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Search indexed bioRxiv preprints in genomics, neuroscience, cell biology and bioinformatics. Read source abstracts and check manuscript versions; preprints are not peer reviewed.

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bioRxiv2016

Modeling the multiple facets of speciation-with-gene-flow towards improving divergence history inference of a recent fish adaptive radiation.

Parallel divergence patterns across replicated species pairs occurring in similar environmental contrasts may arise through distinct evolutionary scenarios. Deciphering whether such parallelism actually reflects repeated parallel divergence driven by divergent selection or a single divergence event with subsequent gene flow needs to be ascertained. Reconstructing historical gene flow is therefore of fundamental interest to understand how demography and selection jointly shaped genomic divergence during speciation. Here, we use an extended modeling framework to explore the multiple facets of speciation-with-gene-flow with demo-genetic divergence models that capture both temporal and genomic variation in effective population size and migration rate. We investigate the divergence history of five sympatric Lake Whitefish limnetic (dwarf) and benthic (normal) species pairs characterized by variable degrees of ecological divergence and reproductive isolation. Genome-wide SNPs were used to document the extent of genetic differentiation in each species pair, and 26 divergence models were fitted and compared to the unfolded joint allele frequency spectrum of each pair. We found evidence that a recent (circa 3000-4000 generations) asymmetrical secondary contact between expanding post-glacial populations has accompanied Whitefish diversification. Our results suggest that heterogeneous genomic differentiation patterns have emerged through the combined effects of linked selection generating variable rates of lineage sorting across the genome during geographical isolation, and heterogeneous introgression eroding divergence at different rates across the genome upon secondary contact. This study thus provides a new retrospective insight into the historical demographic and selective processes that shaped a continuum of divergence associated with ecological speciation.

Evolutionary Biology↗

bioRxiv2016

Reconstructing the backbone of the Saccharomycotina yeast phylogeny using genome-scale data

Understanding the phylogenetic relationships among the yeasts of the subphylum Saccharomycotina is a prerequisite for understanding the evolution of their metabolisms and ecological lifestyles. In the last two decades, the use of rDNA and multi-locus data sets has greatly advanced our understanding of the yeast phylogeny, but many deep relationships remain unsupported. In contrast, phylogenomic analyses have involved relatively few taxa and lineages that were often selected with limited considerations for covering the breadth of yeast biodiversity. Here we used genome sequence data from 86 publicly available yeast genomes representing 9 of the 11 major lineages and 10 non-yeast fungal outgroups to generate a 1,233-gene, 96-taxon data matrix. Species phylogenies reconstructed using two different methods (concatenation and coalescence) and two data matrices (amino acids or the first two codon positions) yielded identical and highly supported relationships between the 9 major lineages. Aside from the lineage comprised by the family Pichiaceae, all other lineages were monophyletic. Most interrelationships among yeast species were robust across the two methods and data matrices. However, 8 of the 93 internodes conflicted between analyses or data sets, including the placements of: the clade defined by species that have reassigned the CUG codon to encode serine, instead of leucine; the clade defined by a whole genome duplication; and of Ascoidea rubescens. These phylogenomic analyses provide a robust roadmap for future comparative work across the yeast subphylum in the disciplines of taxonomy, molecular genetics, evolutionary biology, ecology, and biotechnology. To further this end, we have also provided a BLAST server to query the 86 Saccharomycotina genomes, which can be found at http://y1000plus.org/blast.

Evolutionary Biology↗

bioRxiv2016

Trends in DNA methylation with age replicate across diverse human populations

Aging is associated with widespread changes in genome-wide patterns of DNA methylation. Thousands of CpG sites whose tissue-specific methylation levels are strongly correlated with chronological age have been previously identified. However, the majority of these studies have focused primarily on cosmopolitan populations living in the developed world; it is not known if age-related patterns of DNA methylation at these loci are similar across a broad range of human genetic and ecological diversity. We investigated genome-wide methylation patterns using saliva and whole blood derived DNA from two traditionally hunting and gathering African populations: the Baka of the western Central African rainforest and the =Khomani San of the South African Kalahari Desert. We identify hundreds of CpG sites whose methylation levels are significantly associated with age, thousands that are significant in a meta-analysis, and replicate trends previously reported in populations of non-African descent. We confirm that an age-associated site in the gene ELOVL2 shows a remarkably congruent relationship with aging in humans, despite extensive genetic and environmental variation across populations. We also demonstrate that genotype state at methylation quantitative trait loci (meQTLs) can affect methylation trends at some known age-associated CpG sites. Our study explores the relationship between CpG methylation and chronological age in populations of African hunter-gatherers, who rely on different diets across diverse ecologies. While many age-related CpG sites replicate across populations, we show that considering common genetic variation at meQTLs further improves our ability to detect previously identified age associations.

Genomics↗

bioRxiv2016

Pitfalls in Inferring Human Microbial Dynamics from Temporal Metagenomics Data

Human gut microbiota is a very complex and dynamic ecosystem that plays a crucial role in our health and well-being. Inferring microbial community structure and dynamics directly from time-resolved metagenomics data is key to understanding the community ecology and predicting its temporal behavior. Many methods have been proposed to perform the inference. Yet, we point out that there are several pitfalls along the way, from uninformative temporal measurements to the compositional nature of the relative abundance data, focusing on highly abundant species by ignoring or grouping low-abundance species, and implicit assumptions in various regularization methods. These issues have to be seriously considered in ecological modeling of human gut microbiota.

Bioinformatics↗

bioRxiv2016

Behavioral syndromes can reduce population density: behavior and demographic heterogeneity

Behavioral syndromes are widely recognized as important for ecology and evolution, but most predictions about ecological impacts are based on conceptual models and are therefore imprecise. Borrowing insights from the theory of demographic heterogeneity, we derived insights about the population-dynamic effects of behavioral syndromes. If some individuals are consistently more aggressive than others, not just in interspecific contests, but also in foraging, mating, and anti-predator behavior, then population dynamics could be affected by the resulting heterogeneity in demographic rates. We modeled a population with a boldness-aggressiveness syndrome (with the individual's trait constant through life), showing that the mortality cost of boldness causes aggressive individuals to die earlier, on average, than their non-aggressive siblings. The equilibrium frequency of the aggressive type is strongly affected by the mortality cost of boldness, but not directly by the reproductive benefit of aggressiveness. Introducing aggressive types into a homogeneous non-aggressive population increases the average per-capita mortality rate at equilibrium; under many conditions, this reduces the equilibrium density. One such condition is that the reproductive benefit of aggression is frequency dependent and the population has evolved to equalize the expected fitness of the two types. Finally, if the intensity of aggressiveness can evolve, then the population is likely to evolve to an evolutionarily stable trait value under biologically reasonable assumptions. This analysis shows how a formal model can predict both how a syndrome affects population dynamics and how the population processes constrain evolution of the trait; we suggest some concrete predictions.

Animal Behavior and Cognition↗

bioRxiv2016

Genetic correlations with climate variables suggest Caenorhabditis elegans natural niche preferences

Species inhabit a variety of environmental niches, and the adaptation to a particular niche is often controlled by genetic factors, including gene-by-environment interactions. The genes that vary in order to regulate the ability to colonize a niche are often difficult to identify, especially in the context of complex ecological systems and in experimentally uncontrolled natural environments. Quantitative genetic approaches provide an opportunity to investigate correlations between genetic factors and environmental parameters that might define a niche. Previously, we have shown how a collection of 208 whole-genome sequenced wild Caenorhabditis elegans can facilitate association mapping approaches. To correlate climate parameters with the variation found in this collection of wild strains, we used geographic data to exhaustively curate daily weather measurements in short-term (three month), middle-term (one year), and long-term (three year) durations surrounding the data of strain isolation. These climate parameters were then used as quantitative traits in the mapping approaches. We identified 10 QTL underlying variation in three traits: elevation, relative humidity, and average temperature. We then performed statistical analyses to further narrow the genomic interval of interest to identify gene candidates with variants potentially underlying phenotypic differences. Additionally, we performed two-strain competition assays at high and low temperatures to validate a QTL for temperature preference and found suggestive evidence that genotypes might be adapted to particular temperatures.\n\n100-word summary for G3Quantitative genetic approaches provide an opportunity to investigate correlations between genetic factors and environmental parameters that might define a niche, but these genes are difficult to identify, especially in the context of complex ecological systems. Here, we used a collection of 152 sequenced wild Caenorhabditis elegans to correlate climate parameters with the variation found in this collection of wild strains. We identified 10 QTL in five traits, including elevation, relative humidity, and temperature. Additionally, we performed competition assays to validate a QTL for temperature preference and found suggestive evidence that genotypes might be adapted to particular temperatures.

Genetics↗

bioRxiv2016

Deep-time parallel evolution of myrmecoid syndrome in rove beetle symbionts of army ants

Recent adaptive radiations provide striking examples of convergence, but the predictability of evolution over much deeper timescales is controversial, due to a scarcity of ancient clades exhibiting repetitive patterns of phenotypic evolution. Army ants are ecologically dominant arthropod predators of the world's tropics, with large nomadic colonies housing diverse communities of socially parasitic myrmecophiles. Remarkable among these are many species of rove beetle (Staphylinidae) that exhibit ant-mimicking \"myrmecoid\" body forms and are behaviorally accepted into their aggressive hosts' societies: emigrating with colonies and inhabiting temporary nest bivouacs, grooming and feeding with workers, but also consuming the brood. Here we demonstrate that myrmecoid rove beetles are strongly polyphyletic, with this novel adaptive morphological and behavioral syndrome having evolved at least twelve times during the evolution of a single staphylinid subfamily, Aleocharinae. Each independent myrmecoid clade is restricted to one zoogeographic region and highly host-specific on a single army ant genus. Dating estimates reveal that myrmecoid clades are separated by substantial phylogenetic distances--as much as 105 million years (My). All such groups arose in parallel during the Cenozoic, as army ants are proposed to have risen to ecological dominance. This work uncovers a rare example of an ancient system of complex morphological and behavioral convergence, with replicate beetle lineages following a predictable phenotypic trajectory during their parasitic coevolution with army ants.

Evolutionary Biology↗

bioRxiv2016

Genomic plasticity and rapid host switching promote the evolution of generalism in the zoonotic pathogen Campylobacter

Horizontal gene transfer accelerates bacterial adaptation to novel environments, allowing selection to act on genes that have evolved in multiple genetic backgrounds. This can lead to ecological specialization. However, little is known about how zoonotic bacteria maintain the ability to colonize multiple hosts whilst competing with specialists in the same niche. Here we develop a stochastic evolutionary model and show how genetic transfer of niche specifying genes and the opportunity for host transition can interact to promote the emergence of host generalist lineages of the zoonotic bacterium Campylobacter. Using a modelling approach we show that increasing levels of recombination enhance the efficiency with which selection can fix combinations of beneficial alleles, speeding adaptation. We then show how these predictions change in a multi-host system, with low levels of recombination, consistent with real r/m estimates, increasing the standing variation in the population, allowing a more effective response to changes in the selective landscape. Our analysis explains how observed gradients of host specialism and generalism can evolve in a multihost system through the transfer of ecologically important loci among coexisting strains.

Microbiology↗

bioRxiv2016

THE IDENTIFICATION OF SOURCE AND VECTOR OF A PROLIFIC MARINE INVADER

The source and vector of an introduced species inform its ecological and evolutionary history and may guide management that seeks to prevent future introductions. Surprisingly, few studies have successfully used genetic tools to independently inform the specific source and pathway of biological invasions. The ecological history of many introduced species, including their origins and vectors, is often based on suppositions or educated guesses. Here, we used mitochondrial and microsatellite genotyping to trace the invasion of the Asian seaweed Gracilaria vermiculophylla (Rhodophyta) along the three coastlines of the Northern Hemisphere to which it has been introduced: the western coast of North America, eastern coast of the United States and the coasts of Europe and northwest Africa. Analyzing 37 native and 53 introduced sites, we identified the Pacific coastline of northeastern Japan as the ultimate source of the Northern Hemisphere invasion. Coincidentally, most exports of the oyster Crassostrea gigas historically originated from this region and both species often grow in close proximity. Based on genetic signatures, each of the three coastlines likely received thalli directly from Japan, as well as material from another introduced coastline (i.e., a secondary invasion). Our ability to document a source region, which was enabled by a robust sampling of locations and loci that previous studies lacked, reflected strong phylogeographic structure along native coastlines. We suggest Gracilaria vermiculophylla is an important representative example of many species likely exported out of Japan by the oyster trade and its genetic signatures that may be a hallmark of oyster introduction legacies.

evolutionary biology↗

bioRxiv2016

The structured diversity of specialized gut symbionts of the New World army ants

Symbiotic bacteria play important roles in the biology of their arthropod hosts. Yet the microbiota of many diverse and influential groups remain understudied, resulting in a paucity of information on the fidelities and histories of these associations. Motivated by prior findings from a smaller scale, 16S rRNA-based study, we conducted a broad phylogenetic and geographical survey of microbial communities in the ecologically dominant New World army ants (Formicidae: Dorylinae). Amplicon sequencing of the 16S rRNA gene across 28 species spanning the five New World genera showed that the microbial communities of army ants consist of very few common and abundant bacterial species. The two most abundant microbes, referred to as Unclassified Firmicutes and Unclassified Entomoplasmatales, appear to be specialized army ant associates that dominate microbial communities in the gut lumen of three host genera, Eciton, Labidus and Nomamyrmex. Both are present in other army ant genera, including those from the Old World, suggesting that army ant symbioses date back to the Cretaceous. Extensive sequencing of bacterial protein-coding genes revealed multiple strains of these symbionts co-existing within colonies, but seldom within the same individual ant. Bacterial strains formed multiple host species-specific lineages on phylogenies, which often grouped strains from distant geographic locations. These patterns deviate from those seen in other social insects, and raise intriguing questions about the influence of army ant colony swarm-founding and within-colony genetic diversity on strain co-existence, and the effects of hosting a diverse suite of symbiont strains on colony ecology.

evolutionary biology↗

bioRxiv2016

Theory for the spatiotemporal interaction between lytic phages and biofilm-dwelling bacteria

Many bacteria are adapted for attaching to surfaces and for building complex communities, termed biofilms. The biofilm mode of life is predominant in bacterial ecology. So, too, is exposure of bacteria to ubiquitous viral pathogens, termed bacteriophages. Although biofilmphage encounters are likely to be very common in nature, little is known about how phages might interact with biofilm-dwelling bacteria. It is also unclear how the ecological dynamics of phages and their hosts depend on the biological and physical properties of the biofilm environment. To make headway in this area, here we develop the first biofilm simulation framework that captures key mechanistic features of biofilm growth and phage infection. Using these simulations, we find that the equilibrium state of interaction between biofilms and phages is governed largely by nutrient availability to biofilms, infection likelihood per host encounter, and the ability of phages to diffuse through biofilm populations. Interactions between the biofilm matrix and phage particles are thus likely to be of fundamental importance, controlling the extent to which bacteria and phages can coexist in natural contexts. Our results open avenues to new questions of host-parasite coevolution and horizontal gene transfer in spatially structured biofilm contexts.

microbiology↗

bioRxiv2016

A TOPOLOGICAL/ECOLOGICAL APPROACH TO PERCEPTION

During the exploration of the surrounding environment, the brain links together external inputs, giving rise to perception of a persisting object. During imaginative processes, the same object can be recalled in mind even if it is out of sight. In this proof of concept study, Borsuks theory of shape and the Borsuk-Ulam theorem provide a mathematical foundation for Gibsons notion of persistence perception. Gibsons ecological theory of perception accounts for our knowledge of world objects by borrowing a concept of invariance in topology. A series of transformations can be gradually applied to a pattern, in particular to the shape of an object, without affecting its invariant properties, such as boundedness of parts of a visual scene. High-level representations of objects in our environment are mapped to simplified views (our interpretations) of the objects, in order to construct a symbolic representation of the environment. The representations can be projected continuously to an ecological object that we have seen and continue to see, thanks to the mapping from shapes in our memory to shapes in Euclidean space.

neuroscience↗

bioRxiv2016

Giardia alters commensal microbial diversity throughout the murine gut

Giardia lamblia is the most frequently identified protozoan cause of intestinal infection. Over one billion people are estimated to have acute or chronic giardiasis, with infection rates approaching 90% in endemic areas. Despite its significance in global health, the mechanisms of pathogenesis associated with giardiasis remain unclear as the parasite neither produces a known toxin nor induces a robust inflammatory response. Giardia colonization and proliferation in the small intestine of the host may, however, disrupt the ecological homeostasis of gastrointestinal commensal microbes and contribute to diarrheal disease associated with giardiasis. To evaluate the impact of Giardia infection on the host microbiota, we use culture-independent methods to quantify shifts in the diversity of commensal microbes throughout the entire gastrointestinal tract in mice infected with Giardia. We discovered that Giardias colonization of the small intestine causes a systemic dysbiosis of aerobic and anaerobic bacterial taxa. Specifically, giardiasis is typified by both expansions in aerobic Proteobacteria and decreases in anaerobic Firmicutes and Melainabacteria in the murine foregut and hindgut. Based on these shifts, we created a quantitative index of murine Giardia-induced microbial dysbiosis. This index increased at all gut regions during the duration of infection, including both the proximal small intestine and the colon. Thus giardiasis could be an ecological disease, and the observed dysbiosis may be mediated directly via the parasites unique anaerobic fermentative metabolism or indirectly via parasite induction of gut inflammation. This systemic alteration of murine gut commensal diversity may be the cause or the consequence of inflammatory and metabolic changes throughout the gut. Shifts in the commensal microbiota may explain observed variation in giardiasis between hosts with respect to host pathology, degree of parasite colonization, infection initiation, and eventual clearance.

microbiology↗

bioRxiv2016

Climate-driven range shifts in fragmented ecosystems

Range shift is the primary short-term response of species to rapid climate change but it is hampered by natural or anthropogenic habitat fragmentation. Fragmented habitats expose different critical areas of a species niche to heterogeneous environmental changes resulting in uncoupled effects. Modelling species distribution under complex real-life scenarios and incorporating such uncoupled effects has not been achieved yet. Here we identify the most vulnerable areas and the potential cold refugia of a top-predator with fragmented niche range in the Southern ocean by integrating genomic, ecological and behavioural data with atmospheric and oceanographic models. Our integrative approach constitutes an indispensable example for predicting the effect of global warming on species relying on spatially and ecologically distinct areas to complete their life-cycle (e.g., migratory animals, marine pelagic organisms, central-place foragers) and, in general, on species constrained in fragmented landscapes due to continuously-growing anthropogenic pressure.

evolutionary biology↗

bioRxiv2016

Homeostasis Back and Forth: An Eco-Evolutionary Perspective of Cancer

The role of genetic mutations in cancer is indisputable: they are a key source of tumor heterogeneity and drive its evolution to malignancy. But the success of these new mutant cells relies on their ability to disrupt the homeostasis that characterizes healthy tissues. Mutated clones unable to break free from intrinsic and extrinsic homeostatic controls will fail to establish a tumor. Here we will discuss, through the lens of mathematical and computational modeling, why an evolutionary view of cancer needs to be complemented by an ecological perspective in order to understand why cancer cells invade and subsequently transform their environment during progression. Importantly, this ecological perspective needs to account for tissue homeostasis in the organs that tumors invade, since they perturb the normal regulatory dynamics of these tissues, often co-opting them for its own gain. Furthermore, given our current lack of success in treating advanced metastatic cancers through tumor centric therapeutic strategies, we propose that treatments that aim to restore homeostasis could become a promising venue of clinical research. This eco-evolutionary view of cancer requires mechanistic mathematical models in order to both integrate clinical with biological data from different scales but also to detangle the dynamic feedback between the tumor and its environment. Importantly, for these models to be useful, they need to embrace a higher degree of complexity than many mathematical modelers are traditionally comfortable with.

cancer biology↗

bioRxiv2016

Bacterial communities affected by experimental disturbances to canopy soils of a temperate rainforest

Trees of temperate rainforests host a large biomass of epiphytes, living plants associated with soils formed in the forest canopy. This study provides the first characterization of bacterial communities in canopy soils enabled by high-depth environmental sequencing of 16S rRNA genes. Canopy soil included many of the same major taxonomic groups of Bacteria that are also found in ground soil, but canopy bacterial communities were lower in diversity and contained different species-level operational taxonomic units. A field experiment was conducted to document changes in the bacterial communities of soils associated with epiphytic material that falls to the forest floor. Bacterial diversity and composition of canopy soil was highly similar, but not identical, to adjacent ground soil two years after transfer to the forest floor, indicating that canopy bacteria are almost, but not completely, replaced by ground soil bacteria. Furthermore, soil associated with epiphytic material on branches that were severed from the host tree and suspended in the canopy contained altered bacterial communities that were distinct from those in canopy material moved to the forest floor. Therefore, connection to the living tree is an important factor in the ecology of canopy soil bacteria. These results represent an initial survey of bacterial diversity of the canopy and provide a foundation upon which future studies can more fully investigate the ecological and evolutionary dynamics of these communities.\n\nIMPORTANCETemperate rainforests host large accumulations of epiphytes, plants that live on the branches of trees. This study provides a first look at the unique nature of bacterial communities in soil that is formed by the decomposition of epiphytes in the canopy of a temperate rainforest. Falling of epiphytic material results in the transfer of significant amounts of carbon and nutrients from the canopy to the forest floor. This study also experimentally documented how soil bacterial communities are affected by their movement from the canopy to the forest floor. The bacterial composition of canopy soil was altered by the severing of the epiphytic material from the living tree, even when the epiphytes remained in the canopy. Therefore, the unique nature of canopy soil bacteria is determined in part by the living host tree and not only by the physical environmental conditions associated with the canopy.

microbiology↗

bioRxiv2016

Population dynamics of synthetic Terraformation motifs

Ecosystems are complex systems, currently experiencing several threats associated with global warming, intensive exploitation, and human-driven habitat degradation. Such threats are pushing ecosystems to the brink of collapse. Because of a general presence of multiple stable states, including states involving population extinction, and due to intrinsic nonlinearities associated with feedback loops, collapse can occur in a catastrophic manner. Such catastrophic shifts have been suggested to pervade many of the future transitions affecting ecosystems at many different scales. Many studies have tried to delineate potential warning signals predicting such ongoing shifts but little is known about how such transitions might be effectively prevented. It has been recently suggested that a potential path to prevent or modify the outcome of these transitions would involve designing synthetic organisms and synthetic ecological interactions that could push these endangered systems out of the critical boundaries. Four classes of such ecological engineering designs or Terraformation motifs have been defined in a qualitative way. Here we develop the simplest mathematical models associated with these motifs, defining the expected stability conditions and domains where the motifs shall properly work.

synthetic biology↗

bioRxiv2016

Speciation trajectories in recombining bacterial species

While speciation in eukaryotes is well-studied, a controversy over the nature of bacterial species due to recombination between distant strains continues. It is generally agreed that bacterial diversity can be classified into genetically and ecologically cohesive units, but what produces such variation is a topic of intensive research. Recombination may maintain coherent species of frequently recombining bacteria, but the emergence of distinct clusters within a recombining species, and the impact of habitat structure in this process are not well described, limiting our understanding of how new species are created. Here we present a model of bacterial evolution in overlapping habitat space. We show three different outcomes are possible for a pair of clusters, depending on the size of their habitat overlap: fast divergence with little interaction between the clusters, slow divergence with frequent recombination between the clusters, and stationary or near stationary population structure, where the clusters remain at an equilibrium distance for an indefinite time. We fit our model to two data sets. In Streptococcus pneumoniae, we find a genomically and ecologically distinct subset, held at a relatively constant genetic distance from the majority of the population through frequent recombination with it, while in Campylobacter jejuni, we find a minority population we predict will continue to diverge at a higher rate. This approach may predict and define speciation trajectories in multiple bacterial species.

microbiology↗