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Complex multicellularity in fungi: evolutionary convergence, single origin, or both?

Complex multicellularity comprises the most advanced level of organization evolved on Earth. It has evolved only a few times in metazoans, green plants, brown and red algae and fungi. Compared to other lineages, the evolution of multicellularity in fungi follows different principles; both simple and complex multicellularity evolved via unique mechanisms not seen in other lineages. In this article we review ecological, paleontological, developmental and genomic aspects of complex multicellularity in fungi and discuss the general principles of the evolution of complex multicellularity in light of its fungal manifestations. Fungi represent the only lineage in which complex multicellularity shows signatures of convergent evolution: it appears 8-12 distinct fungal lineages, which show a patchy phylogenetic distribution, yet share some of the genetic mechanisms underlying complex multicellular development. To mechanistically explain the patchy distribution of complex multicellularity across the fungal tree of life we identify four key observations that need to be considered: the large number of apparently independent complex multicellular clades; the lack of documented phenotypic homology between these; the universal conservation of gene circuits regulating the onset of complex multicellular development; and the existence of clades in which the evolution of complex multicellularity is coupled with limited gene family diversification. We discuss how these patterns and known genetic aspects of fungal development can be reconciled with the genetic theory of convergent evolution to explain its pervasive occurrence in across the fungal tree of life.

evolutionary biology

Rapid diversification of Pseudomonas aeruginosa in cystic fibrosis lung-like conditions

Chronic infection of the cystic fibrosis (CF) airway by the opportunistic pathogen Pseudomonas aeruginosa is the leading cause of morbidity and mortality for adult CF patients. Prolonged infections are accompanied by adaptation of P. aeruginosa to the unique conditions of the CF lung environment as well as marked diversification of the pathogen into phenotypically and genetically distinct strains that can coexist for years within a patient. Little is known, however, about the causes of this diversification and its impact on patient health. Here, we show experimentally that, consistent with ecological theory of diversification, the nutritional conditions of the CF airway can cause rapid and extensive diversification of P. aeruginosa. The increased viscosity associated with the thick mucous layer in the CF airway had little impact on within-population diversification but did promote divergence among populations. Notably, in vitro evolution recapitulated patho-adaptive traits thought to be hallmarks of chronic infection, including reduced motility and increased biofilm formation, and the range of phenotypes observed in a collection of clinical isolates. Our results suggest that nutritional complexity and reduced dispersal can drive evolutionary diversification of P. aeruginosa independent of other features of the CF lung such as an active immune system or the presence of competing microbial species. They also underscore the need to obtain diverse samples of P. aeruginosa when developing treatment plans. We suggest that diversification, by generating extensive phenotypic and genetic variation on which selection can act, may be a key first step in the transition from transient to chronic infection.\n\nSignificance StatementChronic infection with the opportunistic pathogen Pseudomonas aeruginosa is the leading cause of lung transplant or death in cystic fibrosis patients. P. aeruginosa diversifies in the CF lung, although why this happens remains a mystery. We allowed P. aeruginosa to evolve in the laboratory under a range of conditions approximating the CF lung. The diversity of evolved populations was highest, and most closely resembled the range of phenotypes among clinical isolates, in environments resembling the spectrum of nutritional resources available in the CF lung. Our results point to the nutritional complexity of the CF lung as a major driver of diversification and they suggest that diversity could be important in the development of chronic infections.

evolutionary biology

Rarefaction, alpha diversity, and statistics

Understanding the drivers of microbial diversity is a fundamental question in microbial ecology. Extensive literature discusses different methods for describing microbial diversity and documenting its effects on ecosystem function. However, it is widely believed that diversity depends on the number of reads that are sequenced. I discuss a statistical perspective on diversity, framing the diversity of an environment as an unknown parameter, and discussing the bias and variance of plug-in and rarefied estimates. I argue that by failing to account for both bias and variance, we invalidate analysis of alpha diversity. I describe the state of the statistical literature for addressing these problems, and suggest that measurement error modeling can address issues with variance, but bias corrections need to be utilized as well. I encourage microbial ecologists to avoid motivating their investigations with alpha diversity analyses that do not use valid statistical methodology.

microbiology

Epithelial stratification shapes infection dynamics

Infections of stratified epithelia collectively represent a large burden on global health. Experimental models provide a means to understand how the cell dynamics themselves influence the outcomes of these infections. Mathematical approaches are needed to improve quantification and theoretical advancement of these complex systems. Here, we develop a general ecology-inspired model for stratified epithelial dynamics, which allows us to simulate infections and to estimate parameters that are difficult to measure with organotypic cell cultures. To explore how epithelial cell dynamics affect infection dynamics, we focus on two contrasting pathogens of the cervicovaginal epithelium: Chlamydia trachomatis and Human papillomaviruses. We find that key infection symptoms stem from differential interactions with the layers, while clearance and pathogen burden are bottom-up processes. Cell protective responses to infections (e.g. increased cell proliferation) generally lowered pathogen load but there were specific effects based on infection strategies. These generic responses by the epithelium, then, will have varying results depending on the pathogens infection strategy. Our modeling approach opens new perspectives for 3D tissue culture experimental systems of infections and, more generally, for developing and testing hypotheses related to infections of stratified epithelia.

systems biology

High-dimensional microbiome interactions shape host fitness

Gut bacteria can affect key aspects of host fitness, such as development, fecundity, and lifespan, while the host in turn shapes the gut microbiome. Microbiomes co-evolve with their hosts and have been implicated in host speciation. However, it is unclear to what extent individual species versus community interactions within the microbiome are linked to host fitness. Here we combinatorially dissect the natural microbiome of Drosophila melanogaster and reveal that interactions between bacteria shape host fitness through life history tradeoffs. We find that the same microbial interactions that shape host fitness also shape microbiome abundances, suggesting a potential evolutionary mechanism by which microbiome communities (rather than just individual species) may be intertwined in co-selection with their hosts. Empirically, we made germ-free flies colonized with each possible combination of the five core species of fly gut bacteria. We measured the resulting bacterial community abundances and fly fitness traits including development, reproduction, and lifespan. The fly gut promoted bacterial diversity, which in turn accelerated development, reproduction, and aging: flies that reproduced more died sooner. From these measurements we calculated the impact of bacterial interactions on fly fitness by adapting the mathematics of genetic epistasis to the microbiome. Host physiology phenotypes were highly dependent on interactions between bacterial species. Higher-order interactions (involving 3, 4, and 5 species) were widely prevalent and impacted both host physiology and the maintenance of gut diversity. The parallel impacts of bacterial interactions on the microbiome and on host fitness suggest that microbiome interactions may be key drivers of evolution.\n\nSignificanceAll animals have associated microbial communities called microbiomes that can influence the physiology and fitness of their host. It is unclear to what extent individual microbial species versus ecology of the microbiome influences fitness of the host. Here we mapped all the possible interactions between individual species of bacteria with each other and with the hosts physiology. Our approach revealed that the same bacterial interactions that shape microbiome abundances also shape host fitness traits. This relationship provides a feedback that may favor the emergence of co-evolving microbiome-host units.

microbiology

Metagenomic signature of natural strongyle infection in susceptible and resistant horses

Gastrointestinal strongyles are a major threat to horses' health and welfare. Given that strongyles inhabit the same niche as the gut microbiota, they may interact with each other. These beneficial or detrimental interactions are unknown in horses and could partly explain contrasted susceptibility to infection between individuals. To address these questions, an experimental pasture trial with 20 worm-free female Welsh ponies (10 susceptible (S) and 10 resistant (R) to parasite infection) was implemented for five months. Fecal egg counts (FEC), hematological and biochemical data, body weight and gut microbiota composition were studied in each individual after 0, 24, 43, 92 and 132 grazing days.\n\nThe predicted R ponies exhibited lower FEC after 92 and 132 grazing days, and showed higher levels of circulating monocytes and eosinophils, while S ponies developed lymphocytosis by the end of the trial. Although the overall microbiota diversity remained similar between the two groups, R and S ponies exhibited sustained differential abundances in Clostridium XIVa, Ruminococcus, Acetivibrio and unclassified Lachnospiracea at day 0. These bacteria may hence contribute to the intrinsic pony resistance towards strongyle infection. Moreover, Paludibacter, Campylobacter, Bacillus, Pseudomonas, Clostridium III, Acetivibrio, members of the unclassified Eubacteriaceae and Ruminococcaceae and fungi loads were increased in infected S ponies, suggesting that strongyle and fungi may contribute to each others success in the ecological niche of the equine intestines. In contrast, butyrate-producing bacteria such as Ruminococcus, Clostridium XIVa and members of the Lachnospiraceae family decreased in S relative to R ponies. Additionally, these gut microbiota alterations induced changes in several immunological pathways in S ponies, including pathogen sensing, lipid metabolism, and activation of signal transduction that are critical for the regulation of immune system and energy homeostasis. These observations shed light on a putative implication of the gut microbiota in the intrinsic resistance to strongyle infection.\n\nOverall, this longitudinal study provides a foundation to better understand the mechanisms that underpin the relationship between host susceptibility to strongyle infection, immune response and gut microbiota under natural conditions in horses and should contribute to the development of novel biomarkers of strongyle susceptibility and provide additional control options.

systems biology

Fitness traits of deoxynivalenol and nivalenol-producing Fusarium graminearum species complex strains from wheat

Fusarium graminearum of the 15-acetyl(A)deoxynivalenol(D0N) chemotype is the main cause of Fusarium head blight (FHB) of wheat in south of Brazil. However, 3-ADON and nivalenol(NIV) chemotypes have been found in other members of the species complex causing FHB in wheat. To improve our understanding of the pathogen ecology, we assessed a range of fitness-related traits in a sample of 30 strains representatives of 15-ADON (F. graminearum), 3-ADON (F. cortaderiae and F. austroamericanum) and NIV (F. meridionale and F. cortaderiae). These included: perithecia formation on three cereal-based substrates, mycelial growth at two suboptimal temperatures, sporulation and germination, pathogenicity towards a susceptible and a moderately resistant cultivar and sensitivity to tebuconazole. The most important trait favoring F. graminearum was its 2x higher sexual fertility (> 40% PPI = perithecia production index) than the other species (< 30% PPI); PPI varied among substrates (maize > rice > wheat). In addition, sensitivity to tebuconazole appeared lower in F. graminearum which had the only strain with EC50 > 1 ppm. In the pathogenicity assays, the DON-producers were generally more aggressive (1.5 to 2x higher final severity) towards the two cultivars, with 3-ADON or 15-ADON leading to higher area under the severity curve than the NIV strains in the susceptible and moderately resistant cv., respectively. There was significant variation among strains of a same species with regards asexual fertility (mycelial growth, macroconidia production and germination), which suggest a strain-rather than a species-specific differences. These results contribute new knowledge to improve our understanding of the pathogen-related traits that may explain the dominance of certain members of the species complex in specific wheat agroecosystems.

microbiology

Selective attention controls olfaction in rodents

Critical animal behaviors, especially among rodents, are guided by odors in remarkably well-coordinated manners. While many extramodal sensory cues compete for cognitive resources in these ecological contexts, that rodents can engage in such odor-guided behaviors suggests that they selectively attend to odors. We developed a behavioral paradigm to reveal that rats are indeed capable of selectively attending to odors in the presence of competing extramodal stimuli and found that this selective attention facilitates accurate odor-guided decisions. Further, we uncovered that attention to odors adaptively sharpens their representation among neurons in a brain region considered integral for odor-driven behaviors. Thus, selective attention contributes to olfaction by enhancing the coding of odors in a manner analogous to that observed among other sensory systems.

neuroscience

Division of labor during biofilm matrix production

Organisms as simple as bacteria can engage in complex collective actions, such as group motility and fruiting body formation. Some of these actions involve a division of labor, where phenotypically specialized clonal subpopulations, or genetically distinct lineages cooperate with each other by performing complementary tasks. Here, we combine experimental and computational approaches to investigate potential benefits arising from division of labor during biofilm matrix production. We show that both phenotypic and genetic strategies for a division of labor can promote collective biofilm formation in the soil bacterium Bacillus subtilis. In this species, biofilm matrix consists of two major components; EPS and TasA. We observed that clonal groups of B. subtilis phenotypically segregate into three subpopulations composed of matrix non-producers, EPS-producers, and generalists, which produce both EPS and TasA. This incomplete phenotypic specialization was outperformed by a genetic division of labor, where two mutants, engineered as specialists, complemented each other by exchanging EPS and TasA. The relative fitness of the two mutants displayed a negative frequency dependence both in vitro and on plant roots, with strain frequency reaching a stable equilibrium at 30% TasA-producers, corresponding exactly to the population composition where group productivity is maximized. Using individual-based modelling, we show that asymmetries in strain ratio can arise due to differences in the relative benefits that matrix compounds generate for the collective; and that genetic division of labor can be favored when it breaks metabolic constraints associated with the simultaneous production of two matrix components.\n\nHighlights- matrix components EPS and TasA are costly public goods in B. subtilis biofilms\n\n- genetic division of labor using {Delta}eps and {Delta}tasA fosters maximal biofilm productivity\n\n- {Delta}eps and {Delta}tasA cooperation is evolutionary stable in laboratory and ecological systems\n\n- costly metabolic coupling of public goods favors genetic division of labor

microbiology

Hydrogen production by Sulfurospirillum spp. enables syntrophic interactions of Epsilonproteobacteria

Hydrogen-producing bacteria are of environmental and biotechnological importance in anoxic environments, since hydrogen is an important electron donor for prokaryotes and of interest as an alternative energy source. Epsilonproteobacteria, inhabiting ecologically, clinically or biotechnologically relevant environments, are currently considered to be hydrogen-oxidizing bacteria exclusively. Here, we report hydrogen production for a genus of free-living Epsilonproteobacteria, Sulfurospirillum spp. inhabiting sediments, wastewater plants, bioelectrodes, oil reservoirs, contaminated areas, or marine habitats. The amount of hydrogen production was largely different in two subgroups of Sulfurospirillum spp., represented by S. cavolei and S. multivorans. The former is shown to be the more potent hydrogen producer and excretes acetate as sole organic acid, while the latter exhibited a more flexible fermentation, producing additionally lactate and succinate. The observed hydrogen production could be assigned to a group 4 hydrogenase similar to Hydrogenase 4 (Hyf) in E. coli. We propose that Sulfurospirillum spp. produce molecular hydrogen with electrons derived from pyruvate oxidation by pyruvate:ferredoxin oxidoreductase and reduced ferredoxin. This hypothesis is supported by comparative proteome data, in which both PFOR and ferredoxin as well as hydrogenase 4 are up-regulated. A co-culture experiment with S. multivorans and Methanococcus voltae cultivated with lactate as sole substrate shows a syntrophic interaction between both organisms, since the former cannot grow fermentatively on lactate alone and the latter relies on hydrogen as electron donor. This opens up new perspectives on microbial communities, since Epsilonproteobacteria could play a yet unrecognized role as hydrogen producers in anoxic microbial communities.

microbiology

Hematology, biochemistry, and toxicology of wild hawksbill turtles (Eretmochelys imbricata) nesting in mangrove estuaries in the eastern Pacific Ocean

Sea turtles are a keystone species and are highly sensitive to changes in their environment, making them excellent environmental indicators. In light of environmental and climate changes, species are increasingly threatened by pollution, changes in ocean health, habitat alteration, and plastic ingestion. There may be additional health related threats and understanding these threats is key in directing future management and conservation efforts, particularly for severely reduced sea turtle populations. Hawksbill turtles (Eretmochelys imbricata) are critically endangered, with those in the eastern Pacific Ocean (Mexico-Peru) considered one of the most threatened sea turtle populations in the world. This study establishes baseline health parameters in hematology and blood biochemistry as well as tested for heavy metals and persitent organic pollutants in eastern Pacific hawksbills at a primary nesting colony located in a mangrove estuary. Whereas hematology and biochemistry results are consistent with healthy populations of other species of sea turtles, we identified differences in packed cell volume, heterophils and lympohcyte counts, and glucose when comparing our data to other adult hawksbill analysis (1), (2), (3). Our analysis of heavy metal contamination revealed a mean blood level of 0.245 ppm of arsenic, 0.045 ppm of lead, and 0.008 ppm of mercury. Blood levels of persistent organic pollutants were below the laboratory detection limit for all turtles. Our results suggest that differences in the feeding ecology of eastern Pacific hawksbills in mangrove estuaries may make them less likely to accumulate persistent organic pollutants and heavy metals in their blood. These baseline data on blood values in hawksbills nesting within a mangrove estuary in the eastern Pacific offer important guidance for health assessments of the species in the wild and in clinical rehabilitation facilities, and underscore the importance of preventing contamination from point and non-point sources in mangrove estuaries, which represent primary habitat to hawksbills and myriad other marine species in the eastern Pacific Ocean.

zoology

The null additivity of multi-drug combinations

From natural ecology 1-4 to clinical therapy 5-8, cells are often exposed to mixtures of multiple drugs. Two competing null models are used to predict the combined effect of drugs: response additivity (Bliss) and dosage additivity (Loewe) 9-11. Here, noting that these models diverge with increased number of drugs, we contrast their predictions with measurements of Escherichia coli growth under combinations of up to 10 different antibiotics. As the number of drugs increases, Bliss maintains accuracy while Loewe systematically loses its predictive power. The total dosage required for growth inhibition, which Loewe predicts should be fixed, steadily increases with the number of drugs, following a square root scaling. This scaling is explained by an approximation to Bliss where, inspired by RA Fishers classical geometric model 12, dosages of independent drugs adds up as orthogonal vectors rather than linearly. This dose-orthogonality approximation provides results similar to Bliss, yet uses the dosage language as Loewe and is hence easier to implement and intuit. The rejection of dosage additivity in favor of effect additivity and dosage orthogonality provides a framework for understanding how multiple drugs and stressors add up in nature and the clinic.

systems biology

Sex-determination and sex chromosomes are shared across the radiation of dioecious Nepenthes pitcher plants

Plants with separate sexes (dioecy) represent a minority but dioecy has evolved multiple times independently in plants. Our understanding of sex determination systems in plants and of the ecological factors and molecular changes associated with the evolution of dioecy remain limited. Here, we study the sex-determination system in dioecious plants that lack heteromorphic sex chromosomes and are not amenable to controlled breeding: Nepenthes pitcher plants. We genotyped wild populations of flowering males and females of three Nepenthes taxa using ddRAD-seq, and sequenced a male inflorescence transcriptome. We developed a novel statistical tool (privacy rarefaction) to distinguish true sex-specificity from stochastic noise in high-throughput sequencing data. Our results support XY-systems in all three Nepenthes taxa and in Silene latifolia which was used as a positive control for its known XY-system. The male-specific region of the Y chromosome showed little conservation among the three Nepenthes taxa, except for the essential pollen development gene DYT1 which was also male-specific in additional taxa. Hence, this homomorphic XY sex-determination system likely has a unique origin older than the crown of the genus Nepenthes at c. 17.7 My. In addition to the characterisation of the previously unknown sex chromosomes of Nepenthes, our work contributes an innovative, highly sensitive statistical method to efficiently detect sex-specific genomic regions in wild populations in general.

evolutionary biology

Decoding the gene co-expression network underlying the ability of Gevuina avellana Mol. to live in diverse light conditions

O_LIGevuina avellana Mol. (Proteaceae) is a typical tree from the South American temperate rainforest. Although this species mostly regenerates in shaded understories, it exhibits an exceptional ecological breadth, being able to live under a wide range of light conditions. Here we studied the genetic basis regulating physiological acclimation of the photosynthetic responses of G. avellana under contrasting light conditions.\nC_LIO_LIWe analyzed carbon assimilation and light energy used for photochemical process in plants acclimated to contrasting light conditions. Also, we used a transcriptional profile of leaf primordia from G. avellana saplings growing under different light environments to identify the gene co-expression network underpinning photosynthetic performance and light-related processes.\nC_LIO_LIThe photosynthetic parameters revealed optimal performance regardless of light conditions. Strikingly, the mechanism involved in dissipation of excess light energy showed no significant differences between high and low-light acclimated plants. The gene co-expression network defined a community structure consistent with the photochemical responses, including genes involved mainly in assembly and functioning of photosystems, photoprotection, and retrograde signaling.\nC_LIO_LIOur ecophysiological genomics approach provides an understanding of the molecular regulatory mechanisms that allows this tree to have an optimal balance between photochemical, photoprotective and antioxidant performance in the diverse light habitats it encounters in nature.\nC_LI

plant biology

Proposal for practical multi-kingdom classification of eukaryotes based on monophyly and comparable divergence time criteria

Much of the ecological, taxonomic and biodiversity research relies on understanding of phylogenetic relationships among organisms. There are multiple available classification systems that all suffer from differences in naming, incompleteness, presence of multiple non-monophyletic entities and poor correspondence of divergence times. These issues render taxonomic comparisons across the main groups of eukaryotes and all life in general difficult at best. By using the monophyly criterion, roughly comparable time of divergence and information from multiple phylogenetic reconstructions, I propose an alternative classification system for the domain Eukarya to improve hierarchical taxonomical comparability for animals, plants, fungi and multiple protist groups. Following this rationale, I propose 32 kingdoms of eukaryotes that are treated in 10 subdomains. These kingdoms are further separated into 43, 115, 140 and 353 taxa at the level of subkingdom, phylum, subphylum and class, respectively (http://dx.doi.org/10.15156/BIO/587483). Most of the names have been used previously or these were deduced from those of the type taxa to be able to unambiguously link genera to higher taxonomic levels. In the era of phylogenomics, understanding about the phylogenetic relationships among organisms is rapidly increasing. Classifications systems must keep pace with this race to serve the research community by consistent improvements in precision in terms of taxonomic resolution and maintaining monophyly of the ingredient taxa.

evolutionary biology

Genome-wide association across Saccharomyces cerevisiae strains reveals substantial variation in underlying gene requirements for toxin tolerance.

Cellulosic plant biomass is a promising sustainable resource for generating alternative biofuels and biochemicals with microbial factories. But a remaining bottleneck is engineering microbes that are tolerant of toxins generated during biomass processing, because mechanisms of toxin defense are only beginning to emerge. Here, we exploited natural diversity in 165 Saccharomyces cerevisiae strains isolated from diverse geographical and ecological niches, to identify mechanisms of hydrolysate-toxin tolerance. We performed genome-wide association (GWA) analysis to identify genetic variants underlying toxin tolerance, and gene knockouts and allele-swap experiments to validate the involvement of implicated genes. In the process of this work, we uncovered a surprising difference in genetic architecture depending on strain background: in all but one case, knockout of implicated genes had a significant effect on toxin tolerance in one strain, but no significant effect in another strain. In fact, whether or not the gene was involved in tolerance in each strain background had a bigger contribution to strain-specific variation than allelic differences. Our results suggest a major difference in the underlying network of causal genes in different strains, suggesting that mechanisms of hydrolysate tolerance are very dependent on the genetic background. These results could have significant implications for interpreting GWA results and raise important considerations for engineering strategies for industrial strain improvement.\n\nAuthor summaryUnderstanding the genetic architecture of complex traits is important for elucidating the genotype-phenotype relationship. Many studies have sought genetic variants that underlie phenotypic variation across individuals, both to implicate causal variants and to inform on architecture. Here we used genome-wide association analysis to identify genes and processes involved in tolerance of toxins found in plant-biomass hydrolysate, an important substrate for sustainable biofuel production. We found substantial variation in whether or not individual genes were important for tolerance across genetic backgrounds. Whether or not a gene was important in a given strain background explained more variation than the alleleic differences in the gene. These results suggest substantial variation in gene contributions, and perhaps underlying mechanisms, of toxin tolerance.

genomics

High-magnitude innovators as keystone individuals in the evolution of culture

Borrowing from the concept of keystone species in ecological food webs, a recent focus in the field of animal behaviour has been keystone individuals: individuals whose impact on population dynamics is disproportionally larger than their frequency in the population. In populations evolving culture, such may be the role of high-magnitude innovators: individuals whose innovations are a major departure from the populations existing behavioural repertoire. Their effect on cultural evolution is twofold: they produce innovations that constitute a cultural leap, and, once copied, their innovations may induce further innovations by conspecifics (socially induced innovations), as they explore the new behaviour themselves. I use computer simulations to study the co-evolution of independent innovations, socially induced innovations, and innovation magnitude, and show that while socially induced innovation is assumed here to be less costly than independent innovation, it does not readily evolve. When it evolves, it may in some conditions select against independent innovation and lower its frequency, despite it requiring independent innovation in order to operate; at the same time, however, it leads to much faster cultural evolution. These results confirm the role of high-magnitude innovators as keystones, and suggest a novel explanation for low frequency of independent innovation.

animal behavior and cognition

The genome of the water strider Gerris buenoi reveals expansions of gene repertoires associated with adaptations to life on the water

The semi-aquatic bugs conquered water surfaces worldwide and occupy ponds, streams, lakes, mangroves, and even open oceans. As such, they inspired a range of scientific studies from ecology and evolution to developmental genetics and hydrodynamics of fluid locomotion. However, the lack of a representative water strider genome hinders thorough investigations of the mechanisms underlying the processes of adaptation and diversification in this group. Here we report the sequencing and manual annotation of the Gerris buenoi (G. buenoi) genome, the first water strider genome to be sequenced so far. G. buenoi genome is about 1 000Mb and the sequencing effort recovered 20 949 predicted protein-coding genes. Manual annotation uncovered a number of local (tandem and proximal) gene duplications and expansions of gene families known for their importance in a variety of processes associated with morphological and physiological adaptations to water surface lifestyle. These expansions affect key processes such as growth, vision, desiccation resistance, detoxification, olfaction and epigenetic components. Strikingly, the G. buenoi genome contains three Insulin Receptors, a unique case among metazoans, suggesting key changes in the rewiring and function of the insulin pathway. Other genomic changes include wavelength sensitivity shifts in opsin proteins likely in association with the requirements of vision in water habitats. Our findings suggest that local gene duplications might have had an important role during the evolution of water striders. These findings along with the G. buenoi genome open exciting research opportunities to understand adaptation and genome evolution of this unique hemimetabolous insect.

genomics