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bioRxiv2014

New whole genome de novo assemblies of three divergent strains of rice (O. sativa) documents novel gene space of aus and indica

The use of high throughput genome-sequencing technologies has uncovered a large extent of structural variation in eukaryotic genomes that makes important contributions to genomic diversity and phenotypic variation. Currently, when the genomes of different strains of a given organism are compared, whole genome resequencing data are aligned to an established reference sequence. However when the reference differs in significant structural ways from the individuals under study, the analysis is often incomplete or inaccurate. Here, we use rice as a model to explore the extent of structural variation among strains adapted to different ecologies and geographies, and show that this variation can be significant, often matching or exceeding the variation present in closely related human populations or other mammals. We demonstrate how improvements in sequencing and assembly technology allow rapid and inexpensive de novo assembly of next generation sequence data into high-quality assemblies that can be directly compared to provide an unbiased assessment. Using this approach, we are able to accurately assess the \"pan-genome\" of three divergent rice varieties and document several megabases of each genome absent in the other two. Many of the genome-specific loci are annotated to contain genes, reflecting the potential for new biological properties that would be missed by standard resequencing approaches. We further provide a detailed analysis of several loci associated with agriculturally important traits, illustrating the utility of our approach for biological discovery. All of the data and software are openly available to support further breeding and functional studies of rice and other species.

Genomics↗

bioRxiv2014

Unravelling the diversity behind Ophiocordyceps unilateralis complex: Three new species of Zombie-Ant fungus from Brazilian Amazon

In tropical forests, one of the most common relationships between parasites and insects is that between the fungus Ophiocordyceps (Ophiocordycipitaceae, Hypocreales, Ascomycota) and ants, especially within the tribe Camponotini. These fungi have the ability to penetrate the exoskeleton of the ant and to manipulate the behavior of the host, making it leave the nest and ascend understorey shrubs, to die biting onto the vegetation: hence, the term zombie-ant fungi to describe this behavioral changes on the host. It is posited that this behavioral change aids spore dispersal and thus increases the chances of infection. Despite their undoubted importance for ecosystem functioning, these fungal pathogens are still poorly documented, especially regarding their diversity, ecology and evolutionary relationships. Here, we describe three new and host-specific species of the genus Ophiocordyceps on Camponotus ants from the central Amazonian region of Brazil which can readily be separated using classic taxonomic criteria, in particular ascospore morphology. In addition, we also employed molecular techniques to show for the first time the phylogenetic relationships between these taxa and closely related species within the Ophiocordyceps unilateralis complex, as well as with other members of the family Ophiocordycipitaceae.

Evolutionary Biology↗

bioRxiv2014

Evolutionary Multiplayer Games

Evolutionary game theory has become one of the most diverse and far reaching theories in biology. Applications of this theory range from cell dynamics to social evolution. However, many applications make it clear that inherent non-linearities of natural systems need to be taken into account. One way of introducing such non-linearities into evolutionary games is by the inclusion of multiple players. An example is of social dilemmas, where group benefits could e.g. increase less than linear with the number of cooperators. Such multiplayer games can be introduced in all the fields where evolutionary game theory is already well established. However, the inclusion of non-linearities can help to advance the analysis of systems which are known to be complex, e.g. in the case of non-Mendelian inheritance. We review the diachronic theory and applications of multiplayer evolutionary games and present the current state of the field. Our aim is a summary of the theoretical results from well-mixed populations in infinite as well as finite populations. We also discuss examples from three fields where the theory has been successfully applied, ecology, social sciences and population genetics. In closing, we probe certain future directions which can be explored using the complexity of multiplayer games while preserving the promise of simplicity of evolutionary games.

Evolutionary Biology↗

bioRxiv2014

Novel Natural Product Discovery from Marine Sponges and their Obligate Symbiotic Organisms

Discovery of novel natural products is an accepted method for the elucidation of pharmacologically active molecules and drug leads. Best known sources for such discovery have been terrestrial plants and microbes, accounting for about 85% of the approved natural products in pharmaceutical use (1), and about 60% of approved pharmaceuticals and new drug applications annually (2). Discovery in the marine environment has lagged due to the difficulty of exploration in this ecological niche. Exploration began in earnest in the 1950s, after technological advances such as scuba diving allowed collection of marine organisms, primarily at a depth to about 15m.\n\nNatural products from filter feeding marine invertebrates and in particular, sponges, have proven to be a rich source of structurally unique pharmacologically active compounds, with over 16,000 molecules isolated thus far (3, 1) and a continuing pace of discovery at hundreds of novel bioactive molecules per year. All classes of pharmaceuticals have been represented in this discovery process, including antiprotazoals, pesticides, TGF-beta inhibitors, cationic channel blockers, anticancer, cytotoxic, antiviral, anti-inflammatory and antibacterial compounds. Important biosynthetic pathways found in sponges which give rise to these compounds include the terpenoid (4), fatty acid, polyketoid, quinone reductase, alkaloid, isoprenoid (5), and non-ribosomal protein synthase pathways.

Pharmacology and Toxicology↗

bioRxiv2014

Complete plastid genome assembly of invasive plant, Centaurea diffusa

New genomic tools are needed to elucidate the evolution of invasive, non-model organisms. Here we present the completed plastome assembly for the problematic invasive weed, Centaurea diffusa. This new tool represents a significant contribution to future studies of the ecological genomics of invasive plants, particularly this weedy genus, and studies of the Asteraceae in general.

Genomics↗

bioRxiv2014

Mesoscale analyses of fungal networks as an approach for quantifying phenotypic traits

We investigate the application of mesoscopic response functions (MRFs) to characterize a large set of networks of fungi and slime moulds grown under a wide variety of different experimental treatments, including inter-species competition and attack by fungivores. We construct structural networks by estimating cord conductances (which yield edge weights) from the experimental data, and we construct functional networks by calculating edge weights based on how much nutrient traffic is predicted to occur along each edge. Both types of networks have the same topology, and we compute MRFs for both families of networks to illustrate two different ways of constructing taxonomies to group the networks into clusters of related fungi and slime moulds. Although both network taxonomies generate intuitively sensible groupings of networks across species, treatments, and laboratories, we find that clustering using the functional-network measure appears to give groups with lower intra-group variation in species or treatments. We argue that MRFs provide a useful quantitative analysis of network behaviour that can (1) help summarize an expanding set of increasingly complex biological networks and (2) help extract information that captures subtle changes in intra-specific and inter-specific phenotypic traits that are integral to a mechanistic understanding of fungal behaviour and ecology. As an accompaniment to our paper, we also make a large data set of fungal networks available in the public domain.

Plant Biology↗

bioRxiv2014

A plea for evidence in ecosystem service science: a framework and its application

The ecosystem service concept is at the interface of ecology, economics and politcs, with scientific results rapidly translated into management or political action. This emphasises the importance of reliable recommendations provided by scientist. We propose to use evidence-based practice in ecosystem service science in order to evaluate and improve the reliability of scientific statements. For this purpose, we introduce a level-of-evidence scale ranking study designs (e.g. review, case-control, descriptive) in combination with a study quality checklist. For illustration, the concept was directly applied to 12 case studies. We also review criticisms levered against evidence-based practice and how it applies to ecosystem services science. We further discuss who should use the evidence-based concept and suggest important next steps, with a focus on the development of guidelines for methods used in ecosystem service assessments.

Scientific Communication and Education↗

bioRxiv2014

Non-respiratory functions of Saccharomyces cerevisiae mitochondria are required for optimal attractiveness to Drosophila melanogaster

While screening a large collection of wild and laboratory yeast isolates for their ability to attract Drosophila melanogaster adults, we noticed a large difference in fly preference for two nearly isogenic strains of Saccharomyces cerevisiae, BY4741 and BY4742. Using standard genetic analyses, we tracked the preference difference to the lack of functional mitochondria the stock of BY4742 used in the initial experiment. We used gas chromatography coupled with mass spectroscopy to examine the volatile compounds produced by BY4741 and the mitochondria-deficient BY4742, and found they differed significantly. We found that several ethyl esters are present at much higher levels in strains with functional mitochondria, even in fermentative conditions. We confirmed the role of these ethyl esters in attraction by examining an EEB1{Delta} strain which reduces ethyl ester production. We found that nitrogen levels in the substrate affect the production of these compounds, and that they are produced at high levels by strains with functional mitochondria in the fermentation of natural substrates. Collectively these observations demonstrate the effect core metabolic processes have in mediating the interaction between yeasts and insect vectors, and highlight the importance of non-respirative mitochondrial functions in yeast ecology.

Genetics↗

bioRxiv2014

Century-scale methylome stability in a recently diverged Arabidopsis thaliana lineage

There has been much excitement about the possibility that exposure to specific environments can induce an ecological memory in the form of whole-sale, genome-wide epigenetic changes that are maintained over many generations. In the model plant Arabidopsis thaliana, numerous heritable DNA methylation differences have been identified in greenhouse-grown isogenic lines, but it remains unknown how natural, highly variable environments affect the rate and spectrum of such changes. Here we present detailed methylome analyses in a geographically dispersed A. thaliana population that constitutes a collection of near-isogenic lines, diverged for at least a century from a common ancestor. We observed little DNA methylation divergence whole-genome wide. Nonetheless, methylome variation largely reflected genetic distance, and was in many aspects similar to that of lines raised in uniform conditions. Thus, even when plants are grown in varying and diverse natural sites, genome-wide epigenetic variation accumulates in a clock-like manner, and epigenetic divergence thus parallels the pattern of genome-wide DNA sequence divergence.

Genomics↗

bioRxiv2014

Analysis of geographic patterns of molecular, morphological, and bioclimatic variation to evaluate hypotheses of species boundaries in the South American montane genus Escallonia (Escalloniaceae)

Escallonia is a morphologically and ecologically diverse clade of shrubs and small trees widely distributed in three hotspots of plant diversity. Previous studies suggested that extant species may have radiated rapidly and/or recently resulting in complex patterns of molecular variation across this genus. This result is apparently mirrored in morphology because species also display complex and overlapping patterns of morphological variation. Taken together, these patterns call into question the identity of all species within Escallonia. To evaluate the currently proposed hypotheses of species boundaries, I used molecular, morphological, and bioclimatic a data for 35 species and assessed three species criteria: genealogical exclusivity, morphological gaps, and climatic niche differences. Interpreting these data in the context of species as segments of evolutionary lineages, I provide evidence that most species (ca. 70%) within Escallonia represent distinct species on independent evolutionary trajectories. Instead of rejecting the current hypotheses of species limit, I argue for taxonomic stability as it provides a useful framework for studies aiming to understand the mechanisms driving the origin and evolution of species in hotspots of biodiversity.

Evolutionary Biology↗

bioRxiv2014

Phinch: An interactive, exploratory data visualization framework for –Omic datasets

Using environmental sequencing approaches, we now have the ability to deeply characterize biodiversity and biogeographic patterns in understudied, uncultured microbial taxa (investigations of bacteria, archaea, and microscopic eukaryotes using 454/Illumina sequencing platforms). However, the sheer volume of data produced from these new technologies requires fundamentally different approaches and new paradigms for effective data analysis. Scientific visualization represents an innovative method towards tackling the current bottleneck in bioinformatic workflows. In addition to giving researchers a unique approach for exploring large datasets, it stands to empower biologists with the ability to conduct powerful analyses without requiring a deep level of computational knowledge. Here we present Phinch, an interactive, browser-based visualization framework that can be used to explore and analyze biological patterns in high-throughput -Omic datasets. This project takes advantage of standard file formats from computational pipelines in order to bridge the gap between biological software (e.g. microbial ecology pipelines) and existing data visualization capabilities (harnessing the flexibility and scalability of technologies such as HTML5).

Genomics↗

bioRxiv2014

Antimicrobial peptides play a functional role in bumblebee anti-trypanosome defense

Bumblebees, amongst the most important of pollinators, are under enormous population pressures. One of these is disease. The bumblebee and its gut trypanosome Crithidia bombi are one of the fundamental models of ecological immunology. Although there is previous evidence of increased immune gene expression upon Crithidia infection, recent work has focussed on the bumblebees gut microbiota. Here, by knocking down gene expression using RNAi, we show for the first time that antimicrobial peptides (AMPs) have a functional role in anti-Crithidia defense.

Immunology↗

bioRxiv2014

The developmental transcriptome of contrasting Arctic charr (Salvelinus alpinus) morphs

Species showing repeated evolution of similar traits can help illuminate the molecular and developmental basis of diverging traits and specific adaptations. Following the last glacial period, dwarfism and specialized bottom feeding morphology evolved rapidly in several landlocked Arctic charr (Salvelinus alpinus) populations in Iceland. To initiate study of the genetic divergence between small benthic morphs and larger morphs with limnetic morphotype, we conducted an RNA-seq transcriptome analysis of developing charr. We sequenced mRNA from whole embryos at four stages in early development of two stocks with contrasting morphologies, the small benthic (SB) charr from Lake Thingvallavatn and Holar aquaculture (AC) charr.\n\nThe data reveal significant differences in expression of several biological pathways during charr development. There was also an expression difference between SB- and AC-charr in genes involved in energy metabolism and blood coagulation genes. We confirmed expression difference of five genes in whole embryos with qPCR, including lysozyme and natterin like which was previously identified as a fish-toxin of a lectin family that may be a putative immunopeptide. We also verified differential expression of 7 genes in developing heads, that associated consistently with benthic v.s. limnetic craniofacial morphology (studied in 4 morphs total). Comparison of Single nucleotide polymorphism (SNP) frequencies reveals extensive genetic differentiation between the SB- and AC-charr (60 fixed SNPs and around 1300 differing by more than 50% in frequency). In SB-charr the high frequency derived SNPs are in genes related to translation and oxidative processes. Curiously, three derived alleles in the otherwise conserved 12s and 16s mitochondrial ribosomal RNA genes are found in benthic charr.\n\nThe data implicate multiple genes and molecular pathways in divergence of small benthic charr and/or the response of aquaculture charr to domestication. Functional, genetic and population genetic studies on more freshwater and anadromous populations are needed to confirm the specific loci and mutations relating to specific ecological or domestication traits in Arctic charr.

Evolutionary Biology↗

bioRxiv2014

Global geographic patterns of sexual size dimorphism in birds: Support for a latitudinal trend?

Sexual size dimorphism (SSD) is widespread among animals, and is a common indication of differential selection among males and females. Sexual selection theory predicts that SSD should increase as one sex competes more fiercely for access to mates, but it is unclear what effect spatial variation in ecology may have on this behavioral process. Here, we examine SSD across the class Aves in a spatial and phylogenetic framework, and test several a priori hypotheses regarding its relationship with climate. We mapped the global distribution of SSD from published descriptions of body size, distribution, and phylogenetic relationships across 2581 species of birds. We examined correlations between SSD and nine predictor variables representing a priori models of physical geography, climate, and climate variability. Our results show guarded support for a global latitudinal trend in SSD based on a weak prevalence of species with low or female-biased SSD in the North, but substantial spatial heterogeneity. While several stronger relationships were observed between SSD and climate predictors within zoogeographical regions, no global relationship emerged that was consistent across multiple methods of analysis. While we found support for a global relationship between climate and SSD, this support lacked consistency and explanatory power. Furthermore the strong phylogenetic signal and conspicuous lack of support from phylogenetically corrected analyses suggests that any such relationship in birds is likely due to the idiosyncratic histories of different lineages. In this manner, our results broadly agree with studies in other groups, leading us to conclude that the relationship between climate and SSD is at best complex. This suggests that SSD is linked to behavioral dynamics that may at a global scale be largely independent of environmental conditions.

Evolutionary Biology↗

bioRxiv2014

Synthesis of phylogeny and taxonomy into a comprehensive tree of life

Reconstructing the phylogenetic relationships that unite all lineages (the tree of life) is a grand challenge. The paucity of homologous character data across disparately related lineages currently renders direct phylogenetic inference untenable. To reconstruct a comprehensive tree of life we therefore synthesized published phylogenies, together with taxonomic classifications for taxa never incorporated into a phylogeny. We present a draft tree containing 2.3 million tips -- the Open Tree of Life. Realization of this tree required the assembly of two additional community resources: 1) a novel comprehensive global reference taxonomy; and 2) a database of published phylogenetic trees mapped to this taxonomy. Our open source framework facilitates community comment and contribution, enabling the tree to be continuously updated when new phylogenetic and taxonomic data become digitally available. While data coverage and phylogenetic conflict across the Open Tree of Life illuminate gaps in both the underlying data available for phylogenetic reconstruction and the publication of trees as digital objects, the tree provides a compelling starting point for community contribution. This comprehensive tree will fuel fundamental research on the nature of biological diversity, ultimately providing up-to-date phylogenies for downstream applications in comparative biology, ecology, conservation biology, climate change, agriculture, and genomics.

Evolutionary Biology↗

bioRxiv2014

Host-parasite coevolution in populations of constant and variable size

The matching-allele and gene-for-gene models are widely used in mathematical approaches that study the dynamics of host-parasite interactions. Agrawal and Lively (Evolutionary Ecology Research 4:79-90, 2002) captured these two models in a single framework and numerically explored the associated time discrete dynamics of allele frequencies. Here, we present a detailed analytical investigation of this unifying framework in continuous time and provide a generalization. We extend the model to take into account changing population sizes, which result from the antagonistic nature of the interaction and follow the Lotka-Volterra equations. Under this extension, the population dynamics become most complex as the model moves away from pure matching-allele and becomes more gene-for-gene-like. While the population densities oscillate with a single oscillation frequency in the pure matching-allele model, a second oscillation frequency arises under gene-for-gene-like conditions. These observations hold for general interaction parameters and allow to infer generic patterns of the dynamics. Our results suggest that experimentally inferred dynamical patterns of host-parasite coevolution should typically be much more complex than the popular illustrations of Red Queen dynamics. A single parasite that infects more than one host can substantially alter the cyclic dynamics.

Evolutionary Biology↗

bioRxiv2015

Rethinking inheritance, yet again: inheritomes, contextomes and dynamic phenotypes

In recent years, there have been many calls for an extended evolutionary synthesis, based in part upon growing evidence for non-genetic mechanisms of inheritance, i.e., similarities in phenotype between parents and offspring that are not due to shared genes. While there has been an impressive marshalling of evidence for diverse forms of non-genetic inheritance (epigenetic, ecological, behavioural, symbolic), there have been relatively few studies trying to integrate the different forms of inheritance into a common conceptual structure, a development that would be important to formalizing elements of the extended evolutionary synthesis. Here, we propose a framework for an extended view of inheritance and introduce some conceptual distinctions that we believe are important to this issue. In this framework, the phenotype is conceived of as a dynamic entity, its state at any point in time resulting from intertwined effects of previous phenotypic state, and of hereditary materials (DNA and otherwise) and environment. We contrast our framework with the standard gene-based view of inheritance, and also discuss our framework in the specific context of recent attempts to accommodate non-genetic inheritance within the framework of classical quantitative genetics and the Price equation. In particular, we believe that the extended view of inheritance and effects on the phenotype developed here is particularly well-suited to individual-based simulation studies of evolutionary dynamics. The results of such simulations, in turn, could be useful for assessing how well extended models based on quantitative genetics or the Price equation perform at capturing complex evolutionary dynamics.

Evolutionary Biology↗

bioRxiv2015

SWS2 visual pigment evolution as a test of historically contingent patterns of plumage color evolution in Warblers

Distantly related clades that occupy similar environments may differ due to the lasting imprint of their ancestors - historical contingency. The New World warblers (Parulidae) and Old World warblers (Phylloscopidae) are ecologically similar clades that differ strikingly in plumage coloration. We studied genetic and functional evolution of the short-wavelength sensitive visual pigments (SWS2 and SWS1) to ask if altered color perception could contribute to the plumage color differences between clades. We show SWS2 is short-wavelength shifted in birds that occupy open environments, such as finches, compared to those in closed environments, including warblers. Sequencing of opsin genes and phylogenetic reconstructions indicate New World warblers were derived from a finch-like form that colonized from the Old World 15-20Ma. During this process the SWS2 gene accumulated 6 substitutions in branches leading to New World warblers, inviting the hypothesis that passage through a finch-like ancestor resulted in SWS2 evolution. In fact, we show spectral tuning remained similar across warblers as well as the finch ancestor. Results reject the hypothesis of historical contingency based on opsin spectral tuning, but point to evolution of other aspects of visual pigment function. Using the approach outlined here, historical contingency becomes a generally testable theory in systems where genotype and phenotype can be connected.

Evolutionary Biology↗