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bioRxiv2020

One gene, multiple ecological strategies: a biofilm regulator is a capacitor for sustainable diversity

Many bacteria cycle between sessile and motile forms in which they must sense and respond to internal and external signals to coordinate appropriate physiology. Maintaining fitness requires genetic networks that have been honed in variable environments to integrate these signals. The identity of the major regulators and how their control mechanisms evolved remain largely unknown in most organisms. During four different evolution experiments with the opportunist betaproteobacterium Burkholderia cenocepacia in a biofilm model, mutations were most frequently selected in the conserved gene rpfR. RpfR uniquely integrates two major signaling systems -- quorum sensing and the motile-sessile switch mediated by cyclic-d-GMP -- by two domains that sense, respond to, and control synthesis of the autoinducer cis-2-dodecenoic acid (BDSF). The BDSF response in turn regulates activity of diguanylate cyclase and phosphodiesterase domains acting on cyclic-di-GMP. Parallel adaptive substitutions evolved in each of these domains to produce unique life history strategies by regulating cyclic-di-GMP levels, global transcriptional responses, biofilm production, and polysaccharide composition. These phenotypes translated into distinct ecology and biofilm structures that enabled mutants to coexist and produce more biomass than expected from their constituents grown alone. This study shows that when bacterial populations are selected in environments challenging the limits of their plasticity, the evolved mutations not only alter genes at the nexus of signaling networks but also reveal the scope of their regulatory functions. Significance statementMany organisms including bacteria live in fluctuating environments requiring attachment and dispersal. These lifestyle decisions require multiple external signals to be processed by several genetic pathways, but how they are integrated is largely unknown. We conducted multiple evolution experiments totaling >20,000 generations with Burkholderia cenocepacia populations grown in a model of the biofilm life cycle and identified parallel mutations in one gene, rpfR, that is a conserved central regulator. Because RpfR has multiple sensor and catalytic domains, different mutations can produce different ecological strategies that can coexist and even increase net growth. This study demonstrates that a single gene may coordinate complex life histories in biofilm-dwelling bacteria and that selection in defined environments can reshape niche breadth by single mutations.

microbiology↗

bioRxiv2020

Host evolutionary history and ecology shape virome composition in fishes

Revealing the determinants of virome composition is central to placing disease emergence in a broader evolutionary context. Fish are the most species-rich group of vertebrates and so provide an ideal model system to study the factors that shape virome compositions and their evolution. We characterised the viromes of 19 wild-caught species of marine fish using total RNA sequencing (meta-transcriptomics) combined with analyses of sequence and protein structural homology to identify divergent viruses that often evade characterisation. From this, we identified 25 new vertebrate-associated viruses and a further 22 viruses likely associated with fish diet or their microbiomes. The vertebrate-associated viruses identified here included the first fish virus in the Matonaviridae (single-strand, negative-sense RNA virus). Other viruses fell within the Astroviridae, Picornaviridae, Arenaviridae, Reoviridae, Hepadnaviridae, Paramyxoviridae, Rhabdoviridae, Hantaviridae, Filoviridae and Flaviviridae and were sometimes phylogenetically distinct from known fish viruses. We also show how key metrics of virome composition - viral richness, abundance and diversity - can be analysed along with host ecological and biological factors as a means to understand virus ecology. Accordingly, these data suggest that that the vertebrate-associated viromes of the fish sampled here are predominantly shaped by the phylogenetic history (i.e. taxonomic order) of their hosts, along with several biological factors including water temperature, habitat depth, community diversity and swimming behaviour. No such correlations were found for viruses associated with porifera, molluscs, arthropods, fungi and algae, that are unlikely to replicate in fish hosts. Overall, these data indicate that fish harbour particularly large and complex viromes and the vast majority of fish viromes are undescribed.

microbiology↗

bioRxiv2020

Working groups, gender and publication impact of Canada's ecology and evolution faculty

ABSTRACTA critical part of science is the extraction of general principles by synthesizing results from many different studies or disciplines. In the fields of ecology and evolution, a popular method to conduct synthesis science is in working groups – that is, research collaborations based around intensive week-long meetings. We present in this report an analysis of the impact of working group participation and gender on the publication impact of ecology and evolution faculty at Canadian universities who were research active over the last three decades (N=1408). Women are underrepresented in this research population relative to the general population, and even the Canadian faculty population. Participation in working groups not only benefits science, but also benefits the researchers involved by accelerating the temporal increase in their H-index. However, this benefit is particularly driven by senior male researchers. The effect is weaker for female researchers and even negative for researchers within 4 years of their PhD. However, gender does not affect current participation rates in working groups, nor reported indirect benefits – such as future collaborations, funding and data resources. The results of this study suggest that working groups can act as career catalysts for researchers, but that – as in many areas of science – there are challenging issues of equity that require action. Because the H-index is a cumulative measure, gender inequities from before the turn of the millenium may still be distorting the perceived publication impact of today’s research-active faculty.Competing Interest StatementThe authors have declared no competing interest.View Full Text

scientific communication and education↗

bioRxiv2020

Transparency in butterflies and moths: structural diversity, optical properties and ecological relevance

In water, transparency seems an ideal concealment strategy, as testified by the variety of transparent aquatic organisms. By contrast, transparency is nearly absent on land, with the exception of insect wings, and knowledge is scarce about its functions and evolution, with fragmentary studies and no comparative perspective. Lepidoptera (butterflies and moths) represent an outstanding group to investigate transparency on land, as species typically harbour opaque wings covered with coloured scales, a key multifunctional innovation. Yet, many Lepidoptera species have evolved partially or fully transparent wings. At the interface between physics and biology, the present study investigates transparency in 123 Lepidopteran species (from 31 families) for its structural basis, optical properties and biological relevance in relation to thermoregulation and vision. Our results establish that transparency has likely evolved multiple times independently. Efficiency at transmitting light is largely determined by clearwing microstructure (scale shape, insertion, colouration, dimensions and density) and macrostructure (clearwing area, species size or wing area). Microstructural traits - density, dimensions - are tightly linked in their evolution, with different constraints according to scale shape, insertion, and colouration. Transparency appears highly relevant for vision, especially for camouflage, with size-dependent and activity-rhythm dependent variations. Links between transparency and latitude are consistent with an ecological relevance of transparency in thermoregulation, and not so for protection against UV radiation. Altogether, our results shed new light on the physical and ecological processes driving the evolution of transparency on land and underline that transparency is a more complex than previously thought colouration strategy.

evolutionary biology↗

bioRxiv2020

Insights on long-distance dispersal, ecological and morphological evolution in the fern genus Microgramma from phylogenetic inferences

The epiphytic fern genus Microgramma (Polypodiaceae) comprises 30 species occurring mainly in the Neotropics with one species in Africa, being an example of trans-Atlantic disjunction. Morphologically and ecologically, Microgramma presents a wide variation that is not seen in its closest related genera. Recent works changed the circumscription of Microgramma to better conform with phylogenetic evidence, but no comprehensively sampled study has addressed the evolution of this lineage. This study aimed to investigate phylogenetic relationships, ecological and morphological evolution within Microgramma, as well as test the role of long-distant dispersal in the history of the genus. Sequences from five plastid regions were used to infer the phylogenetic relationships and estimate divergence times. Our results show five clades in Microgramma that do not corroborate any infrageneric classification system proposed. Several morphological traits seem to be homoplastic, such as leaf dimorphism. Tuber-like myrmecodomatia are suggested to be synapomorphic for one clade, although ant-plant association appears in two distinct lineages. Microgramma lycopodioides and M. mauritiana are not closely related, with the African species nested within an Atlantic Forest clade, indicating a long-distance dispersal event estimated to have occurred around 15 Ma from South America to Africa, followed by speciation.

plant biology↗

bioRxiv2020

The genetic architecture underlying ecological adaptation in Atlantic herring is not consistent with the infinitesimal model

Atlantic herring is widespread in North Atlantic and adjacent waters and is one of the most abundant vertebrates on earth. This species is well suited to explore genetic adaptation due to minute genetic differentiation at selectively neutral loci. Here we report hundreds of loci underlying ecological adaptation to different geographic areas and spawning conditions. Four of these represent megabase inversions confirmed by long read sequencing. The genetic architecture underlying ecological adaptation in the herring is in conflict with the infinitesimal model for complex traits because of the large shifts in allele frequencies at hundreds of loci under selection.

evolutionary biology↗

bioRxiv2020

Adaptive divergence of meiotic recombination rate in ecological speciation

Theories predict that directional selection during adaptation to a novel habitat results in elevated meiotic recombination rate. Yet the lack of population-level recombination rate data leaves this hypothesis untested in natural populations. Here we examine the population-level recombination rate variation in two incipient ecological species, the microcrustacean Daphnia pulex (an ephemeral-pond species) and D. pulicaria (a permanent-lake species). The divergence of D. pulicaria from D. pulex involved habitat shifts from pond to lake habitats as well as strong local adaptation due to directional selection. Using a novel single-sperm genotyping approach, we estimated the male-specific recombination rate of two linkage groups in multiple populations of each species in common garden experiments and identified a significantly elevated recombination rate in D. pulicaria. Most importantly, population genetic analyses show that the divergence in recombination rate between these two species is most likely due to divergent selection in distinct ecological habitats rather than neutral evolution. Significance statementWhether directional selection during adaptation to a novel habitat results in elevated meiotic recombination remains largely untested in natural populations. This work examines the population-level recombination rate in two closely related microcructacean species Daphnia pulex and D. pulicaria using single-sperm genotyping approach. Recombination rate data from two linkage groups show elevated recombination rates in D. pulicaria whose divergence from D. pulex is accompanied by a habitat shift. Importantly, population genetic analysis suggests that this divergence of recombination is likely adaptive rather than neutral.

evolutionary biology↗

bioRxiv2020

Granick Revisited: Synthesizing Evolutionary and Ecological Evidence for the Late Origin of Bacteriochlorophyll via Ghost Lineages and Horizontal Gene Transfer

Photosynthesis--both oxygenic and more ancient anoxygenic forms--has fueled the bulk of primary productivity on Earth since it first evolved more than 3.4 billion years ago. However, the early evolutionary history of photosynthesis has been challenging to interpret due to the sparse, scattered distribution of metabolic pathways associated with photosynthesis, long timescales of evolution, and poor sampling of the true environmental diversity of photosynthetic bacteria. Here, we reconsider longstanding hypotheses for the evolutionary history of phototrophy by leveraging recent advances in metagenomic sequencing and phylogenetics to analyze relationships among phototrophic organisms and components of their photosynthesis pathways, including reaction centers and individual proteins and complexes involved in the multi-step synthesis of (bacterio)-chlorophyll pigments. We demonstrate that components of the photosynthetic apparatus have undergone extensive, independent histories of horizontal gene transfer. This suggests an evolutionary mode by which modular components of phototrophy are exchanged between diverse taxa in a piecemeal process that has led to biochemical innovation. We hypothesize that the evolution of extant anoxygenic photosynthetic bacteria has been spurred by ecological competition and restricted niches following the evolution of oxygenic Cyanobacteria and the accumulation of O2 in the atmosphere, leading to the relatively late evolution of bacteriochlorophyll pigments and the radiation of diverse crown group anoxygenic phototrophs. This hypothesis expands on the classic "Granick hypothesis" for the stepwise evolution of biochemical pathways, synthesizing recent expansion in our understanding of the diversity of phototrophic organisms as well as their evolving ecological context through Earth history.

evolutionary biology↗

bioRxiv2020

Demographic inference provides insights into the extirpation and ecological dominance of eusocial snapping shrimps

Eusocial animals often achieve ecological dominance in the ecosystems where they occur, a process that may be linked to their demography. That is, reproductive division of labor and high reproductive skew in eusocial species is predicted to result in more stable effective population sizes that may make groups more competitive, but also lower effective population sizes that may make groups more susceptible to inbreeding and extinction. We examined the relationship between demography and social organization in one of the few animal lineages where eusociality has evolved recently and repeatedly among close relatives, the Synalpheus snapping shrimps. Although eusocial species often dominate the reefs where they occur by outcompeting their non-eusocial relatives for access to sponge hosts, many eusocial species have recently become extirpated across the Caribbean. Coalescent-based historical demographic inference in 12 species found that across nearly 100,000 generations, eusocial species tended to have lower but more stable effective population sizes through time. Our results are consistent with the idea that stable population sizes may enable eusocial shrimps to be more competitively dominant, but they also suggest that recent population declines are likely caused by eusocial shrimps heightened sensitivity to anthropogenically-driven environmental changes as a result of their low effective population sizes and localized dispersal, rather than to natural cycles of inbreeding and extinction. Thus, although the unique life histories and demography of eusocial shrimps has likely contributed to their persistence and ecological dominance over evolutionary timescales, these social traits may also make them vulnerable to contemporary environmental change.

evolutionary biology↗

bioRxiv2020

Application of an ecology-based analytic approach to discriminate signal and noise in low-biomass microbiome studies: whole lung tissue is the preferred sampling method for amplicon-based characterization of murine lung microbiota

BackgroundLow-biomass microbiome studies (such as those of the lungs, placenta, and skin) are vulnerable to contamination and sequencing stochasticity, which obscure legitimate microbial signal. Since low-biomass microbiome fields have had variable success in establishing the reality and clinical significance of identified microbiota, we sought to develop and apply an analytical approach to discriminate signal from noise in low-biomass microbiome studies. We used this approach to determine the optimal sampling strategy in murine lung microbiome studies, which will be essential for future mechanistic lung microbiome research. MethodsUsing a novel, ecology-based analytic approach, we compared bacterial DNA from the lungs of healthy adult mice collected via two common sampling approaches: homogenized whole lung tissue and bronchoalveolar lavage (BAL) fluid. We quantified bacterial DNA using droplet digital PCR, characterized bacterial communities using 16S rRNA gene sequencing, and systematically assessed the quantity and identity of bacterial DNA in both specimen types. We compared bacteria detected in lung specimens to each other and to potential source communities: negative (background) control specimens and paired oral samples. FindingsBy all measures, whole lung tissue in mice contained greater bacterial signal and less evidence of contamination than did BAL fluid. Relative to BAL fluid, whole lung tissue exhibited a greater quantity of bacterial DNA, distinct community composition, decreased sample-to-sample variation, and greater biological plausibility when compared to potential source communities. In contrast, bacteria detected in BAL fluid were minimally different from those of procedural, reagent, and sequencing controls. InterpretationAn ecology-based analytical approach discriminates signal from noise in low-biomass microbiome studies and identifies whole lung tissue as the preferred specimen type for murine lung microbiome studies. Sequencing, analysis, and reporting of potential source communities, including negative control specimens and contiguous biological sites, is crucial for biological interpretation of low-biomass microbiome studies, independent of specimen type. FundingNational Institutes of Health

microbiology↗

bioRxiv2020

First draft genome of the Labyrinthula genus, an opportunistic seagrass pathogen, reveals novel insight into marine protist phylogeny, ecology and CAZyme cell-wall degradation

Labyrinthula spp. are saprobic, marine protists that also act as opportunistic pathogens and are the causative agents of seagrass wasting disease (SWD). Despite the threat of local- and large-scale SWD outbreaks, there are currently gaps in our understanding of the drivers of SWD, particularly surrounding Labyrinthula virulence and ecology. Given these uncertainties, we investigated Labyrinthula from a novel genomic perspective by presenting the first draft genome and predicted proteome of a pathogenic isolate of Labyrinthula SR_Ha_C, generated from a hybrid assembly of Nanopore and Illumina sequences. Phylogenetic and cross-phyla comparisons revealed insights into the evolutionary history of Stramenopiles. Genome annotation showed evidence of glideosome-type machinery and an apicoplast protein typically found in protist pathogens and parasites. Proteins involved in Labyrinthulas actin-myosin mode of transport, as well as carbohydrate degradation were also prevalent. Further, CAZyme functional predictions revealed a repertoire of enzymes involved in breakdown of cell-wall and carbohydrate storage compounds common to seagrasses. The relatively low number of CAZymes annotated from the genome of Labyrinthula SR_Ha_C compared to other Labyrinthulea species may reflect the conservative annotation parameters, a specialised substrate affinity and the scarcity of characterised protist enzymes. Inherently, there is high probability for finding both unique and novel enzymes from Labyrinthula spp. This study provides resources for further exploration of Labyrinthula ecology and evolution, and will hopefully be the catalyst for new hypothesis-driven SWD research revealing more details of molecular interactions between Labyrinthula species and its host substrate.

genomics↗

bioRxiv2020

LEA 3: Factor models in population genetics and ecological genomics with R

A major objective of evolutionary biology is to understand the processes by which organisms have adapted to various environments, and to predict the response of organisms to new or future conditions. The availability of large genomic and environmental data sets provides an opportunity to address those questions, and the R package LEA has been introduced to facilitate population and ecological genomic analyses in this context. By using latent factor models, the program computes ancestry coefficients from population genetic data, and performs genotype-environment association analyses with correction for unobserved confounding variables. In this study, we present new functionalities of LEA, which include imputation of missing genotypes, fast algorithms for latent factor mixed models using multivariate predictors for genotype-environment association studies, population differentiation tests for admixed or continuous populations, and estimation of genetic offset based on climate models. The new functionalities are implemented in version 3.0 and higher releases of the package. Using simulated and real data sets, our study provides evaluations and examples of applications, outlining important practical considerations when analyzing ecological genomic data in R.

evolutionary biology↗

bioRxiv2020

Machine learning (decision tree analysis) identifies ecological selectivity patterns across the end-Permian mass extinction

Decision tree algorithms are rarely utilized in paleontological research, and here we show that machine learning algorithms can be used to identify determinants of extinction as well as predict extinction risk. This application of decision tree algorithms is important because the ecological selectivity of mass extinctions can reveal critical information on organismic traits as key determinants of extinction and hence the causes of extinction. To understand which factors led to the mass extinction of life during an extreme global warming event, we quantified the ecological selectivity of marine extinctions in the well-studied South China region during the end-Permian mass extinction using the categorized gradient boosting algorithm. We find that extinction selectivity varies between different groups of organisms and that a synergy of multiple environmental stressors best explains the overall end-Permian extinction selectivity pattern. Extinction risk was greater for genera that were limited to deep-water habitats, had a stationary mode of life, possessed a siliceous skeleton or, less critically, had calcitic skeletons. These selective losses directly link the extinction to the environmental effects of rapid injections of carbon dioxide into the ocean-atmosphere system, specifically the combined effects of expanded oxygen minimum zones, rapid warming, and ocean acidification.

evolutionary biology↗

bioRxiv2020

Phylogeny, morphology, and ecology resurrect previously synonymized species of North American Stereum

Stereum is an exceedingly common but taxonomically confounding genus of basidiomycete fungus with a cosmopolitan distribution. Lack of consensus about morphological and geographic boundaries of many Stereum species has resulted in a lack of consistency in identification of physical specimens, a problem that cascades to their associated published DNA sequences. A critical initial step towards addressing these issues is determining the scope of the problem. Here, we first use integrative taxonomy to delimit species in the North American Stereum ostrea complex. We use morphological and ecological characters, alongside ITS rDNA sequences of specimens from midwestern and eastern North America to show that "Stereum ostrea" in this region is a complex of at least three reproductively isolated sister species: S. lobatum, S. fasciatum, and S. subtomentosum. We then extend lessons from this case study to a set of publicly available Stereum ITS sequences to assess the accuracy of species names represented by existing sequence data. ASAP species delimitation successfully discriminates among the three newly revealed species in the S. ostrea species complex, but also reveals considerable cryptic diversity across global Stereum and widespread inconsistency in application of species names. Though ITS alone should not be used to delimit species or describe evolutionary relationships, its application here helps direct new hypotheses and suggests several areas of Stereum taxonomy that require revision. The critical future work of disentangling Stereum taxonomy and evolution should combine a multilocus genetic approach with morphology, ecology, and a global sampling strategy.

evolutionary biology↗

bioRxiv2020

Microbiomes attached to fresh perennial ryegrass- are temporally resilient and adapt to changing ecological niches

Gut microbiomes, such as the rumen, greatly influence host nutrition due to their feed energy-harvesting capacity. We investigated temporal ecological interactions facilitating energy-harvesting at the fresh perennial ryegrass (PRG)-biofilm interface in the rumen using an in sacco approach and prokaryotic metatranscriptomic profiling. Network analysis identified two distinct sub-microbiomes primarily representing primary ([≤]4h) and secondary ([≥]4h) colonisation phases and the most transcriptionally active bacterial families (i.e Fibrobacteriaceae, Selemondaceae and Methanobacteriaceae) did not interact with either sub-microbiome, indicating non-cooperative behaviour. Conversely, Prevotellaceae had most transcriptional activity within the primary sub-microbiome (focussed on protein metabolism) and Lachnospiraceae within the secondary sub-microbiome (focussed on carbohydrate degradation). Putative keystone taxa, with low transcriptional activity, were identified within both sub-microbiomes, highlighting the important synergistic role of minor bacterial families, however, we hypothesise that they may be cheating in order to capitalise on the energy-harvesting capacity of other microbes. In terms of chemical cues underlying transition from primary to secondary colonisation phases, we suggest that AI-2 based quorum sensing plays a role, based on LuxS gene expression data, coupled with changes in PRG chemistry. In summary, this study provides the first major insight into the complex temporal ecological interactions occurring at the plant-biofilm interface within the rumen.

microbiology↗

bioRxiv2020

Transcriptomic divergence predicts morphological and ecological variation underlying an adaptive radiation

Groups of sympatric taxa with low inter-specific genetic differentiation, but considerable ecological differences, offer great opportunities to study the dynamics of divergence and speciation. This is the case of ciscoes (Coregonus spp.) in the Laurentian Great Lakes, which are characterized by a complex evolutionary history and are commonly described as having undergone an adaptive radiation. In this study, morphometrics, stable isotopes and transcriptome sequencing were used to study the relationships within the Coregonus artedi complex in western Lake Superior. We observed general concordance for morphological, ecological and genomic variation, but the latter was more taxonomically informative as it showed less overlap among species in multivariate space. Low levels of genetic differentiation were observed between individuals morphologically identified as C. hoyi and C. zenithicus, and we hypothesize this could be associated with recent hybridization between the two species. Transcriptome-based single nucleotide polymorphisms exhibited significant divergence for genes associated with vision, development, metabolism and immunity, among species that occupy different habitats. This study highlights the importance of using an integrative approach when studying groups of taxa with a complex evolutionary history, as individual-level analyses of multiple independent datasets can provide a clearer picture of the patterns and processes associated with the origins of biodiversity.

evolutionary biology↗

bioRxiv2020

The Wood Image Analysis and Dataset (WIAD): open-access visual analysis tools to advance the ecological data revolution

O_LIEcological data is collected and shared at an increasingly rapid pace, but it is often shared in inconsistent and untraceable processed forms. Images of wood contain a wealth of information such as colours and textures but are most commonly reduced to ring-width measurements before they can be shared in various common file formats. Archiving digital images of wood samples in libraries, that have been developed for ecological analysis and are publicly available, remains the exception. C_LIO_LIWe developed the Wood Image Analysis and Dataset (WIAD) an open-source application including a web-interface to integrate basic visual analysis of wood samples, such as increment cores, thin sections or x-ray films, basic data processing, and archiving of the images and derived data to facilitate transparency and reproducibility in studies using visual characteristics of wood. C_LIO_LIWIAD provides user-friendly tools to manipulate images of wood samples, mark and measure wood characteristics such as growth increments, density fluctuations, early- and latewood widths, and fire scars, and to visualise, process, and archive images, metadata, and the derived data. C_LIO_LIWIAD constitutes a step towards the reproducible automation of tree-ring analysis, while establishing an open-source foundation to create improved community developed repositories which would enable novel ecological studies harnessing the wealth of existing visual data. C_LI

plant biology↗

bioRxiv2020

How do ecological and social environments reflect parental roles in birds? A comparative analysis

Parental roles are highly diverse in animal taxa. Since caring is an important determinant of fitness, understanding the origin and maintenance of various parental care strategies is a key question in evolutionary biology. Here we investigate parental care patterns in birds, which exhibit a remarkable diversity of parental sex roles. By means of phylogenetically informed comparative analyses we investigate whether and how care provisioning is predicted by ecology and social environment. Making use of the most comprehensive dataset including 1101 species that represent 126 avian families, we show that sex differences in parental care are neither related to food type nor to nest type, two key ecological factors. However, we found an effect of the social environment, as males tend to care relatively more in in colonial species than in non-colonial species. Taken together, these results highlight the importance of social effects for evolution of diverse parental sex roles.

evolutionary biology↗