal interconnections remain enigmatic. Here we investigate this central issue for living mammals using time-sliced clades sampled from a comprehensive recent phylogeny (N=5,911 species, [~]70% with DNA) to assess how different levels of unsampled extinction impact the inferred causes of species richness variation. Speciation rates are found to strongly exceed crown age as a predictor of clade species richness at every time slice, rejecting a clock-like model in which the oldest clades are the most speciose. Instead, mammals that are low-vagility or daytime-active show the fastest recent speciation and greatest extant richness. This suggests primary roles for dispersal limitation leading to geographic speciation (peripatric isolation) and diurnal adaptations leading to ecological speciation (time partitioning). Rates of speciation are also faster in temperate than tropical lineages, but only among older clades, consistent with the idea that many temperate lineages are ephemeral. These insights, enabled by our analytical framework, offer straightforward support for ecological effects on speciation-rate variation among clades as the primary cause of uneven phylogenetic richness patterns.

evolutionary biology↗

Genomic analysis of the four ecologically distinct cactus host populations of Drosophila mojavensis

BackgroundRelationships between an organism and its environment can be fundamental in the understanding how populations change over time and species arise. Local ecological conditions can shape variation at multiple levels, among these are the evolutionary history and trajectories of coding genes. This study examines the rate of molecular evolution at protein-coding genes throughout the genome in response to host adaptation in the cactophilic Drosophila mojavensis. These insects are intimately associated with cactus necroses, developing as larvae and feeding as adults in these necrotic tissues. Drosophila mojavensis is composed of four isolated populations across the deserts of western North America and each population has adapted to utilize different cacti that are chemically, nutritionally, and structurally distinct. ResultsHigh coverage Illumina sequencing was performed on three previously unsequenced populations of D. mojavensis. Genomes were assembled using the previously sequenced genome of D. mojavensis from Santa Catalina Island (USA) as a template. Protein coding genes were aligned across all four populations and rates of protein evolution were determined for all loci using a several approaches. ConclusionsLoci that exhibited elevated rates of molecular evolution tended to be shorter, have fewer exons, low expression, be transcriptionally responsive to cactus host use and have fixed expression differences across the four cactus host populations. Fast evolving genes were involved with metabolism, detoxification, chemosensory reception, reproduction and behavior. Results of this study gives insight into the process and the genomic consequences of local ecological adaptation.

genomics↗

The simulation extrapolation technique meets ecology and evolution: A general and intuitive method to account for measurement error

O_LIMeasurement error and other forms of uncertainty are commonplace in ecology and evolution and may bias estimates of parameters of interest. Although a variety of approaches to obtain unbiased estimators are available, these often require that errors are explicitly modeled and that a latent model for the unobserved error-free variable can be specified, which in practice is often difficult. C_LIO_LIHere we propose to generalize a heuristic approach to correct for measurement error, denoted as simulation extrapolation (SIMEX), to situations where explicit error modeling fails. We illustrate the application of SIMEX using the example of estimates of quantitative genetic parameters, e. g. inbreeding depression and heritability, in the presence of pedigree errors. Following the original SIMEX idea, the error in the pedigree is progressively increased to determine how the estimated quantities are affected by error. The observed trend is then extrapolated back to a hypothetical error-free pedigree, yielding unbiased estimates of inbreeding depression and heritability. We term this application of the SIMEX idea to pedigrees "PSIMEX". We tested the method with simulated pedigrees with different pedigree structures and initial error proportions, and with real field data from a free-living population of song sparrows. C_LIO_LIThe simulation study indicates that the accuracy and precision of the extrapolated error-free estimate for inbreeding depression and heritability are good. In the application to the song sparrow data, the error-corrected results could be validated against the actual values thanks to the availability of both an error-prone and an error-free pedigree, and the results indicate that the PSIMEX estimator is close to the actual value. For easy accessibility of the method, we provide the novel R-package PSIMEX. C_LIO_LIBy transferring the SIMEX philosophy to error in pedigrees, we have illustrated how this heuristic approach can be generalized to situations where explicit latent models for the unobserved variables or for the error of the variables of interest are difficult to formulate. Thanks to the simplicity of the idea, many other error problems in ecology and evolution might be amenable to SIMEX-like error correction methods. C_LI

evolutionary biology↗

Genome of the parasitoid wasp Diachasma alloeum, an emerging model for ecological speciation and transitions to asexual reproduction

Parasitoid wasps are among the most speciose animals, yet have relatively few available genomic resources. We report a draft genome assembly of the wasp Diachasma alloeum (Hymenoptera: Braconidae), a host-specific parasitoid of the apple maggot fly Rhagoletis pomonella (Diptera: Tephritidae) and a developing model for understanding how ecological speciation can "cascade" across trophic levels. Identification of gene content confirmed the overall quality of the draft genome, and we manually annotated [~]400 genes as part of this study, including those involved in oxidative phosphorylation, chemosensation, and reproduction. Through comparisons to model hymenopterans such as the European honeybee Apis mellifera and parasitoid wasp Nasonia vitripennis, as well as a more closely related braconid parasitoid Microplitis demolitor, we identified a proliferation of transposable elements in the genome, an expansion of chemosensory genes in D. alloeum and other parasitoid wasps, and the maintenance of several key genes with known roles in sexual reproduction and sex determination. The D. alloeum genome will provide a valuable resource for comparative genomics studies in Hymenoptera as well as specific investigations into the genomic changes associated with ecological speciation and transitions to asexuality.

genomics↗

Integrating behaviour and ecology into global biodiversity conservation strategies

Insights into animal behaviour play an increasingly central role in species-focused conservation practice. However, progress towards incorporating behaviour into regional or global conservation strategies has been far more limited, not least because standardised datasets of behavioural traits are generally lacking at wider taxonomic or spatial scales. Here we make use of the recent expansion of global datasets for birds to assess the prospects for including behavioural traits in systematic conservation priority-setting and monitoring programmes. Using IUCN Red List classification for >9500 bird species, we show that the incidence of threat can vary substantially across different behavioural syndromes, and that some types of behaviour--including particular foraging, mating and migration strategies--are significantly more threatened than others. When all factors are included in a combined model, behavioural traits have a weaker effect than well-established geographical and ecological factors, including range size, body mass and human population pressures. We also show that the association between behavior and extinction risk is partly driven by correlations with these underlying factors. Overall, these results suggest that a multi-species approach at the scale of communities, continents and ecosystems can be used to identify and monitor threatened behaviours, and to flag up cases of latent extinction risk, where threatened status may currently be underestimated. Our findings also highlight the importance of comprehensive standardized descriptive data for ecological and behavioural traits, and point the way forward to a deeper integration of behaviour into quantitative conservation assessments.

animal behavior and cognition↗

Reconstructing the ecology of a Jurassic pseudoplanktonic megaraft colony

Pseudoplanktonic crinoid megaraft colonies are an enigma of the Jurassic. They are among the largest in-situ invertebrate accumulations ever to exist in the Phanerozoic fossil record. These megaraft colonies and are thought to have developed as floating filter-feeding communities due to an exceptionally rich relatively predator free oceanic niche, high in the water column enabling them to reach high densities on these log rafts. However, this pseudoplanktonic hypothesis has never actually been quantitatively tested and some researchers have cast doubt that this mode of life was even possible. The ecological structure of the crinoid colony is resolved using spatial point process techniques and its longevity using moisture diffusion models. Using spatial analysis we found that the crinoids would have trailed preferentially positioned at the back of migrating structures in the regions of least resistance, consistent with a floating, not benthic ecology. Additionally, we found using a series of moisture diffusion models at different log densities and sizes that ecosystem collapse did not take place solely due to colonies becoming overladen as previously assumed. We have found that these crinoid colonies studied could have existed for greater than 10 years, even up to 20 years exceeding the life expectancy of modern documented megaraft systems with implications for the role of modern raft communities in the biotic colonisation of oceanic islands and intercontinental dispersal of marine and terrestrial species.Significance statement Transoceanic rafting is the principle mechanism for the biotic colonisation of oceanic island ecosystems. However, no historic records exist of how long such biotic systems lasted. Here, we use a deep-time example from the Early Jurassic to test the viability of these pseudoplanktonic systems, resolving for the first time whether these systems were truly free floating planktonic and viable for long enough to allow its inhabitants to grow to maturity. Using spatial methods we show that these colonies have a comparable structure to modern marine pesudoplankton on maritime structures, whilst the application of methods normally used in commercial logging is used to demonstrate the viability of the system which was capable of lasting up to 20 years.View Full Text

paleontology↗

Tissue Tropism and Transmission Ecology Predict Virulence of Human RNA Viruses

Novel infectious diseases continue to emerge within human populations. Predictive studies have begun to identify pathogen traits associated with emergence. However, emerging pathogens vary widely in virulence, a key determinant of their ultimate risk to public health. Here, we use structured literature searches to review the virulence of each of the 214 known human-infective RNA virus species. We then use a machine learning framework to determine whether viral virulence can be predicted by ecological traits including human-to-human transmissibility, transmission routes, tissue tropisms and host range. Using severity of clinical disease as a measurement of virulence, we identified potential risk factors using predictive classification tree and random forest ensemble models. The random forest model predicted literature-assigned disease severity of test data with 90.3% accuracy, compared to a null accuracy of 74.2%. In addition to viral taxonomy, the ability to cause systemic infection, having renal and/or neural tropism, direct contact or respiratory transmission, and limited (0 < R0 [&le;] 1) human-to-human transmissibility were the strongest predictors of severe disease. We present a novel, comparative perspective on the virulence of all currently known human RNA virus species. The risk factors identified may provide novel perspectives in understanding the evolution of virulence and elucidating molecular virulence mechanisms. These risk factors could also improve planning and preparedness in public health strategies as part of a predictive framework for novel human infections.\n\nAuthor SummaryNewly emerging infectious diseases present potentially serious threats to global health. Although studies have begun to identify pathogen traits associated with the emergence of new human diseases, these do not address why emerging infections vary in the severity of disease they cause, often termed virulence. We test whether ecological traits of human viruses can act as predictors of virulence, as suggested by theoretical studies. We conduct the first systematic review of virulence across all currently known human RNA virus species. We adopt a machine learning approach by constructing a random forest, a model that aims to optimally predict an outcome using a specific structure of predictors. Predictions matched literature-assigned ratings for 28 of 31 test set viruses. Our predictive model suggests that higher virulence is associated with infection of multiple organ systems, nervous systems or the renal systems. Higher virulence was also associated with contact-based or airborne transmission, and limited capability to transmit between humans. These risk factors may provide novel starting points for questioning why virulence should evolve and identifying causative mechanisms of virulence. In addition, our work could suggest priority targets for infectious disease surveillance and future public health risk strategies.\n\nBlurbComparative analysis using machine learning shows specificity of tissue tropism and transmission biology can act as predictive risk factors for virulence of human RNA viruses.

epidemiology↗

De Novo Growth Of Methanogenic Granules Indicates A Biofilm Life-Cycle With Complex Ecology

Methanogenic sludge granules are densely packed, small (diameter, approx. 0.5-2.0 mm) spherical biofilms found in anaerobic digesters used to treat industrial wastewaters, where they underpin efficient organic waste conversion and biogas production. A single digester contains millions of individual granules, each of which is a highly-organised biofilm comprised of a complex consortium of likely billions of cells from across thousands of species - but not all granules are identical. Whilst each granule theoretically houses representative microorganisms from all of the trophic groups implicated in the successive and interdependent reactions of the anaerobic digestion process, parallel granules function side-by-side in digesters to provide a meta-organism of sorts. Granules from a full-scale bioreactor were size-separated into small, medium and large granules. Laboratory-scale bioreactors were operated using only small (0.6-1 mm), medium (1-1.4 mm) or large (1.4-1.8 mm) granules, or unfractionated (naturally distributed) sludge. After >50 days of operation, the granule size distribution in each of the small, medium and large bioreactor types had diversified beyond - to both bigger and smaller than - the size fraction used for inoculation. New granules were analysed by studying community structure based on high-throughput 16S rRNA gene sequencing. Methanobacterium, Aminobacterium, Propionibacteriaceae and Desulfovibrio represented the majority of the community in new granules. H2-using, and not acetoclastic, methanogens appeared more important, and were associated with abundant syntrophic bacteria. Multivariate integration analyses identified distinct discriminant taxa responsible for shaping the microbial communities in different-sized granules, and along with alpha diversity data, indicated a possible biofilm life cycle.\n\nImportanceMethanogenic granules are spherical biofilms found in the built environment, where despite their importance for anaerobic digestion of wastewater in bioreactors, little is understood about the fate of granules across their entire life. Information on exactly how, and at what rates, methanogenic granules develop will be important for more precise and innovative management of environmental biotechnologies. Microbial aggregates also spark interest as subjects in which to study fundamental concepts from microbial ecology, including immigration and species sorting affecting the assembly of microbial communities. This experiment is the first, of which we are aware, to compartmentalise methanogenic granules into discrete, size-resolved fractions, which were then used to separately start up bioreactors to investigate the granule life cycle. The evidence, and extent, of de novo granule growth, and the identification of key microorganisms shaping new granules at different life-cycle stages, is important for environmental engineering and microbial ecology.

microbiology↗

Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics

The persistent inertia in the ability to culture environmentally abundant microbes from aquatic ecosystems represents an obstacle in disentangling the complex web of ecological interactions spun by a diverse assortment of participants (pro- and eukaryotes and their viruses). In aquatic microbial communities, the numerically most abundant actors, the viruses, remain the most elusive, and especially in freshwaters their identities and ecology remain obscure. Here, using ultra-deep metagenomic sequencing from freshwater habitats we recovered complete genomes of >2000 phages, including small \"miniphages\" and large \"megaphages\" infecting iconic prokaryotic lineages. We also show that many phages encode genes that likely enhance survival of infected microbes during strong eukaryotic grazing pressure. For instance, we describe genes that afford protection to their host from reactive oxygen species (ROS) in the environment and from the oxidative burst in protist phagolysosomes (phage-mediated ROS defense) or those that directly effect targeted killing of the predators upon ingestion of a phage-infected microbe (Trojan horse). Spatiotemporal abundance analyses of phage genomes revealed evanescence as the primary dynamic in upper water layers, where they displayed short-lived existences. In contrast, persistence was characteristic for the deeper layers where many identical phage genomes were recovered repeatedly. Phage and host abundances corresponded closely, with distinct populations displaying preferential distributions in different seasons and depths, closely mimicking overall stratification and mixis.

microbiology↗

Dirichlet-multinomial modelling outperforms alternatives for analysis of microbiome and other ecological count data

Molecular ecology regularly requires the analysis of count data that reflect the relative abundance of features of a composition (e.g., taxa in a community, gene transcripts in a tissue). The sampling process that generates these data can be modeled using the multinomial distribution. Replicate multinomial samples inform the relative abundances of features in an underlying Dirichlet distribution. These distributions together form a hierarchical model for relative abundances among replicates and sampling groups. This type of Dirichlet-multinomial modelling (DMM) has been described previously, but its benefits and limitations are largely untested. With simulated data, we quantified the ability of DMM to detect differences in proportions between treatment and control groups, and compared the efficacy of three computational methods to implement DMM--Hamiltonian Monte Carlo (HMC), variational inference (VI), and Gibbs Markov chain Monte Carlo. We report that DMM was better able to detect shifts in relative abundances than analogous analytical tools, while identifying an acceptably low number of false positives. Among methods for implementing DMM, HMC provided the most accurate estimates of relative abundances, and VI was the most computationally efficient. The sensitivity of DMM was exemplified through analysis of previously published data describing lung microbiomes. We report that DMM identified several potentially pathogenic, bacterial taxa as more abundant in the lungs of children who aspirated foreign material during swallowing; these differences went undetected with different statistical approaches. Our results suggest that DMM has strong potential as a statistical method to guide inference in molecular ecology.

bioinformatics↗

Invasion implies substitution in ecological communities with class-structured populations

Long-term evolution of quantitative traits is classically and usefully described as the directional change in phenotype due to the recurrent fixation of new mutations. A formal justification for such continual evolution ultimately relies on the "invasion implies substitution"-principle. Here, whenever a mutant allele causing a small phenotypic change can successfully invade a population, the ancestral (or wild-type) allele will be replaced, whereby fostering gradual phenotypic change if the process is repeated. It has been argued that this principle holds in a broad range of situations, including spatially and demographically structured populations experiencing frequency and density dependent selection under demographic and environmental fluctuations. However, prior studies have not been able to account for all aspects of population structure, leaving unsettled the conditions under which the "invasion implies substitution"-principle really holds. In this paper, we start by laying out a program to explore and clarify the generality of the "invasion implies substitution"-principle. Particular focus is given on finding an explicit and functionally constant representation of the selection gradient on a quantitative trait. Using geometric singular perturbation methods, we then show that the "invasion implies substitution"-principle generalizes to well-mixed and scalar-valued polymorphic multispecies ecological communities that are structured into finitely many demographic (or physiological) classes. The selection gradient is shown to be constant over the evolutionary timescale and that it depends only on the resident phenotype, individual growth-rates, population steady states and reproductive values, all of which are calculated from the resident dynamics. Our work contributes to the theoretical foundations of evolutionary ecology.

evolutionary biology↗