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How Cognitive and Reactive Fear Circuits Optimize Escape Decisions in Humans

Flight initiation distance (FID), the distance at which an organism flees from an approaching threat, is an ecological metric of cost-benefit functions of escape decisions. We adapted the FID paradigm to investigate how fast or slow attacking virtual predators constrain escape decisions. We show that rapid escape decisions rely on reactive fear circuits in the periaqueductal gray and midcingulate cortex (MCC), while protracted escape decisions, defined by larger buffer zones, were associated with cognitive fear circuits which include posterior cingulate cortex, hippocampus and the ventromedial prefrontal cortex, circuits implicated in strategic avoidance and behavioral flexibility. Using a Bayesian Decision Model, we further show that optimization of escape decisions under rapid flight were localized to the MCC, a region involved in adaptive motor control, while the hippocampus is implicated in optimizing decisions that update and control slower escape initiation. These results demonstrate an unexplored link between defensive survival circuits and their role in adaptive escape decisions.\n\nSignificanceHumans, like other animals, have evolved a set of circuits whose primary function is survival. In the case of predation, these circuits include reactive fear circuits involved in fast and immediate escape decisions and cognitive fear circuits that are involved in the conscious feeling of threat as well as slow strategic escape. Using neuroimaging combined with computational modeling, we support this differentiation of fear circuits by showing that fast escape decisions are elicited by the periaqueductal gray and MCC, regions involved in reactive flight. Conversely, slower escape decisions rely on the hippocampus, posterior cingulate cortex and prefrontal cortex, a circuit implicated in behavioral flexibility. These results support the role of the defensive survival circuitry in escape decisions and a separation of fear into reactive and cognitive circuits.

neuroscience

Retinal specializations to a micro-predatory and crypto-benthic life-style in the Mediterranean triplefin blenny Tripterygion delaisi

The environment and lifestyle of a species are known to exert selective pressure on the visual system, often demonstrating a tight link between visual morphology and ecology. Many studies have predicted the visual requirements of a species by examining the anatomical features of the eye. However, among the vast number of studies on visual specializations in aquatic animals, only a few have focused on small benthic fishes that occupy a heterogeneous and spatially complex visual environment. This study investigates the general retinal anatomy including the topography of both the photoreceptor and ganglion cell populations and estimates the spatial resolving power of the eye of the Mediterranean triplefin Tripterygion delaisi. Retinal wholemounts were prepared to systematically and quantitatively analyze photoreceptor and retinal ganglion cell densities using design-based stereology. To further examine the retinal structure, we also used magnetic resonance imaging and histological examination of retinal cross sections. Observations of the triplefin's eyes revealed them to be highly mobile, allowing them to view the surroundings without body movements. A rostral aphakic gap and the elliptical shape of the eye extend its visual field rostrally and allow for a rostro-caudal accommodatory axis, enabling this species to focus on prey at close range. Single and twin cones dominate the retina and are consistently arranged in one of two regular patterns, which may enhance motion detection and color vision. The retina features a prominent, dorso-temporal, convexiclivate fovea with an average density of 104,400 double and 30,800 single cones per mm2, and 81,000 retinal ganglion cells per mm2. Based on photoreceptor spacing, spatial resolving power was calculated to be between 6.7 and 9.0 cycles per degree. Location and resolving power of the fovea would benefit the detection and identification of small prey in the lower frontal region of the visual field.

animal behavior and cognition

Fish Diversity as a Function of Depth and Body Size

We analyze the number of marine fish species as a function of fish body size and occurrence depth. For this purpose, we analyze the FishBase database. We compare these data to predictions of fish species numbers derived from the neutral theory of biodiversity combined with well-established ecological scaling laws, and measured oceanic biomass data. We consider several variants of these scaling laws, and we find that more large fish species exist compared to the prediction, which is especially true for elasmobranchs, possibly due to their overwhelmingly predatory niches. We find species numbers decreasing with occurrence depth somewhat quicker than our predictions based on the decrease of the number of individuals with depth indicates. This is especially true for the elasmobranchs. This is unsurprising, since the individuals versus depth data did not specifically determine elasmobranch biomass, and since sharks are known to be limited to depths < 3,000 m.\n\nFinally, we discuss how a reduced rate of speciation in larger animals could explain why large species are rare, in spite of the advantages of large body sizes outlined in Copes rule.

evolutionary biology

Image-based methods for phenotyping growth dynamics and fitness in large plant populations

BackgroundThe model species Arabidopsis thaliana has extensive resources to investigate intraspecific trait variability and the genetic bases of ecologically relevant traits. However, the cost of equipment and software required for high-throughput phenotyping is often a bottleneck for large-scale studies, such as mutant screening or quantitative genetics analyses. Simple tools are needed for the measurement of fitness-related traits, like relative growth rate and fruit production, without investment in expensive infrastructures. Here, we describe methods that enable the estimation of biomass accumulation and fruit number from the analysis of rosette and inflorescence images taken with a regular camera.\n\nResultsWe developed two models to predict plant dry mass and fruit number from the parameters extracted with the analysis of rosette and inflorescence images. Predictive models were trained by sacrificing growing individuals for dry mass estimation, and manually measuring a fraction of individuals for fruit number at maturity. Using a cross-validation approach, we showed that quantitative parameters extracted from image analysis predicts more 90% of both plant dry mass and fruit number. When used on 451 natural accessions, the method allowed modelling growth dynamics, including relative growth rate, throughout the life cycle of various ecotypes. Estimated growth-related traits had high heritability (0.65 < H2 < 0.93), as well as estimated fruit number (H2 = 0.68). In addition, we validated the method for estimating fruit number with rev5, a mutant with increased flower abortion.\n\nConclusionsThe method we propose here is based on the automated computerization of plant images with ImageJ, and subsequent statistical modelling in R. It allows plant biologists to measure growth dynamics and fruit number in hundreds of individuals with simple computing steps that can be repeated and adjusted to a wide range of laboratory conditions. It is thus a flexible toolkit for the measurement of fitness-related traits in large plant populations.

bioinformatics

The Cultural Brain Hypothesis: How culture drives brain expansion, underlies sociality, and alters life history

In the last few million years, the hominin brain more than tripled in size. Comparisons across evolutionary lineages suggest that this expansion may be part of a broader trend toward larger, more complex brains in many taxa. Efforts to understand the evolutionary forces driving brain expansion have focused on climatic, ecological, and social factors. Here, building on existing research on learning, we analytically and computationally model the predictions of two closely related hypotheses: The Cultural Brain Hypothesis and the Cumulative Cultural Brain Hypothesis. The Cultural Brain Hypothesis posits that brains have been selected for their ability to store and manage information, acquired through asocial or social learning. The model of the Cultural Brain Hypothesis reveals relationships between brain size, group size, innovation, social learning, mating structures, and the length of the juvenile period that are supported by the existing empirical literature. From this model, we derive a set of predictions--the Cumulative Cultural Brain Hypothesis--for the conditions that favor an autocatalytic take-off characteristic of human evolution. This narrow evolutionary pathway, created by cumulative cultural evolution, may help explain the rapid expansion of human brains and other aspects of our species life history and psychology.

evolutionary biology

Lineage specific histories of Mycobacterium tuberculosis dispersal in Africa and Eurasia

Mycobacterium tuberculosis (M.tb) is a globally distributed, obligate pathogen of humans that can be divided into seven clearly defined lineages. Identifying how the ancestral clone of M.tb spread and differentiated is important for identifying the ecological drivers of the current pandemic. We reconstructed M.tb migration in Africa and Eurasia, and investigated lineage specific patterns of spread. Applying evolutionary rates inferred with ancient M.tb genome calibration, we link M.tb dispersal to historical phenomena that altered patterns of connectivity throughout Africa and Eurasia: trans-Indian Ocean trade in spices and other goods, the Silk Road and its predecessors, the expansion of the Roman Empire and, the European Age of Exploration. We find that Eastern Africa and Southeast Asia have been critical in the dispersal of M.tb. Our results reveal complex relationships between spatial dispersal and expansion of M.tb populations, and delineate the independent evolutionary trajectories of bacterial sub-populations underlying the current pandemic.

evolutionary biology

Genomic characterisation and conservation genetics of the indigenous Irish Kerry cattle breed

Kerry cattle are an endangered landrace heritage breed of cultural importance to Ireland. In the present study we have used genome-wide SNP data (Illumina(R) BovineSNP50 array) to evaluate genomic diversity within the Kerry cattle population and between Kerry cattle and other European cattle breeds. Visualisation of patterns of genetic differentiation and gene flow among cattle breeds using phylogenetic trees with ancestry graphs highlighted, in particular, historical gene flow from the British Shorthorn breed into the ancestral population of modern Kerry cattle. Principal component analysis (PCA) and genetic clustering emphasised the genetic distinctiveness of Kerry cattle relative to comparator British and European cattle breeds. Modelling of genetic effective population size (Ne) revealed a demographic trend of diminishing Ne over time and that recent estimated Ne values for the Kerry breed may be less than the threshold for sustainable genetic conservation. In addition, analysis of genome-wide autozygosity (FROH) showed that genomic inbreeding has increased significantly during the 20 years between 1992 and 2012. Finally, signatures of selection revealed genomic regions subject to natural and artificial selection as Kerry cattle adapted to the climate, physical geography and agro-ecology of southwest Ireland.\n\nNote 1: This is an Associate Editor (D.E.M) Inaugural Article submission to Frontiers in Genetics: Livestock Genomics\n\nNote 2: British English language style preferred for publication of this article.

genomics

Pathogen Population Structure Can Explain Hospital Outbreaks

ObjectiveTo analyze Hospital Acquired Infection (HAI) outbreaks using microbial population biology dynamics in order to understand outbreaks as a biological system.\n\nDesignComputational modeling study.\n\nMethodsThe majority of HAI transmission models describe dynamics on the level of the host rather than on the level of the pathogens themselves. Accordingly, epidemiologists often cannot complete transmission chains without direct evidence of either host-host contact or large reservoir populations. Here, we propose an ecology-based model to explain the transmission of pathogens in hospitals. The model is based upon metapopulation biology, which describes a group of interacting localized populations and island biogeography, which provides a basis for how pathogens may be moving between locales. Computational simulation trials are used to assess the applicability of the model.\n\nResultsResults indicate that pathogens survive for extended periods without the need for large reservoirs by living in localized ephemeral populations while continuously transmitting pathogens to new seed populations. Computational simulations show small populations spending significant portions of time at sizes too small to be detected by most surveillance protocols. The number and type of these ephemeral populations enable the overall pathogen population to be sustained.\n\nConclusionsBy modeling hospital pathogens as a metapopulation, observations characteristic of hospital acquired infection outbreaks for which there has previously been no sufficient biological explanation, including how and why empirically successful interventions work, can now be accounted for using population dynamic hypotheses. Epidemiological links between temporally isolated outbreaks are explained via pathogen population dynamics and potential outbreak intervention targets are identified.

epidemiology

Rolling a mycobiome down a hill: endophytes in the Taiwanese Cloud Forest

Fungal endophytes of plants are ubiquitous and important to host plant health. Despite their ecological importance, landscape-level patterns of microbial communities in plant hosts are not well-characterized. Fungal wood-inhabiting and foliar endophyte communities from multiple tree hosts were sampled at multiple spatial scales across a 25 ha subtropical research plot in northern Taiwan, using culture-free, community DNA amplicon sequencing methods. Fungal endophyte communities were distinct between leaves and wood, but the mycobiomes were highly variable across and within tree species. Of the variance that could be explained, host tree species was the most important driver of mycobiome community-composition. Within a single tree species, \"core\" mycobiomes were characterized using cooccurrence analysis. These core groups of endophytes in leaves and wood show divergent spatial patterns. For wood endophytes, a more consistent, \"minimal\" core mycobiome coexisted with the host across the extent of the study. For leaf endophytes, the core fungi resembled a more dynamic, \"gradient\" model of the core microbiome, changing across the topography and distance of the study.

microbiology

An analytical framework to understand regulatory novelty accompanying allopolyploidization

Allopolyploidy is a prevalent process in plants, having important physiological, ecological, and evolutionary consequences. Massive, genome-wide transcriptomic rewiring in response to genomic merger and doubling has been demonstrated in many allopolyploid systems, encompassing a diversity of phenomena, including homoeolog expression bias, genome dominance, expression-level dominance, and revamping of co-expression networks. Here we present an analytical framework to reconcile these patterns of regulatory novelty as governed by distinct sets of intra- and inter-subgenome cis-trans relationships. This approach is a novel extension of classic allele-specific expression analysis to incorporate and distinguish the separate effects of parental regulatory interactions as well as further complications at the allopolyploid level. We demonstrated that the cis-trans framework devised not only offers new perspective on disentangling genetic from epigenetic and higher-order effects that impact gene expression, but also provides the conceptual basis and tools to unify recently presented models for both genome-wide expression dominance and biased fractionation in allopolyploids.

evolutionary biology

Equality between the sexes in plants for costs of reproduction; evidence from the dioecious Cape genus Leucadendron (Proteaceae)

It has been argued that sexual allocation is greater for female function than male function in plants in general and specifically for the large dioecious Cape genus Leucadendron. Here, we use new interpretations of published information to support the hypothesis of equality between sexes in this genus. The explanations are based on the fire ecology of the Cape that results in reproductive synchrony, reproductive doubling and competitive symmetry. Firstly, strict post-fire seedling establishment of the reseeder life-history in the Cape results in single-aged populations. Consequently, the reproductive and vegetative schedules of males must synchronously track that of females. This implies equal allocation to sex. Secondly, after fires, dioecious females have double the seedling to adult ratio of co-occurring hermaphrodites. This indicates that being liberated from male function allows females access to resources that double their fitness compared to hermaphrodites. Therefore, male and female costs of reproduction are equal in hermaphrodites. Thirdly, competitive symmetry must occur because males and female plants will frequently encounter each other as close near neighbours. Competitive asymmetry would both reduce mating opportunities and skew local sex ratios. The evidence to date is for 1:1 sex ratios in small plots and this indicates competitive symmetry and a lack of dimorphic niches. Finally, vegetatively dimorphic species must also allocate equally to sex, or else sexual asynchrony, lack of reproductive doubling or competitive asymmetry will occur.

evolutionary biology

Testing the Efforts Model of Simultaneous Interpreting: An ERP Study

We utilized the event-related potential (ERP) technique to study neural activity associated with different levels of working memory (WM) load during simultaneous interpretation (SI) in an ecologically valid setting. The amplitude of N1 and P1 components elicited by task-irrelevant tone probes was significantly modulated as a function of WM load but not the direction of interpretation. Furthermore, the latency of the N1 increased insignificantly with WM load. The P1 latency, however, mostly did not depend on either WM load or direction of interpretation. Larger negativity under lower WM loads suggests deeper processing of the auditory stimuli, providing tentative electrophysiological evidence in support of the Efforts Model of SI. Relationships between the direction of interpretation and median WM load are also discussed.

neuroscience

Evolutionary dynamics of mycorrhizal symbiosis in land plant diversification

Mycorrhizal symbiosis between soil fungi and land plants is one of the most widespread and ecologically important mutualisms on earth. It has long been hypothesized that the Glomeromycotina, the mycorrhizal symbionts of the majority of plants, facilitated colonization of land by plants in the Ordovician. This view was recently challenged by the discovery of mycorrhizal associations with Mucoromycotina in several early diverging lineages of land plants. Utilizing a large, species-level database of plants mycorrhizal associations and a Bayesian approach to state transition dynamics we here show that the recruitment of Mucoromycotina is the best supported transition from a non-mycorrhizal state. We further found that transitions between different combinations of either or both of Mucoromycotina and Glomeromycotina occur at high rates and found similar promiscuity among combinations that include either or both of Glomeromycotina and Ascomycota with a nearly fixed association with Basidiomycota. Our results demonstrate that under the most likely scenario symbiosis with Mucoromycotina enabled the establishment of early land plants.

evolutionary biology

The Hallucination Machine: A Deep-Dream VR platform for Studying the Phenomenology of Visual Hallucinations

Altered states of consciousness, such as psychotic or pharmacologically-induced hallucinations, provide a unique opportunity to examine the mechanisms underlying conscious perception. However, the phenomenological properties of these states are difficult to isolate experimentally from other, more general physiological and cognitive effects of psychoactive substances or psychopathological conditions. Thus, simulating phenomenological aspects of altered states in the absence of these other more general effects provides an important experimental tool for consciousness science and psychiatry. Here we describe such a tool, the Hallucination Machine. It comprises a novel combination of two powerful technologies: deep convolutional neural networks (DCNNs) and panoramic videos of natural scenes, viewed immersively through a head-mounted display (panoramic VR). By doing this, we are able to simulate visual hallucinatory experiences in a biologically plausible and ecologically valid way. Two experiments illustrate potential applications of the Hallucination Machine. First, we show that the system induces visual phenomenology qualitatively similar to classical psychedelics. In a second experiment, we find that simulated hallucinations do not evoke the temporal distortion commonly associated with altered states. Overall, the Hallucination Machine offers a valuable new technique for simulating altered phenomenology without directly altering the underlying neurophysiology.

neuroscience

Streptococcus pyogenes infection and the human proteome with a special focus on the IgG-cleaving enzyme IdeS

Infectious diseases are characterized by a complex interplay between host and pathogen, but how these interactions impact the host proteome is unclear. Here we applied a novel mass spectrometry based proteomics strategy to investigate how the human proteome is transiently modified by the pathogen Streptococcus pyogenes, with a particular focus on bacterial cleavage of IgG in vivo. In invasive diseases, S. pyogenes evokes a massive host response in blood, whereas superficial diseases are characterized by a local leakage of several blood plasma proteins at the site of infection including IgG. S. pyogenes produces IdeS, a protease cleaving IgG in the lower hinge region and we find highly effective IdeS-cleavage of IgG in samples from local IgG poor microenvironments. The results show that IdeS contributes to the adaptation of S. pyogenes to its normal ecological niches. Additionally, the work identifies novel clinical opportunities for in vivo pathogen detection.

microbiology

Calcimycocavitological Studies on Seashells from Beaches of North Goa, India

Calcimycocavitology deals with the study of hollowing out of spaces in hard calcareous seashells by the fungi called calcimycocavites. Endolithic fungi in the shells were first reported and named as the trace fossils in 1889 by Bornet and Flahault. Endolithic fungi bore inside the shell by the process of bioturbation by using organic acids (oxalic acid, citrate) and enzymes (proteases, dehydrogenases and oxidoreductases). Previous reports show the presence of tunnels formed by fungal hyphae in the shells. The present work reports preliminary results of calcimycocavitological studies on the seashells from beaches of north Goa, India. The calcareous sand samples were collected from Arambol, Ashvem, Morjim, Vagator, Anjuna, Baga and Miramar beaches by pool sampling method and were separated into different fractions by using standard sieves. Each fraction of sand was subjected to stereomicroscopic studies which revealed that the sand fraction between 150-250 m included irregular shell fragments showing positive colonization by calcimycocavites. Hydrochloric acid treatment was used to dissolve the shells and release calcimycocavites biomass which was stained with Congo Red and tentatively identified as distinct microfungal forms. SEM studies of the calcareous shell fragments revealed the microtunneling behavior of the fungi. Digital analysis of SEM images using Mountain premium 7.2 software revealed the fine topography of calcimycocavites hyphae along with unidentified presumptive biomineral encrustations. The ecological, biological and biogeochemical implications of the findings are presented with respect to possible role of calcimycocavites in Calcium and Carbon cycling by breakdown of the calcareous shells and release of inorganic and organic components in the ecosystem.

microbiology

MetQy: an R package to query metabolic functions of genes and genomes

SummaryWith the rapid accumulation of sequencing data from genomic and metagenomic studies, there is an acute need for better tools that facilitate their analyses against biological functions. To this end, we developed MetQy, an open-source R package designed for query-based analysis of functional units in [meta]genomes and/or sets of genes using the The Kyoto Encyclopedia of Genes and Genomes (KEGG) database. Furthermore, MetQy contains visualization and analysis tools and facilitates KEGGs flat file manipulation. Thus, MetQy enables better understanding of metabolic capabilities of known genomes or user-specified [meta]genomes by using the available information and can help guide studies in microbial ecology, metabolic engineering and synthetic biology.\n\nAvailability and ImplementationThe MetQy R package is freely available and can be downloaded from our groups website (http://osslab.lifesci.warwick.ac.uk) or GitHub (https://github.com/OSS-Lab/MetQy).\n\nContactO.Soyer@warwick.ac.uk

microbiology

A primitive starfish ancestor from the Early Ordovician of Morocco reveals the origin of crown group Echinodermata

The somasteroids are Ordovician star-shaped animals widely regarded as ancestors of Asterozoa, the group of extant echinoderms that includes brittle stars and starfish. The phylogenetic position of somasteroids makes them critical for understanding the origin and early evolution of crown group Echinodermata. However, the early evolution of asterozoans, the origin of their distinctive body organization and their relationships with other Cambrian and Ordovician echinoderms, such as edrioasteroids, blastozoans, crinoids, and other asterozoans, remain problematic due to the difficulties of comparing the calcitic endoskeleton of these disparate groups. Here we describe the new somasteroid Cantabrigiaster fezouataensis from the Early Ordovician (Tremadocian) Fezouata Lagerstatte in Morocco. Cantabrigiaster shares with other somasteroids the presence of rod-like virgal ossicles that articulate with the ambulacrals, but differs from all other known asterozoans in the absence of adambulacral ossicles defining the arm margins. The unique arm construction evokes parallels with non-asterozoan echinoderms. Developmentally informed Bayesian and parsimony based phylogenetic analyses, which reflect the homology of the biserial ambulacral ossicles in Paleozoic echinoderms according to the Extraxial-Axial Theory, recover Cantabrigiaster as basal within stem group Asterozoa. Our results indicate that Cantabrigiaster is the earliest diverging stem group asterozoan, revealing the ancestral morphology of this major clade and clarifying the affinities of problematic Ordovician taxa. Somasteroids are resolved as a paraphyletic grade within stem and crown group Asterozoa (starfishes), whereas stenuroids are paraphyletic within stem group Ophiuroidea (brittle stars). Cantabrigiaster also illuminates the relationship between Ordovician crown group Echinodermata and its Cambrian stem lineage, which includes sessile forms with incipient radial symmetry such as edrioasteroids and blastozoans. The contentious Pelmatozoa hypothesis (i.e. monophyly of blastozoans and crinoids) is not supported; instead, blastozoans represent the most likely sister-taxon of crown group Echinodermata.\n\nAuthor summaryStarfish and brittle stars, collectively known as asterozoans, constitute a diverse and ecologically successful group of echinoderms that first appear in the fossil record some 480Ma. However, the early evolution of asterozoans, the origin of their distinctive body organization, and their phylogenetic relationships with Cambrian echinoderms remain largely unresolved. We describe Cantabrigiaster fezouataensis gen. et sp. nov., a primitive asterozoan from the Fezouata Lagerstatte, Morocco, with a unique endoskeletal arm organization that reveals the ancestral morphology of this major clade. Bayesian and parsimony based phylogenetic analyses indicate that Cantabrigiaster is the earliest diverging stem group asterozoan, and resolve the phylogenetic position of Ordovician asterozoans such as somasteroids. Our analyses clarify the origin of crown group echinoderms relative to their problematic Cambrian stem group representatives.

paleontology