Membrane function is fundamental to life. Each species explores membrane lipid diversity within a genetically predefined range of possibilities. How membrane lipid composition in turn defines the functional space available for evolution of membrane-centered processes remains largely unknown. We address this fundamental question using related fission yeasts Schizosaccharomyces pombe and Schizosaccharomyces japonicus. We show that, unlike S. pombe that generates membranes where both glycerophospholipid acyl tails are predominantly 16–18 carbons long, S. japonicus synthesizes unusual “asymmetrical” glycerophospholipids where the tails differ in length by 6–8 carbons. This results in stiffer bilayers with distinct lipid packing properties. Retroengineered S. pombe synthesizing the S.-japonicus-type phospholipids exhibits unfolded protein response and downregulates secretion. Importantly, our protein sequence comparisons and domain swap experiments support the hypothesis that transmembrane helices co-evolve with membranes, suggesting that, on the evolutionary scale, changes in membrane lipid composition may necessitate extensive adaptation of the membrane-associated proteome.

The hippocampus plays a critical role in sleep-related memory processes [1, 2, 3], but it is unclear which specific sleep features are dependent upon this brain structure. The examination of sleep physiology in patients with focal bilateral hippocampal damage and amnesia could supply important evidence regarding these links. However, there is a dearth of such studies, despite these patients providing compelling insights into awake cognition [4, 5]. Here, we sought to identify the contribution of the hippocampus to the sleep phenotype by characterizing sleep via comprehensive qualitative and quantitative analyses in memory-impaired patients with selective bilateral hippocampal damage and matched control participants using in-home polysomnography on 4 nights. We found that, compared to control participants, patients had significantly reduced slow-wave sleep—likely due to decreased density of slow waves—as well as slow-wave activity. In contrast, slow and fast spindles were indistinguishable from those of control participants. Moreover, patients expressed slow oscillations (SOs), and SO-fast spindle coupling was observed. However, on closer scrutiny, we noted that the timing of spindles within the SO cycle was delayed in the patients. The shift of patients’ spindles into the later phase of the up-state within the SO cycle may indicate a mismatch in timing across the SO-spindle-ripple events that are associated with memory consolidation [6, 7]. The substantial effect of selective bilateral hippocampal damage on large-scale oscillatory activity in the cortex suggests that, as with awake cognition, the hippocampus plays a significant role in sleep physiology, which may, in turn, be necessary for efficacious episodic memory.

Human adults flawlessly and effortlessly navigate boundaries and obstacles in the immediately visible environment, a process we refer to as “visually guided navigation.” Neuroimaging work in adults suggests this ability involves the occipital place area (OPA) [1, 2]—a scene-selective region in the dorsal stream that selectively represents information necessary for visually guided navigation [3, 4, 5, 6, 7, 8, 9]. Despite progress in understanding the neural basis of visually guided navigation, however, little is known about how this system develops. Is navigationally relevant information processing present in the first few years of life? Or does this information processing only develop after many years of experience? Although a handful of studies have found selective responses to scenes (relative to objects) in OPA in childhood [10, 11, 12, 13], no study has explored how more specific navigationally relevant information processing emerges in this region. Here, we do just that by measuring OPA responses to first-person perspective motion information—a proxy for the visual experience of actually navigating the immediate environment—using fMRI in 5- and 8-year-old children. We found that, although OPA already responded more to scenes than objects by age 5, responses to first-person perspective motion were not yet detectable at this same age and rather only emerged by age 8. This protracted development was specific to first-person perspective motion through scenes, not motion on faces or objects, and was not found in other scene-selective regions (the parahippocampal place area or retrosplenial complex) or a motion-selective region (MT). These findings therefore suggest that navigationally relevant information processing in OPA undergoes prolonged development across childhood.

Outcome-guided behavior requires knowledge about the current value of expected outcomes. Such behavior can be isolated in the reinforcer devaluation task, which assesses the ability to infer the current value of specific rewards after devaluation. Animal lesion studies demonstrate that orbitofrontal cortex (OFC) is necessary for normal behavior in this task, but a causal role for human OFC in outcome-guided behavior has not been established. Here, we used sham-controlled, non-invasive, continuous theta-burst stimulation (cTBS) to temporarily disrupt human OFC network activity by stimulating a site in the lateral prefrontal cortex that is strongly connected to OFC prior to devaluation of food odor rewards. Subjects in the sham group appropriately avoided Pavlovian cues associated with devalued food odors. However, subjects in the stimulation group persistently chose those cues, even though devaluation of food odors themselves was unaffected by cTBS. This behavioral impairment was mirrored in changes in resting-state functional magnetic resonance imaging (rs-fMRI) activity such that subjects in the stimulation group exhibited reduced OFC network connectivity after cTBS, and the magnitude of this reduction was correlated with choices after devaluation. These findings demonstrate the feasibility of indirectly targeting the human OFC with non-invasive cTBS and indicate that OFC is specifically required for inferring the value of expected outcomes.

Rhizomes are modified stems that grow horizontally underground in various perennial species, a growth habit that is advantageous for vigorous asexual proliferation. In Oryza longistaminata, a rhizomatous wild relative of cultivated rice (Oryza sativa), leaves in the aerial shoots consist of a distal leaf blade and a proximal leaf sheath [1]. Leaf blade formation is, however, suppressed in rhizome leaves. In O. sativa, BLADE-ON-PETIOLE (BOP) genes are the main regulators of proximal-distal leaf patterning [2]. During the juvenile phase of O. sativa, BOP expression is maintained at high levels by the small regulatory RNA microRNA156 (miR156), leading to formation of leaves consisting predominantly of the sheath. Here, we show that in O. longistaminata, high expression of BOPs caused by miR156 was responsible for suppression of the blade in rhizomes and that bop loss-of-function mutants produced leaves consisting of the leaf blade only. Rhizome growth in soil was also hampered in the mutants due to a severe reduction in rhizome tip stiffness. Leaf blade formation is also suppressed in the stolons of Zoysia matrella, a monocot species, and in the rhizomes of Houttuynia cordata, a dicot species, indicating that leaf blade suppression is widely conserved. We also show that strong expression of BOP homologs in both rhizome and stolon leaves rather than in aerial leaves is another conserved feature. We propose that suppression of the leaf blade by BOP is an evolutionary strategy that has been commonly recruited by both rhizomatous and stoloniferous species to establish their unique growth habit.

Sensory systems need to reliably extract information from highly variable natural signals. Flies, for instance, use optic flow to guide their course and are remarkably adept at estimating image velocity regardless of image statistics. Current circuit models, however, cannot account for this robustness. Here, we demonstrate that the Drosophila visual system reduces input variability by rapidly adjusting its sensitivity to local contrast conditions. We exhaustively map functional properties of neurons in the motion detection circuit and find that local responses are compressed by surround contrast. The compressive signal is fast, integrates spatially, and derives from neural feedback. Training convolutional neural networks on estimating the velocity of natural stimuli shows that this dynamic signal compression can close the performance gap between model and organism. Overall, our work represents a comprehensive mechanistic account of how neural systems attain the robustness to carry out survival-critical tasks in challenging real-world environments.

In visual systems, neurons adapt both to the mean light level and to the range of light levels, or the contrast. Contrast adaptation has been studied extensively, but it remains unclear how it is distributed among neurons in connected circuits, and how early adaptation affects subsequent computations. Here, we investigated temporal contrast adaptation in neurons across Drosophila’s visual motion circuitry. Several ON-pathway neurons showed strong adaptation to changes in contrast over time. One of these neurons, Mi1, showed almost complete adaptation on fast timescales, and experiments ruled out several potential mechanisms for its adaptive properties. When contrast adaptation reduced the gain in ON-pathway cells, it was accompanied by decreased motion responses in downstream direction-selective cells. Simulations show that contrast adaptation can substantially improve motion estimates in natural scenes. The benefits are larger for ON-pathway adaptation, which helps explain the heterogeneous distribution of contrast adaptation in these circuits.

Cellular innovation is central to biological diversification, yet its underlying mechanisms remain poorly understood [1]. One potential source of new cellular traits is environmentally induced phenotypic variation, or phenotypic plasticity. The plasticity-first hypothesis [2, 3, 4] proposes that natural selection can improve upon an ancestrally plastic phenotype to produce a locally adaptive trait, but the role of plasticity for adaptive evolution is still unclear [5, 6, 7, 8, 9, 10]. Here, we show that a structurally novel form of the heterocyst, the specialized nitrogen-fixing cell of the multicellular cyanobacterium Fischerella thermalis, has evolved multiple times from ancestrally plastic developmental variation during adaptation to high temperature. Heterocyst glycolipids (HGs) provide an extracellular gas diffusion barrier that protects oxygen-sensitive nitrogenase [11, 12], and cyanobacteria typically exhibit temperature-induced plasticity in HG composition that modulates heterocyst permeability [13, 14]. By contrast, high-temperature specialists of F. thermalis constitutively overproduce glycolipid isomers associated with high temperature to levels unattained by plastic strains. This results in a less-permeable heterocyst, which is advantageous at high temperature but deleterious at low temperature for both nitrogen fixation activity and fitness. Our study illustrates how the origin of a novel cellular phenotype by the genetic assimilation and adaptive refinement of a plastic trait can be a source of biological diversity and contribute to ecological specialization.

Neuronal axons terminate as synaptic boutons that form stable yet plastic connections with their targets. Synaptic bouton development relies on an underlying network of both long-lived and dynamic microtubules that provide structural stability for the boutons while also allowing for their growth and remodeling. However, a molecular-scale mechanism that explains how neurons appropriately balance these two microtubule populations remains a mystery. We hypothesized that α-tubulin acetyltransferase (αTAT), which both stabilizes long-lived microtubules against mechanical stress via acetylation and has been implicated in promoting microtubule dynamics, could play a role in this process. Using the Drosophila neuromuscular junction as a model, we found that non-enzymatic dαTAT activity limits the growth of synaptic boutons by affecting dynamic, but not stable, microtubules. Loss of dαTAT results in the formation of ectopic boutons. These ectopic boutons can be similarly suppressed by resupplying enzyme-inactive dαTAT or by treatment with a low concentration of the microtubule-targeting agent vinblastine, which acts to suppress microtubule dynamics. Biophysical reconstitution experiments revealed that non-enzymatic αTAT1 activity destabilizes dynamic microtubules but does not substantially impact the stability of long-lived microtubules. Further, during microtubule growth, non-enzymatic αTAT1 activity results in increasingly extended tip structures, consistent with an increased rate of acceleration of catastrophe frequency with microtubule age, perhaps via tip structure remodeling. Through these mechanisms, αTAT enriches for stable microtubules at the expense of dynamic ones. We propose that the specific suppression of dynamic microtubules by non-enzymatic αTAT activity regulates the remodeling of microtubule networks during synaptic bouton development.

Helping others to obtain benefits, even at a cost to oneself, poses an evolutionary puzzle [1]. While kin selection explains such “selfless” acts among relatives, only reciprocity (paying back received favors) entails fitness benefits for unrelated individuals [2]. So far, experimental evidence for both prosocial helping (providing voluntary assistance for achieving an action-based goal) and reciprocity has been reported in a few mammals but no avian species [3]. In order to gain insights into the evolutionary origins of these behaviors, the capacity of non-mammalian species for prosociality and for reciprocity needs to be investigated. We tested two parrot species in an instrumental-helping paradigm involving “token transfer.” Here, actors could provide tokens to their neighbor, who could exchange them with an experimenter for food. To verify whether the parrots understood the task’s contingencies, we systematically varied the presence of a partner and the possibility for exchange. We found that African grey parrots voluntarily and spontaneously transferred tokens to conspecific partners, whereas significantly fewer transfers occurred in the control conditions. Transfers were affected by the strength of the dyads’ affiliation and partially by the receivers’ attention-getting behaviors. Furthermore, the birds reciprocated the help once the roles were reversed. Blue-headed macaws, in contrast, transferred hardly any tokens. Species differences in social tolerance might explain this discrepancy. These findings show that instrumental helping based on a prosocial attitude, accompanied but potentially not sustained by reciprocity, is present in parrots, suggesting that this capacity evolved convergently in this avian group and mammals.

Human activities are shaping the biosphere pervasively, which has led to the concept of the Anthropocene. Although we are already causing a mass extinction, life on Earth is likely to survive for more than a billion years after our species has disappeared. Michael Gross reports.

Animals must distinguish external stimuli from self-generated sensory input to guide appropriate behaviors. A recent study elucidates a cellular mechanism by which zebrafish perform this distinction while maintaining sensitivity to external environmental signals.

Finding the right lure for trapping pest insects is difficult. The typical smell of rain and humid soil, geosmin, now turns out to be a strong attractant for the yellow fever mosquito Aedes aegypti.

Plant-eating dinosaurs evolved varied feeding strategies. A new study demonstrates convergent evolution of their skulls and teeth towards two distinct functional optima, one resembling advanced mammalian herbivory and the other echoing herbivory in birds and other reptiles.

New data are causing the standard model for the effect of selection on linked neutral variation in low recombination regions, combining the effects of background selection and selective sweeps, to be refined to include harmful recessive mutations creating associative overdominance.

Every day and night, the retina undergoes dramatic changes in its physiology and function. The prevailing view is that these daily changes affect the retinal output and thereby visual perception. Recent evidence suggests that modifications in higher-order processing centers, and not in retinal computations, account for variations in visual sensitivity.

How do perennial plants adapt their growth to seasonal changes? A new study in the hybrid aspen reveals that, in short days, repression of a growth-promoting genetic pathway leads to upregulation of the BRANCHED1 genes, which in turn induce growth cessation.

The forces driving membrane protrusion during phagocytosis are poorly understood. A recent study describes how integrins in the phagocyte membrane provide a molecular clutch to enable the exertion of force by actin polymerizing at the leading edge of the pseudopods. These results explain the mechanosensitivity of phagocytic cells.

Two recent studies show that zebrafish larvae alternate between two behavioral modes: exploration and hunting. Both behaviors are structured on multiple time scales, and require the integration of internal and external cues to generate sequences of stereotyped swimming movements.

Vector-borne viral diseases pose an urgent public health challenge, particularly in the tropics. Field releases of mosquitoes carrying bacterial symbionts that reduce vector competence are ongoing in Kuala Lumpur, Malaysia. Early results show that wAlbB Wolbachia can persist in mosquitoes in urban settings and decrease dengue incidence in humans.

Reconstructing prehistoric animal communities is important for understanding the emergence of modern ecosystems and the environmental context of human evolution. A new study of African fossils spanning seven million years shows that ancient large-herbivore assemblages were functionally distinct from those that exist today.

Classically, specific orbitofrontal cortex (OFC) neurons are thought to represent attributes of specific decision options. A new model proposes instead that OFC neurons represent whichever option is currently attended. A recent study, however, tests these two models and rules out the ‘current-focus-of-attention’ model.

For many decades, sleep researchers have sought to determine which species ‘have’ rapid eye movement (REM) sleep. In doing so, they relied predominantly on a template derived from the expression of REM sleep in the adults of a small number of mammalian species. Here, we argue for a different approach that focuses less on a binary decision about haves and have nots, and more on the diverse expression of REM sleep components over development and across species. By focusing on the components of REM sleep and discouraging continued reliance on a restricted template, we aim to promote a richer and more biologically grounded developmental–comparative approach that spans behavioral, physiological, neural, and ecological domains.

Almost all animals can sense light, but only those with spatial vision can “see.” Conventionally, this was restricted to animals possessing discrete visual organs (eyes), but extraocular vision could facilitate vision without eyes. Echinoderms form the focus of extraocular vision research [1, 2, 3, 4, 5, 6, 7], and the brittle star Ophiocoma wendtii, which exhibits light-responsive color change and shelter seeking, became a key species of interest [4, 8, 9]. Both O. wendtii and an apparently light-indifferent congeneric, O. pumila, possess an extensive network of r-opsin-reactive cells, but its function remains unclear [4]. We show that, although both species are strongly light averse, O. wendtii orients to stimuli necessitating spatial vision for detection, but O. pumila does not. However, O. wendtii’s response disappears when chromatophores are contracted within the skeleton. Combining immunohistochemistry, histology, and synchrotron microtomography, we reconstructed models of photoreceptors in situ and extracted estimated angular apertures for O. wendtii and O. pumila. Angular sensitivity estimates, derived from these models, support the hypothesis that chromatophores constitute a screening mechanism in O. wendtii, providing sufficient resolving power to detect the stimuli. RNA sequencing (RNA-seq) identified opsin candidates in both species, including multiple r-opsins and transduction pathway constituents, congruent with immunohistochemistry and studies of other echinoderms [10, 11]. Finally, we note that differing body postures between the two species during experiments may reflect aspect of signal integration. This represents one of the most detailed mechanisms for extraocular vision yet proposed and draws interesting parallels with the only other confirmed extraocular visual system, that of some sea urchins, which also possess chromatophores [1].

Both biological and artificial fliers must contend with aerial perturbations that are ubiquitous in the outdoor environment. Flapping fliers are generally least stable but also most maneuverable around the roll axis, yet our knowledge of roll control in biological fliers remains limited. Hummingbirds are suitable models for linking aerodynamic perturbations to flight control strategies, as these small, powerful fliers are capable of remaining airborne even in adverse wind conditions. We challenged hummingbirds to fly within a steady, longitudinally (streamwise) oriented vortex that imposed a continuous roll perturbation, measured wing kinematics and neuromotor activation of the flight muscles with synchronized high-speed video and electromyography and used computational fluid dynamics (CFD) to estimate the aerodynamic forces generated by observed wing motions. Hummingbirds responded to the perturbation with bilateral differences in activation of the main flight muscles while maintaining symmetry in most major aspects of wing motion, including stroke amplitude, stroke plane angle, and flapping frequency. Hummingbirds did display consistent bilateral differences in subtler wing kinematic traits, including wing rotation and elevation. CFD modeling revealed that asymmetric wing rotation was critical for attenuating the effects of the perturbation. The birds also augmented flight stabilization by adjusting body and tail posture to expose greater surface area to upwash than to the undesirable downwash. Our results provide insight into the remarkable capacity of hummingbirds to maintain flight control, as well as bio-inspiration for simple yet effective control strategies that could allow robotic fliers to contend with unfamiliar and challenging real-world aerial conditions.

Supergenes, clusters of tightly linked genes, play a key role in the evolution of complex adaptive variation [1, 2]. Although supergenes have been identified in many species, we lack an understanding of their origin, evolution, and persistence [3]. Here, we uncover 20–40 Ma of evolutionary history of a supergene associated with polymorphic social organization in Formica ants [4]. We show that five Formica species exhibit homologous divergent haplotypes spanning 11 Mbp on chromosome 3. Despite the supergene’s size, only 142 single nucleotide polymorphisms (SNPs) consistently distinguish alternative supergene haplotypes across all five species. These conserved trans-species SNPs are localized in a small number of disjunct clusters distributed across the supergene. This unexpected pattern of divergence indicates that the Formica supergene does not follow standard models of sex chromosome evolution, in which distinct evolutionary strata reflect an expanding region of suppressed recombination [5]. We propose an alternative “eroded strata model” in which clusters of conserved trans-species SNPs represent functionally important areas maintained by selection in the face of rare recombination between ancestral haplotypes. The comparison of whole-genome sequences across 10 additional Formica species reveals that the most conserved region of the supergene contains a transcription factor essential for motor neuron development in Drosophila [6]. The discovery that a very small portion of this large and ancient supergene harbors conserved trans-species SNPs linked to colony social organization suggests that the ancestral haplotypes have been eroded by recombination, with selection preserving differentiation at one or a few genes generating alternative social organization.

Legumes have the capacity to develop root nodules hosting nitrogen-fixing bacteria, called rhizobia. For the plant, the benefit of the symbiosis is important in nitrogen-deprived conditions, but it requires hosting and feeding massive numbers of rhizobia. Recent studies suggest that innate immunity is reduced or suppressed within nodules [1, 2, 3, 4, 5, 6, 7, 8, 9, 10]; this likely maintains viable rhizobial populations. To evaluate the potential consequences and risks associated with an altered immuni`ty in the symbiotic organ, we developed a tripartite system with the model legume Medicago truncatula [11, 12], its nodulating symbiont of the genus Sinorhizobium (syn. Ensifer) [13, 14], and the pathogenic soil-borne bacterium Ralstonia solanacearum [15, 16, 17, 18]. We show that nodules are frequent infection sites where pathogen multiplication is comparable to that in the root tips and independent of nodule ability to fix nitrogen. Transcriptomic analyses indicate that, despite the presence of the hosted rhizobia, nodules are able to develop weak defense reactions against pathogenic R. solanacearum. Nodule defense response displays specificity compared to that activated in roots. In agreement with nodule innate immunity, optimal R. solanacearum growth requires pathogen virulence factors. Finally, our data indicate that the high susceptibility of nodules is counterbalanced by the existence of a diffusion barrier preventing pathogen spreading from nodules to the rest of the plant.

Climate change is known to affect regional weather patterns and phenology; however, we lack understanding of how climate drives phenological change across local spatial gradients. This spatial variation is critical for determining whether subpopulations and metacommunities are changing in unison or diverging in phenology. Divergent responses could reduce synchrony both within species (disrupting gene flow among subpopulations) and among species (disrupting interspecific interactions in communities). We also lack understanding of phenological change in environments where life history events are frequently aseasonal, such as the tropical, arid, and semi-arid ecosystems that cover vast areas. Using a 33-year-long dataset spanning a 1,267-m semi-arid elevational gradient in the southwestern United States, we test whether flowering phenology diverged among subpopulations within species and among five communities comprising 590 species. Applying circular statistics to test for changes in year-round flowering, we show flowering has become earlier for all communities except at the highest elevations. However, flowering times shifted at different rates across elevations likely because of elevation-specific changes in temperature and precipitation, indicating diverging phenologies of neighboring communities. Subpopulations of individual species also diverged at mid-elevation but converged in phenology at high elevation. These changes in flowering phenology among communities and subpopulations are undetectable when data are pooled across the gradient. Furthermore, we show that nonlinear changes in flowering times over the 33-year record are obscured by traditional calculations of long-term trends. These findings reveal greater spatiotemporal complexity in phenological responses than previously recognized and indicate climate is driving phenological reshuffling across local spatial gradients.

Through the merger of previously independent lineages, symbiosis promotes the acquisition of new traits and exploitation of inaccessible ecological niches [1, 2], driving evolutionary innovation and important ecosystem functions [3, 4, 5, 6]. The transient nature of establishment makes study of symbiotic origins difficult, but experimental comparison of independent origins could reveal the degree of convergence in the underpinning mechanisms [7, 8]. We compared the metabolic mechanisms of two independent origins of Paramecium bursaria-Chlorella photosymbiosis [9, 10, 11] using a reciprocal metabolomic pulse-chase method. This showed convergent patterns of nutrient exchange and utilization for host-derived nitrogen in the Chlorella genotypes [12, 13] and symbiont-derived carbon in the P. bursaria genotypes [14, 15]. Consistent with a convergent primary nutrient exchange, partner-switched host-symbiont pairings were functional. Direct competition of hosts containing native or recombined symbionts against isogenic symbiont-free hosts showed that the fitness benefits of symbiosis for hosts increased with irradiance but varied by genotype. Global metabolism varied more between the Chlorella than the P. bursaria genotypes and suggested divergent mechanisms of light management. Specifically, the algal symbiont genotypes either produced photo-protective carotenoid pigments at high irradiance or more chlorophyll, resulting in corresponding differences in photosynthetic efficiency and non-photochemical quenching among host-symbiont pairings. These data suggest that the multiple origins of P. bursaria-Chlorella symbiosis use a convergent nutrient exchange, whereas other photosynthetic traits linked to functioning of photosymbiosis have diverged. Although convergence enables partner switching among diverse strains, phenotypic mismatches resulting from divergence of secondary symbiotic traits could mediate host-symbiont specificity in nature.

In the early phase of courtship, female fruit flies exhibit an acute rejection response to avoid unfavorable mating. This pre-mating rejection response is evolutionarily paralleled across species, but the molecular and neuronal basis of that behavior is unclear. Here, we show that a putative incoherent feedforward circuit comprising ellipsoid body neurons, cholinergic R4d, and its repressor GABAergic R2/R4m neurons regulates the pre-mating rejection response in the virgin female Drosophila melanogaster. Both R4d and R2/R4m are positively regulated, via specific dopamine receptors, by a subset of neurons in the dopaminergic PPM3 cluster. Genetic deprivation of GABAergic signal via GABAA receptor RNA interference in this circuit induces a massive rejection response, whereas activation of GABAergic R2/R4m or suppression of cholinergic R4d increases receptivity. Moreover, glutamatergic signaling via N-methyl-d-aspartate receptors induces NO-mediated retrograde regulation potentially from R4d to R2/R4m, likely providing flexible control of the behavioral switching from rejection to acceptance. Our study elucidates the molecular and neural mechanisms regulating the behavioral selection process of the pre-mating female.

The hippocampus and surrounding medial-temporal-lobe (MTL) structures are critical for both memory and spatial navigation, but we do not fully understand the neuronal representations used to support these behaviors. Much research has examined how the MTL neurally represents spatial information, such as with “place cells” that represent an animal’s current location or “head-direction cells” that code for an animal’s current heading. In addition to behaviors that require an animal to attend to the current spatial location, navigating to remote destinations is a common part of daily life. To examine the neural basis of these behaviors, we recorded single-neuron activity from neurosurgical patients playing Treasure Hunt, a virtual-reality spatial-memory task. By analyzing how the activity of these neurons related to behavior in Treasure Hunt, we found that the firing rates of many MTL neurons during navigation significantly changed depending on the position of the current spatial target. In addition, we observed neurons whose firing rates during navigation were tuned to specific heading directions in the environment, and others whose activity changed depending on the timing within the trial. By showing that neurons in our task represent remote locations rather than the subject’s own position, our results suggest that the human MTL can represent remote spatial information according to task demands.

Gene flow is an enigmatic evolutionary force because it can limit adaptation but may also rescue small populations from inbreeding depression [1, 2, 3]. Several iconic examples of genetic rescue—increased population growth caused by gene flow [4, 5]—have reversed population declines [6, 7]. However, concerns about outbreeding depression and maladaptive gene flow limit the use of human-mediated gene flow in conservation [8, 9]. Rescue effects of immigration through demographic and/or genetic mechanisms have received theoretical and empirical support, but studies that monitor initial and long-term effects of gene flow on individuals and populations in the wild are lacking. Here, we used individual-based mark-recapture, multigenerational pedigrees, and genomics to test the demographic and evolutionary consequences of manipulating gene flow in two isolated, wild Trinidadian guppy populations. Recipient and source populations originated from environments with different predation, flow, and resource regimes [10]. We documented 10-fold increases in population size following gene flow and found that, on average, hybrids lived longer and reproduced more than residents and immigrants. Despite overall genomic homogenization, alleles potentially associated with local adaptation were not entirely swamped by gene flow. Our results suggest that genetic rescue was caused not just by increasing individual genetic diversity, rather new genomic variation from immigrants combined with alleles from the recipient population resulted in highly fit hybrids and subsequent increases in population size. Contrary to the classic view of maladaptive gene flow, our study reveals conditions under which immigration can produce long-term fitness benefits in small populations without entirely swamping adaptive variation.

Outer retinal degenerative diseases, such as retinitis pigmentosa (RP) and age-related macular degeneration (AMD), are among the leading causes of incurable blindness in the Western world [1]. Retinal prostheses have been shown to restore some useful vision by electrically stimulating the remaining retinal neurons [2]. In contrast to inherited retinal degenerative diseases (e.g., RP), typically leading to a complete loss of the visual field, in AMD patients the disease is localized to the macula, leaving the peripheral vision intact. Implanting a retinal prosthesis in the central macula in AMD patients [3, 4] leads to an intriguing situation where the patient’s central retina is stimulated electrically, whereas the peripheral healthy retina responds to natural light stimulation. An important question is whether the visual cortex responds to these two concurrent stimuli similarly to the interaction between two adjacent natural light stimuli projected onto healthy retina. Here, we investigated the cortical interactions between prosthetic and natural vision based on visually evoked potentials (VEPs) recorded in rats implanted with photovoltaic subretinal implants. Using this model, where prosthetic and natural vision information are combined in the visual cortex, we observed striking similarities in the interactions of natural and prosthetic vision, including similar effect of background illumination, linear summation of non-patterned stimuli, and lateral inhibition with spatial patterns [5], which increased with target contrast. These results support the idea of combined prosthetic and natural vision in restoration of sight for AMD patients.

Linked selection is a major driver of genetic diversity. Selection against deleterious mutations removes linked neutral diversity (background selection [BGS]) [1], creating a positive correlation between recombination rates and genetic diversity. Purifying selection against recessive variants, however, can also lead to associative overdominance (AOD) [2, 3], due to an apparent heterozygote advantage at linked neutral loci that opposes the loss of neutral diversity by BGS. Zhao and Charlesworth [3] identified the conditions under which AOD should dominate over BGS in a single-locus model and suggested that the effect of AOD could become stronger if multiple linked deleterious variants co-segregate. We present a model describing how and under which conditions multi-locus dynamics can amplify the effects of AOD. We derive the conditions for a transition from BGS to AOD due to pseudo-overdominance [4], i.e., a form of balancing selection that maintains complementary deleterious haplotypes that mask the effect of recessive deleterious mutations. Simulations confirm these findings and show that multi-locus AOD can increase diversity in low-recombination regions much more strongly than previously appreciated. While BGS is known to drive genome-wide diversity in humans [5], the observation of a resurgence of genetic diversity in regions of very low recombination is indicative of AOD. We identify 22 such regions in the human genome consistent with multi-locus AOD. Our results demonstrate that AOD may play an important role in the evolution of low-recombination regions of many species.

Nervous systems have evolved to combine environmental information with internal state to select and generate adaptive behavioral sequences. To better understand these computations and their implementation in neural circuits, natural behavior must be carefully measured and quantified. Here, we collect high spatial resolution video of single zebrafish larvae swimming in a naturalistic environment and develop models of their action selection across exploration and hunting. Zebrafish larvae swim in punctuated bouts separated by longer periods of rest called interbout intervals. We take advantage of this structure by categorizing bouts into discrete types and representing their behavior as labeled sequences of bout types emitted over time. We then construct probabilistic models—specifically, marked renewal processes—to evaluate how bout types and interbout intervals are selected by the fish as a function of its internal hunger state, behavioral history, and the locations and properties of nearby prey. Finally, we evaluate the models by their predictive likelihood and their ability to generate realistic trajectories of virtual fish swimming through simulated environments. Our simulations capture multiple timescales of structure in larval zebrafish behavior and expose many ways in which hunger state influences their action selection to promote food seeking during hunger and safety during satiety.

The amount of DNA sequence variability in a genomic region is often positively correlated with its rate of crossing over (CO) [1, 2, 3]. This pattern is caused by selection acting on linked sites, which reduces genetic variability and biases the frequency distribution of segregating variants toward more rare variants than are expected without selection (skew). These effects may involve the spread of beneficial mutations (selective sweeps [SSWs]), the elimination of deleterious mutations (background selection [BGS]), or both, and are expected to be stronger with lower CO rates [1, 2, 3]. However, in a recent study of human populations, the skew was reduced in the lowest CO regions compared with regions with somewhat higher CO rates [4]. A low skew in very low CO regions, compared with theoretical predictions, is seen in the population genomic studies of Drosophila simulans described here and in other Drosophila species. Here, we propose an explanation for lower than expected skew in low CO regions, and validate it using computer simulations; explanations for higher skew with higher CO rates, as in D. simulans, will be explored elsewhere. Partially recessive, linked deleterious mutations can increase neutral variability when the product of the effective population size (Ne) and the selection coefficient against homozygous carriers of mutations (s) is ≤1, i.e., there is associative overdominance (AOD) rather than BGS [5]. AOD can operate in low CO regions, producing a lower skew than in its absence. This opens up a new perspective on how selection affects patterns of variability at linked sites.

The origin of trees and forests in the Mid Devonian (393–383 Ma) was a turning point in Earth history, marking permanent changes to terrestrial ecology, geochemical cycles, atmospheric CO2 levels, and climate. However, how all these factors interrelate remains largely unknown. From a fossil soil (palaeosol) in the Catskill region near Cairo NY, USA, we report evidence of the oldest forest (mid Givetian) yet identified worldwide. Similar to the famous site at Gilboa, NY, we find treefern-like Eospermatopteris (Cladoxylopsida). However, the environment at Cairo appears to have been periodically drier. Along with a single enigmatic root system potentially belonging to a very early rhizomorphic lycopsid, we see spectacularly extensive root systems here assigned to the lignophyte group containing the genus Archaeopteris. This group appears pivotal to the subsequent evolutionary history of forests due to possession of multiple advanced features and likely relationship to subsequently dominant seed plants. Here we show that Archaeopteris had a highly advanced root system essentially comparable to modern seed plants. This suggests a unique ecological role for the group involving greatly expanded energy and resource utilization, with consequent influence on global processes much greater than expected from tree size or rooting depth alone.