Bellenot et al. introduce hydathodes, an oft-overlooked plant organ that acts as a pressure valve to expel excess guttation sap at the leaf margin, typically visible at dawn.

Interview with Martin Giurfa, who studies learning and memory in insects at Paul Sabatier University.

Comment on Curr Biol. 2022 Jul 25;32(14):3016-3032.e3.

Comment on Curr Biol. 2022 Jul 25;32(14):3110-3120.e6.

The vertebrate intestine experiences a range of intrinsically generated and external forces during both development and adult homeostasis. It is increasingly understood how the coordination of these forces shapes the intestine through organ-scale folding and epithelial organization into crypt-villus compartments. Moreover, accumulating evidence shows that several cell types in the adult intestine can sense and respond to forces to regulate key cellular processes underlying adult intestinal functions and self-renewal. In this way, transduction of forces may direct both intestinal homeostasis as well as adaptation to external stimuli, such as food ingestion or injury. In this review, we will discuss recent insights from complementary model systems into the force-dependent mechanisms that establish and maintain the unique architecture of the intestine, as well as its homeostatic regulation and function throughout adult life.

Comment on Curr Biol. 2022 Jun 20;32(12):2730-2738.e5.

Comment in Curr Biol. 2022 Jul 25;32(14):R767-R769.

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Comment on Curr Biol. 2022 Jul 25;32(14):3048-3058.e6.

Comment on Curr Biol. 2022 Jul 25;32(14):3210-3218.e3.

Southern East Asia is the dispersal center regarding the prehistoric settlement and migrations of modern humans in Asia-Pacific regions. However, the settlement pattern and population structure of paleolithic humans in this region remain elusive, and ancient DNA can provide direct information. Here, we sequenced the genome of a Late Pleistocene hominin (MZR), dated ∼14.0 thousand years ago from Red Deer Cave located in Southwest China, which was previously reported possessing mosaic features of modern and archaic hominins. MZR is the first Late Pleistocene genome from southern East Asia. Our results indicate that MZR is a modern human who represents an early diversified lineage in East Asia. The mtDNA of MZR belongs to an extinct basal lineage of the M9 haplogroup, reflecting a rich matrilineal diversity in southern East Asia during the Late Pleistocene. Combined with the published data, we detected clear genetic stratification in ancient southern populations of East/Southeast Asia and some degree of south-versus-north divergency during the Late Pleistocene, and MZR was identified as a southern East Asian who exhibits genetic continuity to present day populations. Markedly, MZR is linked deeply to the East Asian ancestry that contributed to First Americans.

Comment on Nature. 2022 May;605(7909):332-339.

Dietary salt detection and consumption are crucial to maintaining fluid and ionic homeostasis. To optimize salt intake, animals employ salt-dependent activation of multiple taste pathways. Generally, sodium activates attractive taste cells, but attraction is overridden at high salt concentrations by cation non-selective activation of aversive taste cells. In flies, high salt avoidance is driven by both "bitter" taste neurons and a class of glutamatergic "high salt" neurons expressing pickpocket23 (ppk23). Although the cellular basis of salt taste has been described, many of the molecular mechanisms remain elusive. Here, we show that ionotropic receptor 7c (IR7c) is expressed in glutamatergic high salt neurons, where it functions with co-receptors IR76b and IR25a to detect high salt and is essential for monovalent salt taste. Misexpression of IR7c in sweet neurons, which endogenously express IR76b and IR25a, confers responsiveness to non-sodium salts, indicating that IR7c is sufficient to convert a sodium-selective gustatory receptor neuron to a cation non-selective one. Furthermore, the resultant transformation of taste neuron tuning switches potassium chloride from an aversive to an attractive tastant. This research provides insight into the molecular basis of monovalent and divalent salt-taste coding.

Comment on Curr Biol. 2022 Jul 25;32(14):3082-3094.e4.

Many bacterial species are capable of differentiating to create phenotypic heterogeneity. Using the aggregate-forming marine bacterium Vibrio splendidus, a new study reveals how this organism differentiates to form spherical structures with a motile, carbon-storing core and a non-motile shell.

Comment in Curr Biol. 2022 Jul 25;32(14):R779-R781.

Facultative multicellular behaviors expand the metabolic capacity and physiological resilience of bacteria. Despite their ubiquity in nature, we lack an understanding of how these behaviors emerge from cellular-scale phenomena. Here, we show how the coupling between growth and resource gradient formation leads to the emergence of multicellular lifecycles in a marine bacterium. Under otherwise carbon-limited growth conditions, Vibrio splendidus 12B01 forms clonal multicellular groups to collectively harvest carbon from soluble polymers of the brown-algal polysaccharide alginate. As they grow, groups phenotypically differentiate into two spatially distinct sub-populations: a static "shell" surrounding a motile, carbon-storing "core." Differentiation of these two sub-populations coincides with the formation of a gradient in nitrogen-source availability within clusters. Additionally, we find that populations of cells containing a high proportion of carbon-storing individuals propagate and form new clusters more readily on alginate than do populations with few carbon-storing cells. Together, these results suggest that local metabolic activity and differential partitioning of resources leads to the emergence of reproductive cycles in a facultatively multicellular bacterium.

Giant carnivorous dinosaurs such as Tyrannosaurus rex and abelisaurids are characterized by highly reduced forelimbs that stand in contrast to their huge dimensions, massive skulls, and obligate bipedalism.1,2 Another group that follows this pattern, yet is still poorly known, is the Carcharodontosauridae: dominant predators that inhabited most continents during the Early Cretaceous3-5 and reached their largest sizes in Aptian-Cenomanian times.6-10 Despite many discoveries over the last three decades, aspects of their anatomy, especially with regard to the skull, forearm, and feet, remain poorly known. Here we report a new carcharodontosaurid, Meraxes gigas, gen. et sp. nov., based on a specimen recovered from the Upper Cretaceous Huincul Formation of northern Patagonia, Argentina. Phylogenetic analysis places Meraxes among derived Carcharodontosauridae, in a clade with other massive South American species. Meraxes preserves novel anatomical information for derived carcharodontosaurids, including an almost complete forelimb that provides evidence for convergent allometric trends in forelimb reduction among three lineages of large-bodied, megapredatory non-avian theropods, including a remarkable degree of parallelism between the latest-diverging tyrannosaurids and carcharodontosaurids. This trend, coupled with a likely lower bound on forelimb reduction, hypothesized to be about 0.4 forelimb/femur length, combined to produce this short-armed pattern in theropods. The almost complete cranium of Meraxes permits new estimates of skull length in Giganotosaurus, which is among the longest for theropods. Meraxes also provides further evidence that carchardontosaurids reached peak diversity shortly before their extinction with high rates of trait evolution in facial ornamentation possibly linked to a social signaling role.

Comment in Curr Biol. 2022 Jul 25;32(14):R774-R776.

The global COVID-19 pandemic has presented a unique opportunity to explore the consequences of illegal exploitation on wildlife communities, as it continues to have wide-reaching impacts on multiple sectors, including local and national economies, international trade, and conservation enforcement1. The ongoing reductions in monitoring and enforcement during the pandemic have allowed increased opportunities for illegal, unreported, and unregulated activities, particularly for small-scale fisheries2. Even before the pandemic, policymakers and fisheries managers intent on controlling illegal fishing activities established marine protected areas (MPAs) that restrict or prohibit fishing3. Unfortunately, non-compliance with MPAs is often the rule rather than the exception, and less than 10% of the world's MPAs have managed to effectively reduce infringement4. The COVID-19 pandemic has exacerbated these management challenges: a recent review of MPAs worldwide has revealed a general decline in tourism revenue to operate park services during the pandemic, especially revenue needed for supporting personnel to monitor, patrol, and enforce restrictions2. Here, we compile infraction records of illegal fishing activities by both professional (commercial) and amateur (recreational) boats inside and outside of the Tupinambás Ecological Station and the Alcatrazes Wildlife Refuge (Figure 1A), notable for its high reef-fish biomass and diversity in the Southwestern Atlantic5. We show that illegal exploitation has shifted since the onset of the pandemic, targeting larger, higher-value species that contribute disproportionately to the structure and function of reef-fish communities in the region.

Current treatments for trauma-related disorders remain ineffective for many patients.1,2 Fear extinction deficiency is a prominent feature of these diseases,3 and many behavioral treatments rely on extinction training.4,5 However, in many patients, therapy is followed by a relapse of symptoms, and the underpinnings of such interindividual variations in vulnerability to relapse remain unknown.6-8 Here, we modeled interindividual differences in post-therapy fear relapse with an ethologically relevant trauma recovery paradigm. After fear conditioning, male rats underwent fear extinction while foraging in a large enriched arena, permitting the expression of a wide spectrum of behaviors. An automated multidimensional behavioral assessment revealed that post-conditioning fear response profiles clustered into two groups: some animals expressed fear by freezing more, whereas others darted more, as if fleeing from danger. Remarkably, the tendency of an animal to dart or to freeze after CS presentation during the first extinction session was, respectively, associated with stronger or weaker fear renewal. Moreover, genome-wide transcriptional profiling revealed that these groups differentially regulated specific sets of genes, some of which were previously implicated in anxiety and trauma-related disorders. Our results suggest that post-trauma behavioral phenotypes and the associated gene expression landscapes can serve as markers of fear relapse susceptibility and thus may be instrumental for future development of more effective treatments for psychiatric patients.

Comment in Curr Biol. 2022 Jul 25;32(14):R781-R783.

Neural circuits must both execute the behavioral repertoire of individuals and account for behavioral variation across species. Understanding how this variation emerges over evolutionary time requires large-scale phylogenetic comparisons of behavioral repertoires. Here, we describe the evolution of walking in fruit flies by capturing high-resolution, unconstrained movement from 13 species and 15 strains of drosophilids. We find that walking can be captured in a universal behavior space, the structure of which is evolutionarily conserved. However, the occurrence of and transitions between specific movements have evolved rapidly, resulting in repeated convergent evolution in the temporal structure of locomotion. Moreover, a meta-analysis demonstrates that many behaviors evolve more rapidly than other traits. Thus, the architecture and physiology of locomotor circuits can execute precise individual movements in one species and simultaneously support rapid evolutionary changes in the temporal ordering of these modular elements across clades.

Comment in Curr Biol. 2022 Jul 25;32(14):R788-R790.

Globally, species distributions are shifting in response to environmental change,1 and those that cannot disperse risk extinction.2 Many taxa, including marine species, are showing poleward range shifts as the climate warms.3 In the Southern Hemisphere, however, circumpolar oceanic fronts can present barriers to dispersal.4 Although passive, southward movement of species across this barrier has been considered unlikely,5,6 the recent discovery of buoyant kelp rafts on beaches in Antarctica7,8 demonstrates that such journeys are possible. Rafting is a key process by which diverse taxa-including terrestrial, e.g., Lindo,9 Godinot,10 and Censky et al.,11 and marine, e.g., Carlton et al.12 and Gillespie et al.13 species-can cross oceans.14 Kelp rafts can carry passengers7,15-17 and thus can act as vectors for long-distance dispersal of coastal organisms. The small numbers of kelp rafts previously found in Antarctica7,8 do not, however, shed much light on the frequency of such dispersal events.18 We use a combination of high-resolution phylogenomic analyses (>220,000 SNPs) and oceanographic modeling to show that long-distance biological dispersal events in Southern Ocean are not rare. We document tens of kelp (Durvillaea antarctica) rafting events of thousands of kilometers each, over several decades (1950-2019), with many kelp rafts apparently still reproductively viable. Modeling of dispersal trajectories from genomically inferred source locations shows that distant landmasses are well connected, for example South Georgia and New Zealand, and the Kerguelen Islands and Tasmania. Our findings illustrate the power of genomic approaches to track, and modeling to show frequencies of, long-distance dispersal events.

Comment in Curr Biol. 2022 Jul 25;32(14):R776-R778.

Visual skill learning is the process of improving responses to surrounding visual stimuli.1 For individuals with autism spectrum disorders (ASDs), efficient skill learning may be especially valuable due to potential difficulties with sensory processing2 and challenges in adjusting flexibly to changing environments.3,4 Standard skill learning protocols require extensive practice with multiple stimulus repetitions,5-7 which may be difficult for individuals with ASD and create abnormally specific learning with poor ability to generalize.4 Motivated by findings indicating that brief memory reactivations can facilitate skill learning,8,9 we hypothesized that reactivation learning with few stimulus repetitions will enable efficient learning in individuals with ASD, similar to their learning with standard extensive practice protocols used in previous studies.4,10,11 We further hypothesized that in contrast to experience-dependent plasticity often resulting in specificity, reactivation-induced learning would enable generalization patterns in ASD. To test our hypotheses, high-functioning adults with ASD underwent brief reactivations of an encoded visual learning task, consisting of only 5 trials each instead of hundreds. Remarkably, individuals with ASD improved their visual discrimination ability in the task substantially, demonstrating successful learning. Furthermore, individuals with ASD generalized learning to an untrained visual location, indicating a unique benefit of reactivation learning mechanisms for ASD individuals. Finally, an additional experiment showed that without memory reactivations ASD subjects did not demonstrate efficient learning and generalization patterns. Taken together, the results provide proof-of-concept evidence supporting a distinct route for efficient visual learning and generalization in ASD, which may be beneficial for skill learning in other sensory and motor domains.

Comment in Curr Biol. 2022 Aug 8;32(15):R828-R830.

Stomata regulate plant water use and photosynthesis by controlling leaf gas exchange. They do this by reversibly opening the pore formed by two adjacent guard cells, with the limits of this movement ultimately set by the mechanical properties of the guard cell walls and surrounding epidermis.1,2 A body of evidence demonstrates that the methylation status and cellular patterning of pectin wall polymers play a core role in setting the guard cell mechanical properties, with disruption of the system leading to poorer stomatal performance.3-6 Here we present genetic and biochemical data showing that wall arabinans modulate guard cell flexibility and can be used to engineer stomata with improved performance. Specifically, we show that a short-chain linear arabinan epitope associated with the presence of rhamnogalacturonan I in the guard cell wall is required for full opening of the stomatal pore. Manipulations leading to the novel accumulation of longer-chain arabinan epitopes in guard cell walls led to an increase in the maximal pore aperture. Using computational modeling combined with atomic force microscopy, we show that this phenotype reflected a decrease in wall matrix stiffness and, consequently, increased flexing of the guard cells under turgor pressure, generating larger, rounder stomatal pores. Our results provide theoretical and experimental support for the conclusion that arabinan side chains of pectin modulate guard cell wall stiffness, setting the limits for cell flexing and, consequently, pore aperture, gas exchange, and photosynthetic assimilation.

Dissecting neural connectivity patterns within local brain regions is an essential step to understanding the function of the brain.1 Neural microcircuits in brain regions, such as the neocortex and the hippocampus, have been extensively studied.2 By contrast, the microcircuit in the hypothalamus remains largely uncharacterized. The hypothalamus is crucial for animals' survival and reproduction.3 Knowledge of how different hypothalamic nuclei coordinate with each other and outside brain regions for hypothalamus-related functions has been significantly advanced.4-9 Although there are limited studies on the neural microcircuit in the lateral hypothalamus (LHA)10,11 and the suprachiasmatic nucleus (SCN),12,13 the patterns of neural microcircuits in most of the given hypothalamic nuclei remain largely unknown. This study applied combinatory approaches to address the local neural circuit pattern in the ventromedial hypothalamus (VMH) and other hypothalamic nuclei. We discovered a unique neural circuit design in the VMH. Neurons in the VMH were electrically coupled at the early postnatal stage like ones in the neocortex.14 However, unlike neocortical neurons,14,15 they developed very few chemical synapses after the disappearance of electrical synapses. Instead, VMH neurons communicated with neuropeptides. The similar scarceness of synaptic connectivity found in other hypothalamic nuclei further indicated that the lack of synaptic connections is a unique feature for local neural circuits in most adult hypothalamic nuclei. Thus, our findings provide a solid synaptic basis at the cellular level to understand hypothalamic functions better.

Physiological and pathological cardiac stress induced by exercise and hypertension, respectively, increase the hemodynamic load for the heart and trigger specific hypertrophic signals in cardiomyocytes leading to adaptive or maladaptive cardiac hypertrophy responses involving a mechanosensitive remodeling of the contractile cytoskeleton. Integrins sense load and have been implicated in cardiac hypertrophy, but how they discriminate between the two types of cardiac stress and translate mechanical loads into specific cytoskeletal signaling pathways is not clear. Here, we report that the focal adhesion protein β-parvin is highly expressed in cardiomyocytes and facilitates the formation of cell protrusions, the serial assembly of newly synthesized sarcomeres, and the hypertrophic growth of neonatal rat ventricular cardiomyocytes (NRVCs) in vitro. In addition, physiological mechanical loading of NRVCs by either the application of cyclic, uni-axial stretch, or culture on physiologically stiff substrates promotes NRVC elongation in a β-parvin-dependent manner, which is achieved by binding of β-parvin to α/β-PIX, which in turn activates Rac1. Importantly, loss-of-function studies in mice also revealed that β-parvin is essential for the exercise-induced cardiac hypertrophy response in vivo. Our results identify β-parvin as a novel mechano-responsive signaling hub in hypertrophic cardiomyocytes that drives cell elongation in response to physiological mechanical loads.

Diverse light-sensing organs (i.e., eyes) have evolved across animals. Interestingly, several subcellular analogs have been found in eukaryotic microbes.1 All of these systems have a common "recipe": a light occluding or refractory surface juxtaposed to a membrane-layer enriched in type I rhodopsins.1-4 In the fungi, several lineages have been shown to detect light using a diversity of non-homologous photo-responsive proteins.5-7 However, these systems are not associated with an eyespot-like organelle with one exception found in the zoosporic fungus Blastocladiella emersonii (Be).8Be possesses both elements of this recipe: an eyespot composed of lipid-filled structures (often called the side-body complex [SBC]), co-localized with a membrane enriched with a gene-fusion protein composed of a type I (microbial) rhodopsin and guanylyl cyclase enzyme domain (CyclOp-fusion protein).8,9 Here, we identify homologous pathway components in four Chytridiomycota orders (Chytridiales, Synchytriales, Rhizophydiales, and Monoblepharidiales). To further explore the architecture of the fungal zoospore and its lipid organelles, we reviewed electron microscopy data (e.g., the works of Barr and Hartmann10 and Reichle and Fuller11) and performed fluorescence-microscopy imaging of four CyclOp-carrying zoosporic fungal species, showing the presence of a variety of candidate eyespot-cytoskeletal ultrastructure systems. We then assessed the presence of canonical photoreceptors across the fungi and inferred that the last common fungal ancestor was able to sense light across a range of wavelengths using a variety of systems, including blue-green-light detection. Our data imply, independently of how the fungal tree of life is rooted, that the apparatus for a CyclOp-organelle light perception system was an ancestral feature of the fungi.

Comment in Curr Biol. 2022 Jul 25;32(14):R769-R771.

Cyclic GMP-AMP synthase (cGAS) and stimulator of interferon genes (STING, also known as TMEM173) constitute the major signaling pathway in vertebrates that senses non-self DNA and elicits potent immune responses. At the core of this pathway, cGAS senses double-stranded DNA (dsDNA) and synthesizes cyclic GMP-AMP (cGAMP). cGAMP serves as a second messenger that relays its signal to downstream innate immune responses through STING. One of the major consequences triggered by the cGAS-STING pathway is the production of antiviral cytokines of the type I interferon family, which in turn induce expression of hundreds of interferon-stimulated genes (ISGs) with diverse antiviral functions. Recent studies have also revealed functional homologs across phylogenetic kingdoms with innate defense functions, suggesting an ancient evolutionary origin of cGAS-STING signaling. Aberrant activation of the cGAS-STING pathway by host DNA can lead to sterile inflammation associated with tissue damage, degeneration as well as premature aging. In this primer, we will introduce the basic principles of cGAS-STING signaling in the vertebrate system and highlight recent discoveries regarding its connection to other fundamental cellular processes in the context of human diseases.

In this Quick guide, Bertram et al. discuss the environmental sources of endocrine-disrupting chemicals and their effects on biological systems.

Pocket gophers (Geomys spp.) are solitary, root-eating fossorial rodents native to North and Central American grasslands and are presumed to acquire most of their food through excavation of tunnels maintained as part of tunnel systems up to 160 m long1,2. Given that burrowing is 360-3,400 times more energetically costly than surface walking, pocket gophers have high energy requirements3. Roots are scarce at the depths of their tunnels in the sandy soil of our study site (20-64 cm), but here we describe a novel food source for southeastern pocket gophers (Geomys pinetis, hereafter gophers): roots that grow into their tunnels. These roots could supply an average of 21% but up to 62% of their daily basal energetic needs.

Comment on Curr Biol. 2022 Jul 11;32(13):2871-2883.e4.

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Comment on Nature. 2022 Jun;606(7916):937-944.

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Comment on Curr Biol. 2022 Jun 20;32(12):2621-2631.e3.

Climate change adversely affects plant nutrition, which serves as a major hurdle in the production of enough nutritious food to meet the needs of the growing global population. Here, we discuss how various climatic stressors impact nutrient homeostasis and how natural variation studies can yield resilient crop production systems to ensure future food security.

Comment on Nature. 2022 Apr;604(7906):517-524.

Pollen, a neighbor-less cell containing the male gametes, undergoes mechanical challenges during plant sexual reproduction, including desiccation and rehydration. It was previously shown that the pollen-specific mechanosensitive ion channel MscS-like (MSL)8 is essential for pollen survival during hydration and proposed that it functions as a tension-gated osmoregulator. Here, we test this hypothesis with a combination of mathematical modeling and laboratory experiments. Time-lapse imaging revealed that wild-type pollen grains swell, and then they stabilize in volume rapidly during hydration. msl8 mutant pollen grains, however, continue to expand and eventually burst. We found that a mathematical model, wherein MSL8 acts as a simple-tension-gated osmoregulator, does not replicate this behavior. A better fit was obtained from variations of the model, wherein MSL8 inactivates independent of its membrane tension gating threshold or MSL8 strengthens the cell wall without osmotic regulation. Experimental and computational testing of several perturbations, including hydration in an osmolyte-rich solution, hyper-desiccation of the grains, and MSL8-YFP overexpression, indicated that the cell wall strengthening model best simulated experimental responses. Finally, the expression of a nonconducting MSL8 variant did not complement the msl8 overexpansion phenotype. These data indicate that contrary to our hypothesis and to the current understanding of MS ion channel function in bacteria, MSL8 does not act as a simple membrane tension-gated osmoregulator. Instead, they support a model wherein ion flux through MSL8 is required to alter pollen cell wall properties. These results demonstrate the utility of pollen as a cellular scale model system and illustrate how mathematical models can correct intuitive hypotheses.

The ring-like cohesin complex plays an essential role in chromosome segregation, organization, and double-strand break repair through its ability to bring two DNA double helices together. Scc2 (NIPBL in humans) together with Scc4 functions as the loader of cohesin onto chromosomes. Chromatin adapters such as the RSC complex facilitate the localization of the Scc2-Scc4 cohesin loader. Here, we identify a broad range of Scc2-chromatin protein interactions that are evolutionarily conserved and reveal a role for one complex, Mediator, in the recruitment of the cohesin loader. We identified budding yeast Med14, a subunit of the Mediator complex, as a high copy suppressor of poor growth in Scc2 mutant strains. Physical and genetic interactions between Scc2 and Mediator are functionally substantiated in direct recruitment and cohesion assays. Depletion of Med14 results in defective sister chromatid cohesion and the decreased binding of Scc2 at RNA Pol II-transcribed genes. Previous work has suggested that Mediator, Nipbl, and cohesin connect enhancers and promoters of active mammalian genes. Our studies suggest an evolutionarily conserved fundamental role for Mediator in the direct recruitment of Scc2 to RNA Pol II-transcribed genes.

Symbiosis is one of the most important evolutionary processes shaping the biodiversity on Earth. Symbiotic associations often bring together organisms from different domains of life, which can provide an unparalleled route to evolutionary innovation.1-4 The phylum Apicomplexa encompasses 6,000 ubiquitous animal parasites; however, species in the recently described apicomplexan family, Nephromycidae, are reportedly non-virulent.5,6 The members of the genus Nephromyces live within a specialized organ of tunicates, called the renal sac, in which they use concentrated uric acid as a primary nitrogen source.7,8 Here, we report genomic and transcriptomic data from the diverse genus Nephromyces, as well as the three bacterial symbionts that live within this species complex. We show that the diversity of Nephromyces is unexpectedly high within each renal sac, with as many as 20 different species inhabiting the renal sacs in wild populations. The many species of Nephromyces can host three different types of bacterial endosymbionts; however, FISH microscopy allowed us to demonstrate that each individual Nephromyces cell hosts only a single bacterial type. Through the reconstruction and analyses of the endosymbiont bacterial genomes, we infer that each bacterial type supplies its host with different metabolites. No individual species of Nephromyces, in combination with its endosymbiont, can produce a complete set of essential amino acids, and culture experiments demonstrate that individual Nephromyces species cannot form a viable infection. Therefore, we hypothesize that Nephromyces spp. depend on co-infection with congeners containing different bacterial symbionts in order to exchange metabolites to meet their needs.

The evolution of eusociality has allowed ants to become one of the most conspicuous and ecologically dominant groups of organisms in the world. A large majority of the current ∼14,000 ant species belong to the formicoids,1 a clade of nine subfamilies that exhibit the most extreme forms of reproductive division of labor, large colony size,2 worker polymorphism,3 and extended queen longevity.4 The eight remaining non-formicoid subfamilies are less well studied, with few genomes having been sequenced so far and unclear phylogenetic relationships.5 By sequencing 65 genomes, we provide a robust phylogeny of the 17 ant subfamilies, retrieving high support to the controversial leptanillomorph clade (Leptanillinae and Martialinae) as the sister group to all other extant ants. Moreover, our genomic analyses revealed that the emergence of the formicoids was accompanied by an elevated number of positive selection events. Importantly, the top three gene functions under selection are linked to key features of complex eusociality, with histone acetylation being implicated in caste differentiation, gene silencing by RNA in worker sterility, and autophagy in longevity. These results show that the key pathways associated with eusociality have been under strong selection during the Cretaceous, suggesting that the molecular foundations of complex eusociality may have evolved rapidly in less than 20 Ma.

Comment in Curr Biol. 2022 Jul 11;32(13):R748-R750.

In temperate and boreal regions, perennials adapt their annual growth cycle to the change of seasons. These adaptations ensure survival in harsh environmental conditions, allowing growth at different latitudes and altitudes, and are therefore tightly regulated. Populus tree species cease growth and form terminal buds in autumn when photoperiod falls below a certain threshold.1 This is followed by establishment of dormancy and cold hardiness over the winter. At the center of the photoperiodic pathway in Populus is the gene FLOWERING LOCUS T2 (FT2), which is expressed during summer and harbors significant SNPs in its locus associated with timing of bud set.1-4 The paralogous gene FT1, on the other hand, is hyper-induced in chilling buds during winter.3,5 Even though its function is so far unknown, it has been suggested to be involved in the regulation of flowering and the release of winter dormancy.3,5 In this study, we employ CRISPR-Cas9-mediated gene editing to individually study the function of the FT-like genes in Populus trees. We show that while FT2 is required for vegetative growth during spring and summer and regulates the entry into dormancy, expression of FT1 is absolutely required for bud flush in spring. Gene expression profiling suggests that this function of FT1 is linked to the release of winter dormancy rather than to the regulation of bud flush per se. These data show how FT duplication and sub-functionalization have allowed Populus trees to regulate two completely different and major developmental control points during the yearly growth cycle.

The cerebral cortices of human and nonhuman primate brains are characterized by submillimeter functional domains. However, little is known about the connections of single functional domains. Here, in macaque monkey visual cortex, we have developed a targeted focal electrical stimulation method, coupled with functional optical imaging, to map cortical networks with submillimeter precision in vivo. We find that single functional domains are a part of highly specific and sparse intra-areal and inter-areal micro-networks. Across color-related and orientation-related functionalities, these micro-networks exhibit parallel connection patterns, suggesting a common domain-based architecture. Moreover, these micro-networks shift topographically at a submillimeter scale, suggesting that they serve as a fundamental unit for cortical information processing. Our findings establish a domain-based connectional architecture in the primate brain and present new constraints for cortical map representation.

When faced with imminent danger, animals must rapidly take defensive actions to reach safety. Mice can react to threatening stimuli in ∼250 milliseconds1 and, in simple environments, use spatial memory to quickly escape to shelter.2,3 Natural habitats, however, often offer multiple routes to safety that animals must identify and choose from.4 This is challenging because although rodents can learn to navigate complex mazes,5,6 learning the value of different routes through trial and error during escape could be deadly. Here, we investigated how mice learn to choose between different escape routes. Using environments with paths to shelter of varying length and geometry, we find that mice prefer options that minimize path distance and angle relative to the shelter. This strategy is already present during the first threat encounter and after only ∼10 minutes of exploration in a novel environment, indicating that route selection does not require experience of escaping. Instead, an innate heuristic assigns survival value to each path after rapidly learning the spatial environment. This route selection process is flexible and allows quick adaptation to arenas with dynamic geometries. Computational modeling shows that model-based reinforcement learning agents replicate the observed behavior in environments where the shelter location is rewarding during exploration. These results show that mice combine fast spatial learning with innate heuristics to choose escape routes with the highest survival value. The results further suggest that integrating prior knowledge acquired through evolution with knowledge learned from experience supports adaptation to changing environments and minimizes the need for trial and error when the errors are costly.

Bats have evolved behavioral specializations that are unique among mammals, including self-propelled flight and echolocation. However, areas of motor cortex that are critical in the generation and fine control of these unique behaviors have never been fully characterized in any bat species, despite the fact that bats compose ∼25% of extant mammalian species. Using intracortical microstimulation, we examined the organization of motor cortex in Egyptian fruit bats (Rousettus aegyptiacus), a species that has evolved a novel form of tongue-based echolocation.1,2 We found that movement representations include an enlarged tongue region containing discrete subregions devoted to generating distinct tongue movement types, consistent with their behavioral specialization generating active sonar using tongue clicks. This magnification of the tongue in motor cortex is comparable to the enlargement of somatosensory representations in species with sensory specializations.3-5 We also found a novel degree of coactivation between the forelimbs and hindlimbs, both of which are involved in altering the shape and tension of wing membranes during flight. Together, these findings suggest that the organization of motor cortex has coevolved with peripheral morphology in bats to support the unique motor demands of flight and echolocation.

The mouse visual cortex contains interconnected higher visual areas, but their functional specializations are unclear. Here, we used a data-driven approach to examine the representations of complex visual stimuli by L2/3 neurons across mouse higher visual areas, measured using large-field-of-view two-photon calcium imaging. Using specialized stimuli, we found higher fidelity representations of texture in area LM, compared to area AL. Complementarily, we found higher fidelity representations of motion in area AL, compared to area LM. We also observed this segregation of information in response to naturalistic videos. Finally, we explored how receptive field models of visual cortical neurons could produce the segregated representations of texture and motion we observed. These selective representations could aid in behaviors such as visually guided navigation.

Comment in Curr Biol. 2022 Jul 11;32(13):R741-R743.

Although pain-related excessive fear is known to be a key factor in chronic pain disability, which involves the anterior cingulate cortex (ACC), little is known about the downstream circuits of the ACC for fear avoidance in pain processing. Using behavioral experiments and functional magnetic resonance imaging with optogenetics at 15.2 T, we demonstrate that the ACC is a part of the abnormal circuit changes in chronic pain and its downstream circuits are closely related to modulating sensorimotor integration and generating active movement rather than carrying sensory information. The projection from the ACC to the dorsolateral and lateral parts of the periaqueductal gray (dl/lPAG) especially enhances both reflexive and active avoidance behavior toward pain. Collectively, our results indicate that increased signals from the ACC to the dl/lPAG might be critical for excessive fear avoidance in chronic pain disability.

Comment on Curr Biol. 2022 Jul 11;32(13):2848-2857.e6.

As tropical forests are becoming increasingly fragmented, understanding the magnitude and time frame of biodiversity declines is vital for 21st century sustainability goals. Over three decades, we monitored post-isolation changes in small mammal species richness and abundance within a forest landscape fragmented by the construction of a dam in Thailand.1,2 We observed the near-complete collapse of species richness within 33 years, with no evidence of a recolonization effect across repeatedly sampled islands. Our results further revealed a decline in species richness as island size decreased and isolation time increased, accelerated by the increasing dominance of the ubiquitous Malayan field rat, Rattus tiomanicus. This species was already hyper-abundant on smaller islands in the initial surveys (1992-1994, 66% of individuals) but became monodominant on all islands, regardless of island size, by the most recent survey (2020, 97%). Our results suggest that insular forest fragments are highly susceptible to rapid species loss, particularly due to the competitive nature of Rattus accelerating the rate at which extinction debts are paid. To mitigate these impacts, reducing the extent of habitat degradation, as triggered by fragmentation and exacerbated by isolation time, can help to sustain native biodiversity while averting Rattus hyper-abundance.

Alternative splicing of Drosophila Dscam1 into 38,016 isoforms provides neurons with a unique molecular code for self-recognition and self-avoidance. A canonical model suggests that the homophilic binding of identical Dscam1 isoforms on the sister branches of mushroom body (MB) axons supports segregation with high fidelity, even when only a single isoform is expressed. Here, we generated a series of mutant flies with a single exon 4, 6, or 9 variant, encoding 1,584, 396, or 576 potential isoforms, respectively. Surprisingly, most of the mutants in the latter two groups exhibited obvious defects in the growth, branching, and segregation of MB axonal sister branches. This demonstrates that the repertoires of 396 and 576 Dscam1 isoforms were not sufficient for the normal patterning of axonal branches. Moreover, reducing Dscam1 levels largely reversed the defects caused by reduced isoform diversity, suggesting a functional link between Dscam1 expression levels and isoform diversity. Taken together, these results indicate that canonical self-avoidance alone does not explain the function of Dscam1 in MB axonal wiring.

In many instances, external sensory-evoked neuronal activity is used by the brain to select the most appropriate behavioral response. Predator-avoidance behaviors such as freezing and escape1,2 are of particular interest since these stimulus-evoked responses are behavioral manifestations of a decision-making process that is fundamental to survival.3,4 Over the lifespan of an individual, however, the threat value of agents in the environment is believed to undergo constant revision,5 and in some cases, repeated avoidance of certain stimuli may no longer be an optimal behavioral strategy.6 To begin to study this type of adaptive control of decision-making, we devised an experimental paradigm to probe the properties of threat escape in the laboratory mouse Mus musculus. First, we found that while robust escape to visual looming stimuli can be observed after 2 days of social isolation, mice can also rapidly learn that such stimuli are non-threatening. This learned suppression of escape (LSE) is extremely robust and can persist for weeks and is not a generalized adaptation, since flight responses to novel live prey and auditory threat stimuli in the same environmental context were maintained. We also show that LSE cannot be explained by trial number or a simple form of stimulus desensitization since it is dependent on threat-escape history. We propose that the action selection process mediating escape behavior is constantly updated by recent threat history and that LSE can be used as a robust model system to understand the neurophysiological mechanisms underlying experience-dependent decision-making.

Some prokaryotes possess CRISPR-Cas systems that use DNA segments called spacers, which are acquired from invading phages, to guide immune defense. Here, we propose that cross-reactive CRISPR targeting can, however, lead to "heterologous autoimmunity," whereby foreign spacers guide self-targeting in a spacer-length-dependent fashion. Balancing antiviral defense against autoimmunity predicts a scaling relation between spacer length and CRISPR repertoire size. We find evidence for this scaling through a comparative analysis of sequenced prokaryotic genomes and show that this association also holds at the level of CRISPR types. By contrast, the scaling is absent in strains with nonfunctional CRISPR loci. Finally, we demonstrate that stochastic spacer loss can explain variations around the scaling relation, even between strains of the same species. Our results suggest that heterologous autoimmunity is a selective factor shaping the evolution of CRISPR-Cas systems, analogous to the trade-offs between immune specificity, breadth, and autoimmunity that constrain the diversity of adaptive immune systems in vertebrates.

Comment in Curr Biol. 2022 Jul 11;32(13):R736-R738.

Comment in Curr Biol. 2022 Jul 11;32(13):R746-R748.

Comment in Curr Biol. 2022 Jul 11;32(13):R738-R741.

To create an accurate percept of the world, the visual system relies on past experience and prior assumptions.1 For example, although the retinal projection of an object moving in depth changes drastically, we still perceive the object at a constant size and velocity.2,3 Consequently, if we see the same object with a constant retinal size at two different depth levels, the perceived size differs (illustrated by the Ponzo illusion). Past experience also directly influences perceptual judgments, an effect known as serial dependence.4,5 Such sequential effects have also been reported for oculomotor behavior, even on the trial-by-trial level.6-10 An integration of past experiences seems like a smart and sophisticated mechanism to reduce uncertainty and improve behavior in a world full of statistical regularities. By leveraging the Ponzo illusion to dissociate perceived size and speed from retinal signals, we show that serial-dependence effects for oculomotor control are mediated by retinal error signals. These sequential effects likely take place in early sensory processing because they transfer to different visual stimuli. In contrast to recently reported history effects for perceptual decisions,11 sequential effects for oculomotor control deviate from perceptual mechanisms by not integrating spatial context and by ignoring size and velocity constancy. Although this dissociation might appear suboptimal, we argue that this effect reveals the different goals of the oculomotor and perceptual systems. The oculomotor system tries to reduce retinal error signals to bring and keep the target close to the fovea, whereas the visual system interprets retinal input to achieve an accurate representation of the world.12.