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The spread of resistance to imidacloprid is restricted by thermotolerance in natural populations of Drosophila melanogaster

Imidacloprid, the worlds most utilised insecticide1, has raised considerable controversy due to its harmful effects on non-pest species2-6 and there is increasing evidence showing that insecticides have become the primary selective force in many insect species7-14. The genetic response to insecticides is heterogeneous across population and environment15-17, leading to more complex patterns of genetic variation than previously thought. This motivated the investigation of imidacloprid resistance at different temperatures in natural populations of Drosophila melanogaster originating from four climate extremes replicated across two continents. Population and quantitative genomic analysis, supported by functional tests, demonstrated a polygenic basis to resistance and a major trade-off with thermotolerance. Reduced genetic differentiation at resistance-associated loci indicate enhanced gene flow at these loci. Resistance alleles showed stronger evidence of positive selection in temperate populations compared to tropical populations. Polygenic architecture and ecological factors should be considered when developing sustainable management strategies for both pest and beneficial insects.

evolutionary biology

Social touch observation in adults with autism: intact neural representations of affective meaning but lack of embodied resonance

Humans can easily grasp the affective meaning of touch when observing social interactions. Several neural systems support this ability, including theory of mind (ToM) and somatosensory resonance systems, but it is unclear how these systems are affected in autism spectrum disorder (ASD). Individuals with ASD are characterized by impairments in social interaction and the use of (non)verbal communication such as social and reciprocal touch. The present study applies an ecologically valid stimulus set and multivoxel pattern fMRI neuroimaging to pinpoint atypicalities in the neural circuitry underlying socio-affective touch observation in adults with ASD as compared to matched neurotypical controls. The MVPA results reveal that the affective meaning of touch is well represented in the temporoparietal junction, a core ToM mentalizing area, in both groups. Conversely, only the neurotypical group hosts affective touch representations in the somatosensory cortex, not the ASD group, yielding a significant group difference. Lastly, individuals with a more positive attitude towards receiving, witnessing, and providing social touch and with a higher score on social responsivity, show more differentiated representations of the affective meaning of touch in these somatosensory areas. Together, our findings imply that individuals with ASD are able to cognitively represent the affective meaning of touch, but they lack the spontaneous embodied somatosensory resonance when observing social touch communications. Individual differences in this diminished resonance appear to be related to social touch avoidance and quantitative autism traits.\n\nSignificance StatementAutism is characterized by socio-communicative impairments, including abnormal processing of interpersonal touch. Little is known about the neural basis of atypicalities in social touch processing in autism. Here, adults with and without autism watched video clips displaying social touch interactions and judged the affective valence of the touch. Subsequently, they underwent functional magnetic resonance imaging while watching the same videos. Brain activity patterns demonstrate that adults with autism show intact cognitive understanding (i.e. \"knowing\") of observed socio-affective touch experiences but lack of embodied emotional resonance (i.e. \"feeling\"). This lack of emotional resonance is linked to social touch avoidance and quantitative autism traits. These findings highlight that the depth of experiencing the state of others is shallower in people with autism.

neuroscience

Multilocus sequence analysis, a rapid and accurate identification tool for taxonomic classification, evolutionary relationship and population biology of the genus Shewanella.

The genus Shewanella comprises a group of marine-dwelling species with worldwide distribution. Several species are regarded as causative agents of food spoilage and opportunistic pathogens of human diseases. In this study, a standard multilocus sequence analysis (MLSA) based on six protein-coding genes (gyrA, gyrB, infB, recN, rpoA and topA) was established as a rapid and accurate identification tool in fifty-nine type Shewanella strains. This method yielded sufficient resolving power in regard to enough informative sites, adequate sequence divergences and distinct interspecies branches. The stability of phylogenetic topology was supported by high bootstrap values and concordance with different methods. The reliability of the MLSA scheme was further validated by identical phylogenies and high correlations of genomes. The MLSA approach provided a robust system to exhibit evolutionary relationships in the Shewanella genus. The split network tree proposed twelve distinct monophyletic clades with identical G+C contents and high genetic similarities. Eighty-six tested strains were investigated to explore the population biology of the Shewanella genus in China. The most prevalent Shewanella species were Shewanella algae, Shewanella xiamenensis, Shewanella chilikensis, Shewanella indica, Shewanella seohaensis and Shewanella carassii. The strains frequently isolated from clinical and food samples highlighted the importance of increasing the surveillance of Shewanella species. Combined with the genetic, genomic and phenotypic analyses, Shewanella upenei should be considered a synonym of S. algae, and Shewanella pacifica should be reclassified as a synonym of Shewanella japonica.\n\nIMPORTANCEThe MLSA scheme based on six HKGs (gyrA, gyrB, infB, recN, rpoA and topA) is well established as a reliable tool for taxonomic, evolutionary and epidemiological analyses of the genus Shewanella in this study. The standard MLSA method allows researchers to make rapid, economical and precise identification of Shewanella strains. The robust phylogenetic network of MLSA provides profound insight into the evolutionary structure of the genus Shewanella. The population genetics of Shewanella species determined by the MLSA approach plays a pivotal role in clinical diagnosis and routine monitoring. Further studies on remaining species and genomic analysis will enhance a more comprehensive understanding of the microbial systematics, phylogenetic relationships and ecological status of the genus Shewanella.

microbiology

Berry and pip form covariation in wild and domesticated grapevines: eco-evo-devo implications and archaeobotanical perspectives

The phenotypic changes that occurred during the domestication and diversification of grapevine are well known, particularly changes in seed morphology, but the functional causes and consequences behind these variations are poorly understood. Wild and domesticate grapes differ, among others, in the form of their pips: wild grapes produce roundish pips with short stalks and cultivated varieties have more elongated pips with longer stalks. Such variations of form are of first importance for archaeobotany since the pip form is, most often, the only remaining information in archaeological settings. This study aims to enlight archaeobotanical record and grapevine pip development by better understanding how size and shape (co)variates between pip and berry in both wild and domesticated Vitis vinifera. The covariation of berry size, number of seeds per berry ("piposity"), pip size and pip shape were explored on 49 grapevine accessions sampled among Euro-Mediterranean traditional cultivars and wild grapevines. We show that for wild grapevine, the higher the piposity, the bigger the berry and the more elongated the pip. For both wild and domesticated grapevine, the longer is the pip, the more it has a "domesticated" shape. Consequences for archaeobotanical studies are tested and discussed, and these covariations allowed the inference of berry dimensions from archaeological pips from a Southern France Roman site. This systematic exploration sheds light on new aspects of pip-berry relationship, in both size and shape, on grapevine eco-evo-devo changes during domestication, and invites to explore further the functional ecology of grapevine pip and berry and notably the impact of cultivation practices and human selection on grapevine morphology.

plant biology

Indolergic receptors of the elephant mosquito Toxorhynchites amboinensis

The conservation of the mosquito indolergic receptors across the Culicinae and Anophelinae mosquito lineages, which spans 200 million years of evolution, is a testament to the central role of indolic compounds in the biology of these insects. Indole and skatole have been associated with the detection of oviposition sites and animal hosts. To evaluate the potential ecological role of these two compounds, we have used a pharmacological approach to characterize homologs of the indolergic receptors Or2 and Or10 in the non-hematophagous elephant mosquito Toxorhynchites amboinensis. We provide evidence that both receptors are narrowly tuned to indole and skatole like their counterparts from hematophagous mosquitoes. These findings indicate that indole and skatole are operating in a non-animal-host seeking context in Toxorhynchites and underscore the importance of understanding their roles in hematophagous mosquitoes.

evolutionary biology

The Proteome of Tetrasphaera elongata is Prepadapted to Changing Environmental Conditions in Wastewater Treatment Plants

The activated sludge in wastewater treatment plants (WWTP) designed for enhanced biological phosphorus removal (EBPR) experiences periodically changing nutrient and oxygen availability. Tetrasphaera is the most abundant genus in Danish WWTP and represent up to 20-30% of the activated sludge community based on 16S rRNA amplicon sequencing and quantitative fluorescence in situ hybridization analyses, although it is in low abundance in the influent wastewater. Here we investigate how Tetrasphaera can successfully out-compete most other microorganisms in such highly dynamic ecosystems. To achive this, we analyze the physiological adaptations of the WWTP isolate T. elongata str. LP2 during an aerobic to anoxic shift by label-free quantitative proteomics and NMR-metabolomics. Escherichia coli was used as reference organism as it shares several metabolic capabilities and is regularly introduced to wastewater treatment plants, but without succeeding there. When compared to E. coli, only minor changes in the proteome of T. elongata were observed after the switch to anoxic conditions. This indicates that metabolic pathways for anaerobic energy harvest were already expressed during the aerobic growth. This allows continuous growth of Tetrasphaera immediately after the switch to anoxic conditions. Metabolomics furthermore revealed that the substrates provided were exploited far more efficiently by Tetrasphaera than by E. coli. These results suggest that T. elongata prosper in the dynamic WWTP environment due to adaptation to the changing environmental conditions. Significance of the studyMembers of the genus Tetrasphaera are widely distributed and highly abundant in most well-operating WWTPs with EBPR configuration. However, despite their high abundance in situ, little is known about their physiology and ecological role. Although the importance of Tetrasphaera in engineered wastewater treatment systems is slowly being recognized, additional information is needed to understand the full extent of functions the microorganisms have in many of the essential biological processes in the WWTP. Such information may improve available process models and ultimately lead to better wastewater treatment as well as resource recovery. This study supplies proteomic and metabolomic data on the aerobic/anoxic adaptation of Tetrasphaera and provides a hypothesis on how Tetrasphaera might compete in dynamic engineered systems.

microbiology

Coupled fast and slow feedbacks lead to continual evolution: A general modeling approach

The Red Queen Hypothesis, which suggests that continual evolution can result from solely biotic interactions, has been studied in macroevolutionary and microevolutionary contexts. While microevolutionary studies have described examples in which evolution does not cease, understanding which general conditions lead to continual evolution or to stasis remains a major challenge. In many cases, it is unclear which experimental features or model assumptions are necessary for the observed continual evolution to emerge, and whether the described behavior is robust to variations in the given setup. Here, we aim to find the minimal set of conditions under which continual evolution occurs. To this end, we present a theoretical framework that does not assume any specific functional form and, therefore, can be applied to a wide variety of systems. Our framework is also general enough to cast predictions about both monomorphic and polymorphic populations. We show that the combination of a fast positive and a slow negative feedback causes continual evolution to emerge even from the evolution of one single evolving trait, provided that the ecological timescale is sufficiently separated from the timescales of mutation and the negative feedback. Our approach and results thus contribute to a deeper understanding of the evolutionary dynamics resulting from biotic interactions.

evolutionary biology

EvolvingSTEM: A microbial evolution-in-action curriculum that enhances learning of evolutionary biology and increases interest in STEM

Evolution is a central, unifying theory for all of life science, yet the subject is poorly represented in most secondary-school biology courses, especially in the United States. One challenge to learning evolution is that it is taught as a conceptual, retrospective subject with few tangible outcomes for students. These typical passive learning strategies lead to student disengagement with the material and misunderstanding of evolutionary concepts. To promote greater investment and comprehension, we developed EvolvingSTEM, an inquiry-based laboratory curriculum that demonstrates concepts of natural selection, heredity, and ecological diversity through experimental evolution of a benign bacterium. Students transfer populations of Pseudomonas fluorescens growing on plastic beads, which selects for biofilm formation and mutants with new, conspicuous phenotypes. We introduced our curriculum to four introductory high school biology classes alongside their standard curriculum materials and found that students who learned evolution through EvolvingSTEM scored significantly better on a common assessment targeted to Next Generation Science Standards than students taught only the standard curriculum. This latter group subsequently achieved similar scores once they too completed our curriculum. Our work demonstrates that inquiry-based, hands-on experiences with evolving bacterial populations can greatly enhance student learning of evolutionary concepts.

evolutionary biology

From Habitat Use to Social Behavior: Natural History of a Voiceless Poison Frog, Dendrobates tinctorius

Descriptive studies of natural history have always been a source of knowledge on which experimental work and scientific progress rely. Poison frogs are a well-studied group of small Neotropical frogs with diverse parental behaviors, distinct calls, and bright colors that warn predators about their toxicity; and a showcase of advances in fundamental biology through natural history observations. The dyeing poison frog, Dendrobates tinctorius, is emblematic of the Guianas region, widespread in the pet-trade, and increasingly popular in research. This species shows several unusual behaviors, such as the lack of advertisement calls and the aggregation around tree-fall gaps, which remain poorly described and understood. Here, we summarize our observations from a natural population of D. tinctorius in French Guiana collected over various field trips between 2009 and 2017; our aim is to provide groundwork for future fundamental and applied research spanning parental care, animal dispersal, disease spread, habitat use in relation to color patterns, and intra specific communication, to name a few. We report sex differences in habitat use and the striking invasion of tree-fall gaps; describe their courtship and aggressive behaviors; document egg development and tadpole transport; and discuss how the knowledge generated by this study could set the grounds for further research on the behavior, ecology, and conservation of this species.

animal behavior and cognition

Character displacement within the breeding area questions reinforcement in Ficedula flycatchers

At present, studies of reinforcement should be focused on demonstrating how often this process occurs in nature and how important it is for speciation. Here we study the character displacement within the breeding area in the Pied Flycatcher to check the validity of the reinforcement in Ficedula flycatchers. We used point-referenced spatial data and a random forest to find the most important explanatory factors of the character displacement, and to reconstruct the phenotypic structure of the populations. The environmental temperature, and not the distance to sympatry, were proven to better describe the geographic pattern of the mean breeding plumage colour of the Pied Flycatcher populations. We conclude that ecologically distinct adaptations drive the morphological differentiation of the Old World flycatchers, and not reinforcement.

evolutionary biology

Candidate regulators and target genes of drought stress in needles and roots of Norway spruce

Drought stress impacts on seedling establishment, survival and whole-plant productivity. Drought stress responses have been extensively studied at the physiological and molecular level in angiosperms, particularly in agricultural species and the model Arabidopsis thaliana, with the vast majority of work performed on aboveground tissues. Boreal forests are dominated by coniferous tree species and cover vast areas of the terrestrial surface. These areas are predicted to be particularly influenced by ongoing climate change and will be exposed to more frequent and acute drought. The associated impact at all stages of the forest tree life cycle is expected to have large-scale ecological and economic impacts. To provide a comprehensive understanding of the drought response mechanisms of Picea abies seedlings, we assayed the physiological response of needles and transcriptional responses of roots and needles after exposure to mild and severe drought. Shoots and needles showed extensive reversible plasticity for physiological measures indicative of drought response mechanisms, including stomatal conductance (gs) and shoot water potential. Root and needle transcriptional responses contrasted, with an extensive root-specific down-regulation of growth. When we compared the responses of P. abies with previously-characterised A. thaliana drought response genes, we found that the majority of the genes were conserved across lineages. However, in P. abies, transcription factors (TFs) previously identified as belonging to the ABA-dependent pathway had a more limited role and most differentially expressed genes were specific to the stress response of P. abies. These results highlight the importance of profiling both above- and below-ground tissues and provide a comprehensive framework to advance understanding of the drought response mechanism of P. abies.\n\nOne sentence summaryAnalysis of the drought transcriptome of Norway spruce reveals divergent molecular response pathways in conifers.

plant biology

Inferring lifestyle for Aves and Theropoda: a model based on curvatures of extant avian ungual bones

Claws are involved in a number of behaviours including locomotion and prey capture, and as a result animals evolve claw morphologies that enable these functions. Past authors have found geometry of the keratinous sheath of the claw to correlate with mode of life for extant birds and squamates; this relationship has frequently been cited to infer lifestyles for Mesozoic theropods including Archaeopteryx. However, claw sheaths rarely fossilise and are prone to deformation; past inferences are thus compromised. As the ungual phalanx within the claw is relatively resistant to deformation and more commonly preserved in the fossil record, geometry of this bone would provide a more useful metric for paleontological analysis. In this study, ungual bones of 108 birds and 5 squamates were imaged using X-ray techniques and a relationship was found between curvatures of the ungual bone within the claw of pedal digit III and four modes of life; ground-dwelling, perching, predatory, and scansorial; using linear discriminant analysis with Kappa equal to 0.69. Our model predicts arboreal lifestyles for certain key taxa Archaeopteryx and Microraptor and a predatory ecology for Confuciusornis. These findings demonstrate the utility of our model in answering questions of palaeoecology, the theropod-bird transition, and the evolution of avian flight.View Full Text

paleontology

Capturing the Diversity of Subsurface Microbiota - Choice of Carbon Source for Microcosm Enrichment and Isolation of Groundwater Bacteria

Improved and innovative enrichment/isolation techniques that yield to relevant isolates representing the true diversity of environmental microbial communities would significantly advance exploring the physiology of ecologically important taxa in ecosystems. Traditionally, either simple organic carbon (C) or yeast extract is used as C source in culture medium for microbial enrichment/isolation in laboratory. In natural environment, however, microbial population and evolution are greatly influenced by the property and composition of natural organic C. In this study, 8 types of organic C sources were fed to intrinsic groundwater microbes collected at Oak Ridge Reservation Field Research Center (ORR-FRC) background site for a 30-day incubation period to investigate the response of indigenous bacterial communities to different C sources. The tested C sources included simple organic C (glucose, acetate, benzoate, oleic acid, and cellulose) that are either traditionally used as C source in bacterial culture medium or present in natural environments; naturally occurring undefined complex C (bacterial cell lysate and sediment-derived natural organic matter (NOM)); as well as vitamin mixture which is a commonly used ingredient in culture medium. Our results clearly indicate that natural complex C substrates served better in enriching diverse bacteria compared to other C sources. Microcosms amended with small organic C (glucose, acetate, benzoate, or oleic acid) showed significantly lower biodiversity than control groups, dominated by only a few phyla of bacteria such as Proteobacteria and Bacteroidetes which are commonly isolated and already have diverse representative isolates, while those amended with natural complex C (cell lysate or NOM) displayed significantly higher biodiversity than control groups, in which three phyla (Verrucomicrobia, Planctomycetes, and Armatimonadetes) that are poorly represented in published culture collections were abundantly enriched. Further isolation of pure bacterial strains from complex C-amended enrichments led to 51 species representing 4 phyla, 13 orders. Furthermore, 5 isolates with low similarities to published strains were considered to be novel. Results from this study will aid in the design of better cultivation and isolation strategy for maximize the diversity of organisms recovered from subsurface environment.

microbiology

Recent origin of an XX/XY sex-determination system in the ancient plant lineage Ginkgo biloba

Sexual dimorphism like dioecy (separate male and female individuals) have evolved in diverse multicellular eukaryotes while the molecular mechanisms underlying the development of such a key biological trait remains elusive (1). The living fossil Ginkgo biloba represents an early diverged lineage of land plants with dioecy. However, its sex-determination system and molecular basis have long been controversial or unknown. In the present research, we assembled the first and largest to date chromosome-level genome of a non-model tree species using Hi-C data. With this reference genome, we addressed both questions using genome resequencing data gathered from 97 male and 265 female trees of ginkgo, as well as transcriptome data from three developmental stages for both sexes. Our results support vertebrate-like XY chromosomes for ginkgo and five potential sex-determination genes, which may originate ~14 million years ago. This is the earliest diverged sex determination region in all reported plants as yet. The present research resolved a long-term controversy, lay a foundation for future studies on the origin and evolution of plant sexes, and provide genetic markers for sex identification of ginkgo which will be valuable for both nurseries and field ecology of ginkgo.

evolutionary biology

Genomic evidence of genetic variation with pleiotropic effects on caterpillar fitness and plant traits in a model legume

Plant-insect interactions are ubiquitous, and have been studied intensely because of their relevance to damage and pollination in agricultural plants, and to the ecology and evolution of biodiversity. Variation within species can affect the outcome of these interactions, such as whether an insect successfully develops on a plant species. Whereas specific genes and chemicals that mediate these interactions have been identified, studies of genome-or metabolome-wide intraspecific variation might be necessary to better explain patterns of host-plant use and adaptation often observed in the wild. Here, we present such a study. Specifically, we assess the consequences of genome-wide genetic variation in the model plant Medicago truncatula for Lycaeides melissa caterpillar growth and survival (i.e., larval performance). Using a rearing experiment and a whole-genome SNP data set (>5 million SNPs), we show that polygenic variation in M. truncatula explains 9-41% of the observed variation in caterpillar growth and survival. We detect genetic correlations among caterpillar performance and other plant traits, such as structural defenses and some anonymous chemical features; these genetic correlations demonstrate that multiple M. truncatula alleles have pleiotropic effects on plant traits and caterpillar growth or survival (or that there is substantial linkage disequilibrium among loci affecting these traits). We further show that a moderate proportion of the genetic effect of M. truncatula alleles on L. melissa performance can be explained by the effect of these alleles on the plant traits we measured, especially leaf toughness. Taken together, our results show that intraspecific genetic variation in M. truncatula has a substantial effect on the successful development of L. melissa caterpillars (i.e., on a plant-insect interaction), and further point toward traits mediating this genetic effect.

evolutionary biology

How to pour a cup of coffee

Pouring a drink feels deceptively trivial, yet it requires guiding a boundary-free fluid into a vessel without spilling, overflowing, or toppling it -- a task at which robots remain notoriously brittle. How humans achieve this so effortlessly is unknown, as motor control has predominantly been studied in brief, highly constrained laboratory tasks, leaving the control principles underlying ecological tasks largely unknown. Here we measured continuous sensorimotor control during liquid pouring across various containers, vessels, and speed demands. Despite substantial variation in movement trajectories and durations, individuals maintained a strikingly invariant preferred fill level. Counterintuitively, fill level variability decreased at higher fill levels, and precision was maintained even under time pressure. A stochastic optimal control model combining a data-driven nonlinear approximation of flow dynamics with a cost that balanced individualised fill level, energy expenditure and flow-rate reproduced the behaviour. Humans thus pour optimally, given their sensorimotor limits and idiosyncratic notion of "full".

neuroscience

Cross-Kingdom Control: Yeast Prion Protein Modulates Host Physiology in Drosophila

Prions, once mainly studied for their pathogenic roles, are now gaining recognition as adaptive elements in microbial physiology. Over one-third of wild yeast isolates harbor prion proteins, yet their impact on host-microbe interactions remains poorly characterized. Given the ecological dominance of yeasts in the Drosophila mycobiome, we leveraged the Drosophila melanogaster-Saccharomyces cerevisiae system to investigate how the mycobiome-derived prion, [MRPL10+], modulates host physiology. We show that flies exposed to [MRPL10+] yeast exhibit significantly enhanced cold tolerance and increased locomotor activity. This effect persists with heat-killed yeast and diluted culture, suggesting a stable, potent bioactive factor. Using the genetically diverse Drosophila Global Diversity Lines (GDL), we identified natural variation in responsiveness to [MRPL10+] yeast. Genome-wide association and functional RNAi screening revealed a gut-brain signaling axis involving genes critical for digestion, intercellular communication, transcription regulation, and neural transmission. Notably, serotonin and octopamine pathways were essential for [MRPL10+]-induced changes in cold tolerance and locomotion, implicating neuromodulatory circuits in prion-mediated microbial signaling. Our findings establish a mechanistic link between a fungal prion and host metabolic and neural adaptation. This work provides the first genetic dissection of a prion-mediated host-microbe interaction, laying the groundwork for investigating beneficial prions in complex microbial communities and highlighting a new dimension of the mycobiomes influence on animal physiology.

evolutionary biology

Stronger brain responses to acute stress reflect greater everyday stress variability

Laboratory stress tasks are widely used to assess individual differences in acute stress reactivity, yet it remains unclear how these responses correspond to stress experienced in everyday life. Here, we combined the Montreal imaging stress task (MIST) with ecological momentary assessment (EMA) over three months to assess acute and everyday stress in 67 healthy women. Greater within-person variability in everyday stress, but not average stress levels, were associated with stronger overall stress-related brain responses (b = 0.73, p = .039), with a whole-brain association particularly evident in the bilateral caudate (rROI = .32, pcluster.FWE < .001). Greater everyday stress variability was also associated with stronger stress-related functional connectivity between the ventromedial prefrontal cortex (vmPFC) and parietal and posterior medial regions (pcluster.FWE < .001). We conclude that acute neural stress responses relate more closely to fluctuations in perceived stress than to how stressed an individual feels on average. This suggests that laboratory stress tasks capture acute stress responsivity that is distinct from average stress exposure, highlighting the importance of considering what these tasks measure when interpreting individual differences in acute stress responses.

neuroscience