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Tunable bet hedging in yeast responses to osmotic stress

Microbes limit risk by stochastic bet hedging - low frequency expression of less fit, slow growing cells constitutively preadapted against many stresses including antibiotics. By contrast, here we report continuous variation in the induced frequency of cells with slow osmotic stress signaling, survival and proliferation among 50 ecologically-distinct strains of budding yeast challenged by sudden hyperosmotic stress. Despite extensive variation in early mortality, strains displayed robust perfect adaptation and recovery of steady-state viability in moderate stress. In severe stress survival depended on strain-specific proportions of cells with divergent strategies. Cautious cells survived without dividing; reckless cells attempted to divide too soon and failed, killing both mother and daughter. We show that heritable frequencies of cautious and reckless cells produce a rapidly diversifying template for microbial bet hedging that mimics natural variation in stress responses whose timing, amplitude and frequency could evolve - be tuned by - different patterns of environmental stress.

Evolutionary Biology

Micro- and macroevolutionary trade-offs in plant-feeding insects

A long-standing hypothesis asserts that plant-feeding insects specialize on particular host plants because of negative interactions (trade-offs) between adaptations to alternative hosts, yet empirical evidence for such trade-offs is scarce. Most studies have looked for microevolutionary performance trade-offs within insect species, but host-use could also be constrained by macroevolutionary trade-offs caused by epistasis and historical contingency. On the other hand, evolutionary interactions between adaptations to diverse hosts could be neutral or positive rather than negative. Here we used a phylogenetic approach to estimate the micro-and macroevolutionary correlations between use of alternative host plants within two major orders of plant-feeding insects: Lepidoptera (caterpillars) and Hemiptera (true bugs). Across 1604 caterpillar species, we found both positive and negative pairwise correlations between use of diverse host taxa, with overall network patterns suggesting that different host-use constraints act over micro-and macroevolutionary timescales. In contrast, host-use patterns of 955 true bug species revealed uniformly positive correlations between presence on the same host taxa over both timescales. The lack of consistent patterns across timescales and insect orders indicates that host-use trade-offs are historically contingent rather than universal constraints. Moreover, we observed few negative correlations overall despite the wide taxonomic and ecological diversity of the focal host taxa, suggesting that positive interactions between host-use adaptations, not trade-offs, dominate the long-term evolution of host use in plant-feeding insects.

Evolutionary Biology

Evidence for selective attention in the insect brain

The capacity for selective attention appears to be required for any animal responding to an environment containing multiple objects, although this has been difficult to study in smaller animals such as insects. Clear operational characteristics of attention however make study of this crucial brain function accessible to any animal model. Whereas earlier approaches have relied on freely behaving paradigms placed in an ecologically relevant context, recent tethered preparations have focused on brain imaging and electrophysiology in virtual reality environments. Insight into brain activity during attention-like behavior has revealed key elements of attention in the insect brain. Surprisingly, a variety of brain structures appear to be involved, suggesting that even in the smallest brains attention might involve widespread coordination of neural activity.\n\nHighlightsO_LIInsect behavior shows attention-like filtering and allows concurrent neural recording\nC_LIO_LIRecent work finds compelling correlates of visual attention in the central complex\nC_LIO_LIPutative goal-directed stimulus-filtering is present in neuropils across the brain\nC_LI

Neuroscience

Common species link global ecosystems to climate change

Common species shape the world around us, and changes in their commonness signify large-scale shifts in ecosystem structure and function1-4. Dominant taxa drive productivity and biogeochemical cycling, in direct interaction with abiotic components of the Earth system3,4. However, our understanding of the dynamic response of ecosystems to global environmental changes in the past is limited by our ability to robustly estimate fossil taxonomic richness5,6, and by our neglect of the importance of common species. To rectify this, we use observations of the most common and widespread species to track global changes in their distribution in the deep geological past. Our simple approach is robust to factors that bias richness estimators, including widely used sampling-standardization methods5, which we show are highly sensitive to variability in the species-abundance distribution. Causal analyses of common species frequency in the deep-sea sedimentary record detect a lagged response in the ecological prominence of planktonic foraminifera to oceanographic changes captured by deep-ocean temperature records over the last 65 million years, encompassing one of Earth's major climate transitions. Our results demonstrate that common species can act as tracers of a past global ecosystem and its response to physical changes in Earth's dynamic history.

Paleontology

Wedding higher taxonomic ranks with metabolic signatures coded in prokaryotic genomes

Taxonomy of prokaryotes has remained a controversial discipline due to the extreme plasticity of microorganisms, causing inconsistencies between phenotypic and genotypic classifications. The genomics era has enhanced taxonomy but also opened new debates about the best practices for incorporating genomic data into polyphasic taxonomy protocols, which are fairly biased towards the identification of bacterial species. Here we use an extensive dataset of Archaea and Bacteria to prove that metabolic signatures coded in their genomes are informative traits that allow to accurately classify organisms coherently to higher taxonomic ranks, and to associate functional features with the definition of taxa. Our results support the ecological coherence of higher taxonomic ranks and reconciles taxonomy with traditional chemotaxonomic traits inferred from genomes. KARL, a simple and free tool useful for assisting polyphasic taxonomy or to perform functional prospections is also presented (https://github.com/giraola/KARL).

Microbiology

Absence of Genome Reduction In Diverse, Facultative Endohyphal Bacteria

Fungi interact closely with bacteria both on the surfaces of hyphae, and within their living tissues (i.e., endohyphal bacteria, EHB). These EHB can be obligate or facultative symbionts, and can mediate a diverse phenotypic traits in their hosts. Although EHB have been observed in many major lineages of fungi, it remains unclear how widespread and general these associations are, and whether there are unifying ecological and genomic features found across all EHB strains. We cultured 11 bacterial strains after they emerged from the hyphae of diverse Ascomycota that were isolated as foliar endophytes of cupressaceous trees, and generated nearly complete genome sequences for all. Unlike the genomes of largely obligate EHB, genomes of these facultative EHB resemble those of closely related strains isolated from environmental sources. Although all analyzed genomes encode structures that can be used to interact with eukaryotic hosts, we find no known pathways that facilitate intimate EHB-fungal interactions in all strains. We isolated two strains with nearly identical genomes from different classes of fungi, consistent with previous suggestions of horizontal transfer of EHB across endophytic hosts. Because bacteria are differentially present during the fungal life cycle, these genomes could shed light on the mechanisms of plant growth promotion by fungal endophytes during the symbiotic phase as well as degradation of plant material during saprotrophic and reproductive phases. Given the capacity of EHB to influence fungal phenotypes, these findings illuminate a new dimension of fungal biodiversity.

Microbiology

Evolutionary determinants of morphological polymorphism in colonial animals

Colonial animals commonly exhibit morphologically polymorphic modular units that are phenotypically distinct and specialize in specific functional tasks. But how and why these polymorphic modules have evolved is poorly understood. Across colonial invertebrates there is wide variation in the degree of polymorphism from none in colonial ascidians, to extreme polymorphism in siphonophores such as the Portuguese Man of War. Bryozoa are a phylum of exclusively colonial invertebrates that uniquely exhibit almost the entire range of polymorphism from monomorphic species to others that rival siphonophores in their polymorphic complexity. Previous approaches to understanding the evolution of polymorphism have been based upon analyses of (1) the functional role of polymorphs or (2) presumed evolutionary costs and benefits based upon evolutionary theory that postulates polymorphism should only be evolutionarily sustainable in more \"stable\" environments because polymorphism commonly leads to the loss of feeding and sexual competence. Here we use bryozoans from opposite shores of the Isthmus of Panama to revisit the environmental hypothesis by comparison of faunas from distinct oceanographic provinces that differ greatly in environmental variability and we then examine the correlations between the extent of polymorphism in relation to patterns of ecological succession and variation in life histories. We find no support for the environmental hypothesis. Distributions of the incidence of polymorphism in the oceanographically unstable Eastern Pacific are indistinguishable from those in the more stable Caribbean. In contrast, the temporal position of species in a successional sequence is collinear with the degree of polymorphism because species with fewer types of polymorphs are competitively replaced by species with higher numbers of polymorphs on the same substrata. Competitively dominant species also exhibit patterns of growth that increase their competitive ability. The association between degrees of polymorphism and variations in life histories is fundamental to understanding of the macroevolution of polymorphism.

Evolutionary Biology

Evidence and role for bacterial mucin degradation in cystic fibrosis airway disease

Chronic respiratory infections are composed of complex microbial communities that incite persistent inflammation and airway damage. Despite the high density of bacteria that colonize the airways, nutrient sources that sustain bacterial growth in vivo are unknown. Here we examine the role of respiratory mucins in the ecological dynamics of the cystic fibrosis lung microbiota. While P. aeruginosa was unable to efficiently utilize mucins, saliva-derived anaerobes stimulated the growth of opportunistic pathogens when provided mucins as the sole carbon source. The fermentative metabolisms of these oral anaerobes generated amino acids and short chain fatty acids (propionate and acetate) during mucin enrichment in vitro, which were also found within expectorated sputum from CF patients. The significance of these findings was supported by in vivo P. aeruginosa gene expression, which revealed a heightened response to propionate. Given that propionate is exclusively derived from bacterial fermentation, these data support a central role for mucin fermentation in the carbon flux of the lower airways. More specifically, commensal oral bacteria may contribute to airway disease by degrading mucins, in turn providing nutrients for pathogens otherwise unable to obtain carbon in the lung.

Microbiology

Approach-induced biases in human information sampling

Information sampling is often biased towards seeking evidence that confirms ones prior beliefs. Despite such biases being a pervasive feature of human behavior, their underlying causes remain unclear. Many accounts of these biases appeal to limitations of human hypothesis testing and cognition, de facto evoking notions of bounded rationality, but neglect more basic aspects of behavioral control. Here we demonstrate involvement of Pavlovian approach biases in determining which information humans will choose to sample. We collected a large novel dataset from 32,445 human subjects, making over 3 million decisions, who played a gambling task designed to measure the latent causes and extent of information-sampling biases. We identified three novel approach-related biases, formalized by comparing subject behavior to a dynamic programming model of optimal information gathering. These biases reflected the amount of information sampled ( positive evidence approach), the selection of which information to sample ( sampling the favorite), and the interaction between information sampling and subsequent choices ( rejecting unsampled options). The prevalence of all three biases was related to a Pavlovian approach-avoid parameter quantified within an entirely independent economic decision task. Our large dataset also revealed that individual differences in information seeking are a stable trait across multiple gameplays, and can be related to demographic measures including age and educational attainment. As well as revealing limitations in cognitive processing, our findings suggest information sampling biases reflect the expression of primitive, yet potentially ecologically adaptive, behavioral repertoires. One such behavior is sampling from options that will eventually be chosen, even when other sources of information are more pertinent for guiding future action.

Animal Behavior and Cognition

Promoter architecture and sex-specific gene expression in the microcrustacean Daphnia pulex revealed by large-scale profiling of 5′-mRNA ends

Large-scale identification of transcription start sites (TSSs) using Cap Analysis of Gene Expression (CAGE) has yielded insight into promoter location, architecture, and regulation for a small set of taxa representing major model organisms, including human. However, comparative and evolutionary genomics studies of cis-regulatory control of transcription initiation for a wider spectrum of Metazoa are still outstanding. To broaden our understanding of core promoter structure in species from metazoan clades with currently scant genome data, we sought to characterize the landscape of cis-regulatory elements in the microcrustacean water flea Daphnia pulex, an important model organism for studies in ecology, toxicology, and genetics. We performed CAGE from total RNA derived from three states: sexual females, asexual females, and males, reflecting distinct sexes and modes of reproduction. We mapped over 120 million CAGE reads to the D. pulex genome and generated a Daphnia promoter atlas containing 12,662 unique promoters. Characterization of the transcription initiation sites showed the expected enrichment of the CA-dinucleotide at TSSs [-1,1] (associated with Initiator-motif containing promoters) but also significant over-representation of GN-dinucleotides. Overall, these data suggest that D. pulex initiation sites are among the most GC-rich yet observed in metazoans. Computational de novo motif discovery around CAGE-identified TSSs revealed eight putative core promoter elements, including the canonical TATA (TATAWAA) and Initiator (CAGWY) motifs, as well as statistically significant motifs with no obvious orthologs in other metazoans. Analysis of the differentially-expressed genes suggests that a considerable number of cell cycle genes (each with net negative regulatory effects on meiosis) are upregulated in asexual females, providing a glimpse of the molecular events that underpin the cyclical parthenogenesis in D. pulex. Taken together, this work provides the first picture of transcription initiation and promoter architecture within Crustacea. The Daphnia promoter atlas we present here provides a basis for future study among Daphnia spp. as well as for comparative genomic analyses of metazoan transcriptional control.

Genomics

Microevolution of Bank Voles (Myodes glareolus) at Neutral and Immune Related Genes During Multiannual Dynamic Cycles: Consequences for Puumala hantavirus Epidemiology

Understanding how host dynamics, including variations of population size and dispersal, may affect the epidemiology of infectious diseases through ecological and evolutionary processes is an active research area. Here we focus on a bank vole (Myodes glareolus) metapopulation surveyed in Finland between 2005 and 2009. Bank vole is the reservoir of Puumala hantavirus (PUUV), the agent of nephropathia epidemica (NE, a mild form of hemorrhagic fever with renal symptom) in humans. M glareolus populations experience multiannual density fluctuations that may influence the level of genetic diversity maintained in bank voles, PUUV prevalence and NE occurrence. We examine bank vole metapopulation genetics at presumably neutral markers and immune-related genes involved in susceptibility to PUUV (Tnf-promoter, Mhc-Drb, Tlr4, Tlr7 and Mx2 gene) to investigate the links between population dynamics, microevolutionary processes and PUUV epidemiology. We show that genetic drift slightly and transiently affects neutral and adaptive genetic variability within the metapopulation. Gene flow seems to counterbalance its effects during the multiannual density fluctuations. The low abundance phase may therefore be too short to impact genetic variation in the host, and consequently viral genetic diversity. Environmental heterogeneity does not seem to affect vole gene flow, which might explain the absence of spatial structure previously detected in PUUV in this area. Besides, our results suggest the role of vole dispersal on PUUV circulation through sex-specific and density-dependent movements. We find little evidence of selection acting on immune-related genes within this metapopulation. Footprint of positive selection is detected at Tlr-4 gene in 2008 only. We observe marginally significant associations between Mhc-Drb haplotypes and PUUV serology, and between Mx2 genotype and PUUV genogroups. These results show that microevolutionary changes and PUUV epidemiology in this metapopulation are mainly driven by neutral processes, although the relative effects of neutral and adaptive forces could vary temporally with density fluctuations.

Evolutionary Biology

Do aye-ayes echolocate? Studying convergent genomic evolution in a primate auditory specialist

Several taxonomically distinct mammalian groups - certain microbats and cetaceans (e.g. dolphins) - share both morphological adaptations related to echolocation behavior and strong signatures of convergent evolution at the amino acid level across seven genes related to auditory processing. Aye-ayes (Daubentonia madagascariensis) are nocturnal lemurs with a derived auditory processing system. Aye-ayes tap rapidly along the surfaces of dead trees, listening to reverberations to identify the mines of wood-boring insect larvae; this behavior has been hypothesized to functionally mimic echolocation. Here we investigated whether there are signals of genomic convergence between aye-ayes and known mammalian echolocators. We developed a computational pipeline (BEAT: Basic Exon Assembly Tool) that produces consensus sequences for regions of interest from shotgun genomic sequencing data for non-model organisms without requiring de novo genome assembly. We reconstructed complete coding region sequences for the seven convergent echolocating bat-dolphin genes for aye-ayes and another lemur. Sequences were compared in a phylogenetic framework to those of bat and dolphin echolocators and appropriate non-echolocating outgroups. Our analysis reaffirms the existence of amino acid convergence at these loci among echolocating bats and dolphins; we also detected unexpected signals of convergence between echolocating bats and both mice and elephants. However, we observed no significant signal of amino acid convergence between aye-ayes and echolocating bats and dolphins; our results thus suggest that aye-aye tap-foraging auditory adaptations represent distinct evolutionary innovations. These results are also consistent with a developing consensus that convergent behavioral ecology is not necessarily a reliable guide to convergent molecular evolution.

Evolutionary Biology

Analytical considerations for comparative transcriptomics of wild organisms.

Comparative transcriptomics can now be conducted on organisms in natural settings, which has greatly enhanced understanding of genome-environment interactions. However, important data handling and quality control challenges remain, particularly when working with non-model species outside of a controlled laboratory environment. Here, we demonstrate the utility and potential pitfalls of comparative transcriptomics of wild organisms, with an example from three cyprinid fish species (Teleostei:Cypriniformes). We present computational solutions for processing, annotating and summarizing comparative transcriptome data for assessing genome-environment interactions across species. The resulting bioinformatics pipeline addresses the following points: (1) the potential importance of \"essential genes\", (2) the influence of microbiomes and other exogenous DNA, (3) potentially novel, species-specific genes, and (4) genomic rearrangements (e.g., whole genome duplication). Quantitative consideration of these points contributes to a firmer foundation for future comparative work across distantly related taxa for a variety of sub-disciplines, including stress and immune response, community ecology, ecotoxicology, and climate change.

Genomics

Eukaryotic Association Module in Phage WO Genomes from Wolbachia

Viruses are trifurcated into eukaryotic, archaeal and bacterial categories. This domain-specific ecology underscores why eukaryotic genes are typically co-opted by eukaryotic viruses and bacterial genes are commonly found in bacteriophages. However, the presence of bacteriophages in symbiotic bacteria that obligately reside in eukaryotes may promote eukayotic DNA transfers to bacteriophages. By sequencing full genomes from purified bacteriophage WO particles of Wolbachia, we discover a novel eukaryotic association module with various animal proteins domains, such as the black widow latrotoxin-CTD, that are uninterrupted in intact bacteriophage genomes, enriched with eukaryotic protease cleavage sites, and combined with additional domains to forge some of the largest bacteriophage genes (up to 14,256 bp). These various protein domain families are central to eukaryotic functions and have never before been reported in packaged bacteriophages, and their phylogeny, distribution and sequence diversity implies lateral transfer from animal to bacteriophage genomes. We suggest that the evolution of these eukaryotic protein domains in bacteriophage WO parallels the evolution of eukaryotic genes in canonical eukaryotic viruses, namely those commandeered for viral life cycle adaptations. Analogous selective pressures and evolutionary outcomes may occur in bacteriophage WO as a result of its \"two-fold cell challenge\" to persist in and traverse cells of obligate intracellular bacteria that strictly reside in animal cells. Finally, the full WO genome sequences and identification of attachment sites will advance eventual genetic manipulation of Wolbachia for disease control strategies.

Genomics

Allele Surfing Promotes Microbial Adaptation from Standing Variation

The coupling of ecology and evolution during range expansions enables mutations to establish at expanding range margins and reach high frequencies. This phenomenon, called allele surfing, is thought to have caused revolutions in the gene pool of many species, most evidently in microbial communities. It has remained unclear, however, under which conditions allele surfing promotes or hinders adaptation. Here, using microbial experiments and simulations, we show that, starting with standing adaptive variation, range expansions generate a larger increase in mean fitness than spatially uniform population expansions. The adaptation gain results from soft selective sweeps emerging from surfing beneficial mutations. The rate of these surfing events is shown to sensitively depend on the strength of genetic drift, which varies among strains and environmental conditions. More generally, allele surfing promotes the rate of adaptation per biomass produced, which could help developing biofilms and other resource-limited populations to cope with environmental challenges.

Evolutionary Biology

Radical changes persist longer in the absence of sex

Harmful mutations are ubiquitous and inevitable, and the rate at which these mutations are removed from populations is a critical determinant of evolutionary fate. Closely related sexual and asexual taxa provide a particularly powerful setting to study deleterious mutation elimination because sexual reproduction should facilitate mutational clearance by reducing selective interference between sites and by allowing the production of offspring with different mutational complements than their parents. Here, we compared the rate of removal of conservative (i.e., similar biochemical properties) and radical (i.e., distinct biochemical properties) nonsynonymous mutations from mitochondrial genomes of sexual vs. asexual Potamopyrgus antipodarum, a New Zealand freshwater snail characterized by coexisting and ecologically similar sexual and asexual lineages. Our analyses revealed that radical nonsynonymous mutations are cleared at higher rates than conservative changes and that sexual lineages eliminate radical changes more rapidly than asexual counterparts. These results are consistent with reduced efficacy of purifying selection in asexual lineages allowing harmful mutations to remain polymorphic longer than in sexual lineages. Together, these data illuminate some of the population-level processes contributing to mitochondrial mutation accumulation and suggest that mutation accumulation could influence the outcome of competition between sexual and asexual lineages.

Evolutionary Biology

The rate and effect of de novo mutations in natural populations of Arabidopsis thaliana

By following the evolution of populations that are initially genetically homogeneous, much can be learned about core biological principles. For example, it allows for detailed studies of the rate of emergence of de novo mutations and their change in frequency due to drift and selection. Unfortunately, in multicellular organisms with generation times of months or years, it is difficult to set up and carry out such experiments over many generations. An alternative is provided by \"natural evolution experiments\" that started from colonizations or invasions of new habitats by selfing lineages. With limited or missing gene flow from other lineages, new mutations and their effects can be easily detected. North America has been colonized in historic times by the plant Arabidopsis thaliana, and although multiple intercrossing lineages are found today, many of the individuals belong to a single lineage, HPG1. To determine in this lineage the rate of substitutions - the subset of mutations that survived natural selection and drift -, we have sequenced genomes from plants collected between 1863 and 2006. We identified 73 modern and 27 herbarium specimens that belonged to HPG1. Using the estimated substitution rate, we infer that the last common HPG1 ancestor lived in the early 17th century, when it was most likely introduced by chance from Europe. Mutations in coding regions are depleted in frequency compared to those in other portions of the genome, consistent with purifying selection. Nevertheless, a handful of mutations is found at high frequency in present-day populations. We link these to detectable phenotypic variance in traits of known ecological importance, life history and growth, which could reflect their adaptive value. Our work showcases how, by applying genomics methods to a combination of modern and historic samples from colonizing lineages, we can directly study new mutations and their potential evolutionary relevance.

Genomics

Convergent evolution of sperm gigantism and the developmental origins of sperm size variability in Caenorhabditis nematodes

Sperm cells provide crucial, if usually diminutive, ingredients to successful sexual reproduction as the source of centrioles and half the diploid genome. Despite this essential conserved function, sperm competition and coevolution with female traits can drive spectacular change in size and shape of these motile cells. Here we characterize four repeated instances of convergent evolution of sperm gigantism in Caenorhabditis nematodes using phylogenetic comparative methods on 26 species. Species at the extreme end of the 50-fold range of sperm-cell volumes across the genus have sperm capable of comprising up to 5% of egg-cell volume, representing severe attenuation of the magnitude of anisogamy. Exploring potential genetic and developmental determinants of Caenorhabditis sperm size variation, we uncover significant differences in mean and variance of sperm size among genotypes, between sexes of androdioecious species, as well as within and between individuals of identical genotypes. We demonstrate that the developmental basis of sperm size variation, both within and between species, becomes established during an early stage of sperm development, i.e. at the formation of primary spermatocytes while subsequent meiotic divisions contribute little further sperm size variability. These findings provide first insights into the developmental determinants of inter-and intraspecific sperm size differences in Caenorhabditis. Together, our results provide a novel integrative view on the developmental and evolutionary origins of Caenorhabditis sperm size variation. We hypothesize that life history and/or ecological differences among species favoured the evolution of alternative sperm competition strategies toward either many smaller sperm or fewer larger sperm, with gigantic sperm potentially providing a means of paternal care via gametic provisioning or as a potent vehicle for sexual conflict over offspring development.

Evolutionary Biology