Comment on Nature. 2022 Mar;603(7900):302-308.

Comment on Curr Biol. 2022 Jun 6;32(11):2539-2547.e5.

Comment on Curr Biol. 2022 Jun 6;32(11):2375-2389.e6.

Little is known about the spatiotemporal dynamics of gray wolves in the Pleistocene across low-latitude regions of Eurasia. In Japan, a small-bodied endemic subspecies of Japanese wolves existed and went extinct in the early 1900s. The fossil record indicates that a giant wolf, which reached 70 cm in body height, inhabited Japan during the Pleistocene, but its evolutionary relationship, if any, with the Japanese wolf remains uncertain. Here, to reveal the genetic origin of the Japanese wolf, we analyzed ancient DNA from remains (recovered in Japan) of one Pleistocene wolf that lived 35,000 years ago and one Holocene wolf from 5,000 years ago. The analysis of the mitochondrial DNA revealed that the Pleistocene wolf was not part of the Japanese wolf clade but rather an earlier-diverging lineage. The analysis of the nuclear DNA of the Holocene Japanese wolf revealed that it was an admixture of the Japanese Pleistocene wolf and continental wolf lineages. These findings suggest that the Japanese wolf originated via waves of colonization of multiple Pleistocene wolf populations at 57-35 and 37-14 ka, respectively, followed by interpopulation hybridization.

Comment in Curr Biol. 2022 Jun 20;32(12):R559-R561.

Comment in Curr Biol. 2022 Jun 6;32(11):R523-R525.

Comment on Curr Biol. 2022 Apr 11;32(7):1623-1628.e3.

Comment on Curr Biol. 2022 Jun 6;32(11):2556-2562.e2.

Yuri Shibata and David Komander discuss the composition, regulation and functions of the linear ubiquitin chain assembly complex (LUBAC).

Greco et al. describe their experience learning to be more effective and humane PIs. The key to their growth was regular and consistent work with a diverse group of their peers aided by the guidance of an organizational psychologist.

During mitosis and meiosis in the majority of eukaryotes, centromeric chromatin comprised of CENP-A nucleosomes and their reader CENP-C recruits components of the outer kinetochore to build an interface with spindle microtubules.1,2 One exception is C. elegans oocyte meiosis, where outer kinetochore proteins form cup-like structures on chromosomes independently of centromeric chromatin.3 Here, we show that the nucleoporin MEL-28 (ortholog of human ELYS) and CENP-CHCP-4 act in parallel to recruit outer kinetochore components to oocyte meiotic chromosomes. Unexpectedly, co-inhibition of MEL-28 and CENP-CHCP-4 resulted in chromosomes being expelled from the meiotic spindle prior to anaphase onset, a more severe phenotype than what was observed following ablation of the outer kinetochore.4,5 This observation suggested that MEL-28 and the outer kinetochore independently link chromosomes to spindle microtubules. Consistent with this, the chromosome expulsion defect was observed following co-inhibition of MEL-28 and the microtubule-coupling KNL-1/MIS-12/NDC-80 (KMN) network of the outer kinetochore. Use of engineered mutants showed that MEL-28 acts in conjunction with the microtubule-binding NDC-80 complex to keep chromosomes within the oocyte meiotic spindle and that this function likely involves the Y-complex of nucleoporins that associate with MEL-28; by contrast, the ability to dock protein phosphatase 1, shared by MEL-28 and KNL-1, is not involved. These results highlight nuclear pore-independent functions for a conserved nucleoporin and explain two unusual features of oocyte meiotic chromosome segregation in C. elegans: centromeric chromatin-independent outer kinetochore assembly, and dispensability of the outer kinetochore for constraining chromosomes in the acentrosomal meiotic spindle.

Shapes of vegetables and fruits are the result of adaptive evolution and human selection. Modules controlling organ shape have been identified. However, little is known about signals coordinating organ development and shape. Here, we describe the characterization of a melon mutation rf1, leading to round fruit. Histological analysis of rf1 flower and fruits revealed fruit shape is determined at flower stage 8, after sex determination and before flower fertilization. Using positional cloning, we identified the causal gene as the monoecy sex determination gene CmACS7, and survey of melon germplasms showed strong association between fruit shape and sexual types. We show that CmACS7-mediated ethylene production in carpel primordia enhances cell expansion and represses cell division, leading to elongated fruit. Cell size is known to rise as a result of endoreduplication. At stage 8 and anthesis, we found no variation in ploidy levels between female and hermaphrodite flowers, ruling out endoreduplication as a factor in fruit shape determination. To pinpoint the gene networks controlling elongated versus round fruit phenotype, we analyzed the transcriptomes of laser capture microdissected carpels of wild-type and rf1 mutant. These high-resolution spatiotemporal gene expression dynamics revealed the implication of two regulatory modules. The first module implicates E2F-DP transcription factors, controlling cell elongation versus cell division. The second module implicates OVATE- and TRM5-related proteins, controlling cell division patterns. Our finding highlights the dual role of ethylene in the inhibition of the stamina development and the elongation of ovary and fruit in cucurbits.

From swimming to walking and flying, animals have evolved specific locomotor strategies to thrive in different habitats. All types of locomotion depend on the integration of motor commands and sensory information to generate precisely coordinated movements. Cerebrospinal-fluid-contacting neurons (CSF-cN) constitute a vertebrate sensory system that monitors CSF composition and flow. In fish, CSF-cN modulate swimming activity in response to changes in pH and bending of the spinal cord; however, their role in mammals remains unknown. We used mouse genetics to study their function in quadrupedal locomotion. We found that CSF-cN are directly integrated into spinal motor circuits. The perturbation of CSF-cN function does not affect general motor activity nor the generation of locomotor rhythm and pattern but results in specific defects in skilled movements. These results identify a role for mouse CSF-cN in adaptive motor control and indicate that this sensory system evolved a novel function to accommodate the biomechanical requirements of limb-based locomotion.

Comment in Curr Biol. 2022 Jun 20;32(12):R564-R566.

Recent studies have shown that stimulus history can be decoded via the use of broadband sensory impulses to reactivate mnemonic representations.1-4. However, memories of previous stimuli can also be used to form sensory predictions about upcoming stimuli.5,6 Predictive mechanisms allow the brain to create a probable model of the outside world, which can be updated when errors are detected between the model predictions and external inputs. 7-10 Direct recordings in the auditory cortex of awake mice established neural mechanisms for how encoding mechanisms might handle working memory and predictive processes without "overwriting" recent sensory events in instances where predictive mechanisms are triggered by oddballs within a sequence.11 However, it remains unclear whether mnemonic and predictive information can be decoded from cortical activity simultaneously during passive, implicit sequence processing, even in anesthetized models. Here, we recorded neural activity elicited by repeated stimulus sequences using electrocorticography (ECoG) in the auditory cortex of anesthetized rats, where events within the sequence (referred to henceforth as "vowels," for simplicity) were occasionally replaced with a broadband noise burst or omitted entirely. We show that both stimulus history and predicted stimuli can be decoded from neural responses to broadband impulses, at overlapping latencies but based on independent and uncorrelated data features. We also demonstrate that predictive representations are dynamically updated over the course of stimulation.

Comment in Curr Biol. 2022 Jun 6;32(11):R525-R528.

Comment on Curr Biol. 2022 Jun 6;32(11):2517-2528.e6.

Indigenous peoples are important stewards of biodiversity, often living near and possessing intimate knowledge of ecosystems. As a result, species new to science may be long known to indigenous people. While the scientific endeavor has long benefitted from indigenous knowledge, it has usually not engaged with it on equal footing1,2. While Linnaean taxonomy offers a broad framework for global comparisons, it may lack the detailed local insights possessed by indigenous peoples. This study illustrates how meaningful engagement with indigenous knowledge - throughout the scientific process - can improve biodiversity science and promote conservation1,2, particularly in studies of crop wild relatives, an international priority3 for food security in the face of climate change4. Two species of fruit trees recognized as distinct by the Iban and Dusun peoples, but considered a single species in current Linnaean taxonomy, were confirmed as distinct taxa by molecular studies. They correspond to Artocarpus odoratissimus Blanco and Artocarpus mutabilis Becc., whose distinguishing characteristics were clarified by members of indigenous communities.

The detection of motion direction is a fundamental visual function and a classic model for neural computation. In the non-primate retina, direction selectivity arises in starburst amacrine cell (SAC) dendrites, which provide selective inhibition to direction-selective retinal ganglion cells (dsRGCs). Although SACs are present in primates, their connectivity and the existence of dsRGCs remain open questions. Here, we present a connectomic reconstruction of the primate ON SAC circuit from a serial electron microscopy volume of the macaque central retina. We show that the structural basis for the SACs' ability to confer directional selectivity on postsynaptic neurons is conserved. SACs selectively target a candidate homolog to the mammalian ON-sustained dsRGCs that project to the accessory optic system (AOS) and contribute to gaze-stabilizing reflexes. These results indicate that the capacity to compute motion direction is present in the retina, which is earlier in the primate visual system than classically thought.

Visual plasticity declines sharply after the critical period, yet we easily learn to recognize new faces and places, even as adults. Such learning is often characterized by a "moment of insight," an abrupt and dramatic improvement in recognition. The mechanisms that support abrupt learning are unknown, but one hypothesis is that they involve changes in synchronization between brain regions. To test this hypothesis, we used a behavioral task in which non-human primates rapidly learned to recognize novel images and to associate them with specific responses. Simultaneous recordings from inferotemporal and prefrontal cortices revealed a transient synchronization of neural activity between these areas that peaked around the moment of insight. Synchronization was strongest between inferotemporal sites that encoded images and reward-sensitive prefrontal sites. Moreover, its magnitude intensified gradually over image exposures, suggesting that abrupt learning is the culmination of a search for informative signals within a circuit linking sensory information to task demands.

Comment in Curr Biol. 2022 Jun 6;32(11):R515-R517.

Photosynthesis shapes the symbiotic relationships between cnidarians and Symbiodiniaceae algae-with many cnidarian hosts requiring symbiont photosynthate for survival-but little is known about how photosynthesis impacts symbiosis establishment. Here, we show that during symbiosis establishment, infection, proliferation, and maintenance can proceed without photosynthesis, but the ability to do so is dependent on specific cnidarian-Symbiodiniaceae relationships. The evaluation of 31 pairs of symbiotic relationships (five species of Symbiodiniaceae in sea anemone, coral, and jellyfish hosts) revealed that infection can occur without photosynthesis. A UV mutagenesis method for Symbiodiniaceae was established and used to generate six photosynthetic mutants that can infect these hosts. Without photosynthesis, Symbiodiniaceae cannot proliferate in the sea anemone Aiptasia or jellyfish Cassiopea but can proliferate in the juvenile polyps of the coral Acropora. After 6 months of darkness, Breviolum minutum is maintained within Aiptasia, indicating that Symbiodiniaceae maintenance can be independent of photosynthesis. Manipulating photosynthesis provides insights into cnidarian-Symbiodiniaceae symbiosis.

The acquisition of stomata is one of the key innovations that led to the colonisation of the terrestrial environment by the earliest land plants. However, our understanding of the origin, evolution and the ancestral function of stomata is incomplete. Phylogenomic analyses indicate that, firstly, stomata are ancient structures, present in the common ancestor of land plants, prior to the divergence of bryophytes and tracheophytes and, secondly, there has been reductive stomatal evolution, especially in the bryophytes (with complete loss in the liverworts). From a review of the evidence, we conclude that the capacity of stomata to open and close in response to signals such as ABA, CO2 and light (hydroactive movement) is an ancestral state, is present in all lineages and likely predates the divergence of the bryophytes and tracheophytes. We reject the hypothesis that hydroactive movement was acquired with the emergence of the gymnosperms. We also conclude that the role of stomata in the earliest land plants was to optimise carbon gain per unit water loss. There remain many other unanswered questions concerning the evolution and especially the origin of stomata. To address these questions, it will be necessary to: find more fossils representing the earliest land plants, revisit the existing early land plant fossil record in the light of novel phylogenomic hypotheses and carry out more functional studies that include both tracheophytes and bryophytes.

Comment on Cell. 2022 May 26;185(11):1842-1859.e18.

Comment on Curr Biol. 2022 Jun 6;32(11):2505-2516.e8.

Comment on Curr Biol. 2022 Jun 6;32(11):2416-2429.e6.

Comment on Curr Biol. 2022 Jun 6;32(11):2357-2374.e6.

Visual perception in human adults varies throughout the visual field, both across eccentricity - decreasing with distance from the center of gaze - and around isoeccentric locations - that is, with polar angle at a constant distance from the center of gaze. At isoeccentric locations, the same visual information yields better performance along the horizontal than vertical meridian (horizontal-vertical anisotropy, HVA) and along the lower than upper vertical meridian (vertical-meridian asymmetry, VMA). These perceptual polar angle asymmetries in adults have been well characterized. Poor perception at upper visual field locations would be particularly detrimental to children: in their perceptual world, given their height, many important events occur above eye level. Developmental aspects of visual perception have been well characterized1, and some basic dimensions, such as contrast sensitivity, continue to develop through childhood2, but there is no research on polar angle asymmetries before adulthood. Here, we investigated whether these asymmetries are present in children, and if so, whether they differ from those of adults. We found clear differences between children and adults in performance around the visual field: the HVA is less pronounced and the VMA is not present for children.

Interview with Jan Traas, who studies shoot meristem function at the École normale supérieure de Lyon.

Memory consolidation-the transformation of labile memory traces into stable long-term representations-is facilitated by post-learning sleep. Computational and biophysical models suggest that sleep spindles may play a key mechanistic role for consolidation, igniting structural changes at cortical sites involved in prior learning. Here, we tested the resulting prediction that spindles are most pronounced over learning-related cortical areas and that the extent of this learning-spindle overlap predicts behavioral measures of memory consolidation. Using high-density scalp electroencephalography (EEG) and polysomnography (PSG) in healthy volunteers, we first identified cortical areas engaged during a temporospatial associative memory task (power decreases in the alpha/beta frequency range, 6-20 Hz). Critically, we found that participant-specific topographies (i.e., spatial distributions) of post-learning sleep spindle amplitude correlated with participant-specific learning topographies. Importantly, the extent to which spindles tracked learning patterns further predicted memory consolidation across participants. Our results provide empirical evidence for a role of post-learning sleep spindles in tracking learning networks, thereby facilitating memory consolidation.

Among all invertebrates, soft-bodied cephalopods have the largest central nervous systems and the greatest brain-to-body mass ratios, yet unlike other big-brained animals, cephalopods are unusually short lived.1-5 Primates and corvids survive for many decades, but shallow-water octopuses, such as the California two-spot octopus (Octopus bimaculoides), typically live for only 1 year.6,7 Lifespan and reproduction are controlled by the principal neuroendocrine center of the octopus: the optic glands, which are functional analogs to the vertebrate pituitary gland.8-10 After mating, females steadfastly brood their eggs, begin fasting, and undergo rapid physiological decline, featuring repeated self-injury and leading to death.11 Removal of the optic glands completely reverses this life history trajectory,10 but the signaling factors underlying this major life transition are unknown. Here, we characterize the major secretions and steroidogenic pathways of the female optic gland using mass spectrometry techniques. We find that at least three pathways are mobilized to increase synthesis of select sterol hormones after reproduction. One pathway generates pregnane steroids, known in other animals to support reproduction.12-16 Two other pathways produce 7-dehydrocholesterol and bile acid intermediates, neither of which were previously known to be involved in semelparity. Our results provide insight into invertebrate cholesterol pathways and confirm a remarkable unity of steroid hormone biology in life history processes across Bilateria.

Comment in Curr Biol. 2022 Jun 6;32(11):R520-R523.

Comment in Curr Biol. 2022 Jun 6;32(11):R513-R515.

Comment in Curr Biol. 2022 Jun 6;32(11):R530-R532.

Comment in Curr Biol. 2022 Jun 6;32(11):R518-R520.

Forces produced by motor proteins and microtubule dynamics within the mitotic spindle are crucial for proper chromosome segregation. In addition to linear forces, rotational forces or torques are present in the spindle, which are reflected in the left-handed twisted shapes of microtubule bundles that make the spindle chiral. However, the biological role and molecular origins of spindle chirality are unknown. By developing methods for measuring the spindle twist, we show that spindles are most chiral near the metaphase-to-anaphase transition. To assess the role of chirality in spindle mechanics, we compressed the spindles along their axis. This resulted in a stronger left-handed twist, suggesting that the twisted shape allows for a mechanical response to forces. Inhibition or depletion of motor proteins that perform chiral stepping, Eg5/kinesin-5, Kif18A/kinesin-8, MKLP1/kinesin-6, and dynein, decreased the left-handed twist or led to right-handed twist, implying that these motors regulate the twist by rotating microtubules within their antiparallel overlaps or at the spindle pole. A right-handed twist was also observed after the depletion of the microtubule nucleator augmin, indicating its contribution to the twist through the nucleation of antiparallel bridging microtubules. The uncovered switch from left-handed to right-handed twist reveals the existence of competing mechanisms that promote twisting in opposite directions. As round spindles are more twisted than the elongated ones are, we infer that bending and twisting moments are generated by similar molecular mechanisms and propose a physiological role for spindle chirality in allowing the spindle to absorb mechanical load. VIDEO ABSTRACT.

Before visiting your local supermarket, do you write your food shopping list in the order you expect to encounter the items as you walk around, aisle by aisle? This way, you minimise your travel distance, saving time and effort. Many other animals do the same. Baboons (Papio ursinus) plan their foraging journeys to out-of-sight resources, moving in an efficient, goal-directed way, and nectar-collecting bumble bees (Bombus impatiens) use efficient travel routes when foraging on familiar resources.

Emily Shepard introduces ways flying animals conserve energy inflight.

Walking through a garden or a crop field, you may notice that plants damaged by pests (insects or pathogens) look smaller than the same kind of plants nearby that are not damaged. An obvious explanation would be that damaged plants may have lost substantial photosynthetic tissue due to insect and pathogen activities. As such, plants may have a reduced ability to capture light and perform photosynthesis, which fuels the growth of plants. While this is likely part of the reason why damaged plants look smaller, there is also another and perhaps more fascinating explanation that we would like to discuss here in this primer. It turns out that plants attacked by insects, pathogens and other biotic stressors may 'purposely' slow down their growth and that this response is often systemic, meaning that it occurs throughout the plant and beyond the tissue that is damaged by pests. Interestingly, some chemicals or plant genetic mutations that simulate insect or pathogen attacks without causing a loss of photosynthetic tissue can also slow plant growth, suggesting the physical loss of photosynthetic tissue per se is not always a prerequisite for slowing down plant growth. In contrast, there are conditions under which plants need to grow rapidly. For example, plants grow quickly when searching for light during germination or under a shaded canopy due to crowding from neighboring plants. Under these conditions, rapid plant growth is often accompanied by increased susceptibility to pests, presumably because growth is prioritized over defense. This inverse growth-defense relationship is commonly known as the 'growth-defense trade-off' and may be considered one of the most fundamental principles of 'plant economics' that allows plants to adjust growth and defense based on external conditions (Figure 1). As plants must both grow and defend in order to reproduce and survive in the natural world, growth-defense trade-offs have important ecological consequences. In agricultural settings, crops have often been bred to maximize growth-related traits, which could inadvertently result in the loss of useful genetic traits for biotic defenses. Thus, deciphering the molecular mechanisms underlying growth-defense trade-off phenomena could impact future crop breeding strategies aimed at designing superior crop plants with high yields as well as the ability to defend against biotic stressors. Here, we discuss some of the prevailing hypotheses about growth-defense trade-offs, our current understanding of the underlying mechanisms, and the ongoing efforts to optimize growth-defense trade-offs in crop plants.

Energy derived from food is a precious resource to animals. Those finite calories are often well-earned through exhaustive foraging effort, which can dominate waking hours, to support physiological processes (e.g. body maintenance and growth) and ecological necessities (e.g. predator avoidance and courting) that are pertinent to the production of progeny. So, it is unsurprising to find that animals have evolved strategies to guard against the gratuitous waste of hard-won caloric energy. Yet, it remains surprising to find such diversity, and elegant creativity, in those solutions. Brief examples of energy-saving innovation could include the very shape of animals and how they move, from streamlined swimming sharks to skyward-soaring seabirds; or the evolutionary appearance of various states of dormancy, such as endothermic animals sacrificing high body temperature through modest (torpor) or severe (hibernation) curtailments to metabolic heat production. Another reversibly dormant state with energetic benefits is sleep.

Consider how advantageous it might be to have eyes on our hands, rather than on our faces: depth perception would be improved by the greater distance between the eyes, and it would be easy to look into relatively inaccessible spaces by appropriate movement of the hands. The absence of mammals that use this visual strategy draws attention to constraints on how evolution is able to 'design' the nervous system. Energy use in particular, in this case the large amount of energy that would be needed to send visual information along the ∼106 optic nerve axons over the length of the arms to the brain (instead of along the much shorter optic nerve), imposes significant design constraints on the nervous system.

Plants growing in temperate and boreal regions of the world have to face strikingly different environmental conditions during summer and winter. Being sessile organisms, plants have had to develop various strategies to adapt to these changes in light, temperature, and water availability, thereby optimizing their 'economy of growth'. While annual plants can endure unfavorable winter conditions in the form of a seed, or under a protective cover of thick snow, perennial plants such as trees adapt by going into a stage of deep sleep called winter dormancy. To enter dormancy, vegetative growth is stopped in the late summer or early autumn and the shoots are converted into buds, where the shoot apical meristems are protected by tightly closed and hardened bud scales (Figures 1 and 2). At the same time, cold hardiness develops and the need for water and nutrient uptake is drastically reduced. Deciduous trees also go through leaf senescence whereby the leaves develop their autumn colors and are shed (Figure 1A). The trees then spend the beginning of the winter in a state of deep sleep in which they are completely unreceptive to any environmental signals telling them to wake up. However, as winter progresses, the trees are gradually released from this slumber and will eventually flush their buds in the spring. Vegetative growth then resumes with the formation of new leaves and shoots during summer until the trees again go into growth cessation and the cycle is closed (Figures 1 and 2). This cycle of growth and dormancy is central for the ability of trees to adapt to growth at different latitudes and elevations. The further north, or the higher the elevation at which the trees grow, the earlier in the season the trees enter growth cessation and the later they flush their buds in the spring. This is because meteorological winter arrives earlier in the season and lasts longer into the spring. The trees therefore have to stop growth earlier in the season to ensure that they have enough time to complete bud formation and to develop cold hardiness and dormancy. They also have to be sure that winter is really over before flushing their buds. Winter dormancy is therefore a clear case of a trade-off between the length of the growing season and the protection against winter damage - a nice example of 'economy in biology', the theme of this special issue. This primer will briefly summarize what we know about the environmental signals that influence the annual growth cycle in trees, as well as our current understanding of the genetic pathways and molecular mechanisms regulated by these signals.

Parasitism has independently evolved multiple times across the entire tree of life, and there are numerous parasitic representatives from every major eukaryote kingdom. In animals alone, parasitism has independently evolved at least 200 times. If there are any organisms that one might think would have access to limitless resources, it would be parasites. You would think that living in or on the body of their host, which serves as both a habitat and a food source, would provide parasites with bountiful resources to maximise every aspect of their existence, especially reproduction. But parasitism is not a loophole out of life history trade-offs. There is still a finite amount of resources that a parasite can obtain and allocate to its many needs. Living in a resource-rich environment has allowed many parasites to grow to sizes that are of multiple orders of magnitude larger than their free-living relatives. But that does not mean that the underlying economy of nature and its limitations are inapplicable to parasites.

All else being equal, evolution is going to drive animals to require the least food to move a unit distance. What is the best way to do that? Some efficiencies can be 'hard-wired' into the body - the relatively unchanging morphology of the animal. But flexibility is also needed - given the task at hand, state of the body, or state of the external environment, it may be best to dynamically choose an appropriate mode of locomotion. For example, slow walking may be great for searching and foraging, but it won't catch fast moving prey. Similarly, maximum speed gallops may be great for escaping danger, but they preclude eating along the way. This primer summarizes what we know about the determinants of locomotor costs and the strategies animals use to minimize cost. It summarizes key findings across levels of organization, from individual muscles to interactions with other organisms and the environment. At the mid-level of organization we highlight gaits, a particularly interesting topic of inquiry with a rich history. We are in an exciting time for the science of movement because we have more, better tools than ever before for observing and manipulating systems, from the molecular level to herds of animals on the Savannah. Even more importantly, there are so many open, exciting questions to ask.

Plants need at least 13 different nutrients to maintain optimal growth. Nitrogen and phosphorus, from the Greek 'phôs' (meaning 'light') and 'phoros' (meaning 'bearer'), are the main nutrients limiting plant growth in both agricultural and natural ecosystems. Agriculture has relied heavily since the mid 1950s on the use of synthetic ammonium- and phosphorus-based fertilizers to increase crop productivity. While industrial synthesis of ammonium relies on the chemical conversion of atmospheric nitrogen, phosphorus is mined from finite reserves concentrated in a few countries. Considering our current dependence on phosphorus fertilizers for food production and the geopolitical aspects associated with current resources, it will be important to develop technologies enabling the maintenance of high crop yield with reduced fertilizer input. This will require an in-depth knowledge on the various pathways that enable plants to acquire phosphorus from the soil and maximize its economical use for growth and reproduction. In this primer, we give an overview of the factors limiting phosphorus acquisition by plants and highlight various pathways and strategies plants have evolved at the level of development, metabolism and signal transduction to adapt to phosphorus deficiency.

Maintaining nutrient and energy homeostasis is crucial for the survival and function of cells and organisms in response to environmental stress. Cells have evolved a stress-induced catabolic pathway, termed autophagy, to adapt to stress conditions such as starvation. During autophagy, damaged or non-essential cellular structures are broken down in lysosomes, and the resulting metabolites are reused for core biosynthetic processes or energy production. Recent studies have revealed that autophagy can target and degrade different types of nutrient stores and produce a variety of metabolites and fuels, including amino acids, nucleotides, lipids and carbohydrates. Here, we will focus on how autophagy functions to balance cellular nutrient and energy demand and supply - specifically, how energy deprivation switches on autophagic catabolism, how autophagy halts anabolism by degrading the protein synthesis machinery, and how bulk and selective autophagy-derived metabolites recycle and feed into a variety of bioenergetic and anabolic pathways during stress conditions. Recent new insights and progress in these areas provide a better understanding of how resource mobilization and reallocation sustain essential metabolic and anabolic activities under unfavorable conditions.

Economic models predominate in life history research, which investigates the allocation of an organism's resources to growth, reproduction, and maintenance. These approaches typically employ a heuristic Y model of resource allocation, which predicts trade-offs among tasks within a fixed budget. The common currency among tasks is not always specified, but most models imply that metabolic energy, either from food or body stores, is the critical resource. Here, we review the evidence for metabolic energy as the common currency of growth, reproduction, and maintenance, focusing on studies in humans and other vertebrates. We then discuss the flow of energy to competing physiological tasks (physical activity, maintenance, and reproduction or growth) and its effect on life history traits. We propose a Ψ model of energy flow to these tasks, which provides an integrative framework for examining the influence of environmental factors and the expansion and contraction of energy budgets in the evolution of life history strategies.

Movement is an integral part of animal biology. It enables organisms to escape from danger, acquire food, and perform courtship displays. Changing the speed or vertical position of a body requires mechanical energy. This energy is typically provided by the biological motor, striated muscle. Striated muscle uses chemical (metabolic) energy to produce force, to move this force over a distance to do work, and to do this work within some time to generate power. The metabolic energy consumed in producing these mechanical outputs is a major component of an organism's energy budget, particularly during repetitive, cyclical movements. This energy could otherwise be used for maintenance, growth, and reproduction. Hence, fitness may be enhanced by improving locomotor efficiency - the ratio between work done and metabolic energy consumed. This may be achieved by reducing the need for muscle to do work, and by increasing the efficiency with which muscle does work.

Across the animal kingdom, we see remarkable variation in brain size. This variation has even increased over evolutionary time. Traditionally, studies aiming to explain brain size evolution have looked at the fitness benefits of increased brain size in relation to its increased cognitive performance in the social and/or ecological domain. However, brains are among the most energetically expensive tissues in the body and also require an uninterrupted energy supply. If not compensated, these energetic demands inevitably lead to a reduction in energy allocation to other vital functions. In this review, we summarize how an increasing number of studies show that to fully comprehend brain size evolution and the large variation in brain size across lineages, it is important to look at the economics of brains, including the different pathways through which the high energetic costs of brains can be offset. We further show how numerous studies converge on the conclusion that cognitive abilities can only drive brain size evolution in vertebrate lineages where they result in an improved energy balance through favourable ecological preconditions. Cognitive benefits that do not directly improve the organism's energy balance can only be selectively favoured when they produce such large improvements in reproduction or survival that they outweigh the negative energetic effects of the large brain.

Biology and economics are surprisingly similar disciplines. At their core, both fields are the study of competitive interactions for scarce resources and the consequences of those interactions over time. Perhaps the first person to notice this similarity was Charles Darwin, who credited his reading of the influential economist Thomas Robert Malthus with catalysing his understanding of natural selection as the driving force of evolution. While it may not have been recognised at the time, this was not the only area of Darwin's thinking to parallel economic concepts.

Mitochondria are central to cellular metabolism. They provide intermediate metabolites that are used in biosynthetic pathways and they process diet-derived nutrients into the energy-rich compound ATP. Mitochondrial ATP biosynthesis is a marvel of thermodynamic efficiency. Via the tricarboxylic acid cycle (TCA) and fatty acid β-oxidation, mitochondria extract electrons from dietary carbon compounds and pass them to nucleotides that ultimately deliver them to the respiratory chain complexes located in invaginations in the inner mitochondrial membrane (IMM) known as cristae. The respiratory chain complexes donate electrons in stepwise redox reactions to molecular oxygen and, with the exception of complex II, use the liberated energy to pump protons across the proton-impermeable IMM, generating a proton electrochemical gradient. This gradient is then utilized by the ATP synthase, which, in a rotary mechanism, catalyzes the formation of the high-energy γ-phosphate chemical bond between ADP and inorganic phosphate. The conversion of the chemical energy of carbon compounds into a physical, vectorial form of energy (the electrochemical gradient) maximizes the yield of the ATP biosynthetic process and is perhaps one of the foundations of life as we know it.

Cell growth relies upon the ability to produce new proteins, which requires energy and chemical precursors, and an adequate supply of the molecular machines for protein synthesis - ribosomes. Although not widely appreciated, ribosomes are remarkably abundant in all cells. For example, in a rapidly growing yeast cell there are ∼2-4 x 105 ribosomes, produced and exported to the cytoplasm at a rate of ∼2,000-4,000 per minute, with ribosomal proteins making up ∼50% of total cellular protein number and ∼30% of cellular protein mass. Even in a typical human cell ribosomal proteins constitute ∼4-6% of total protein mass, and ribosomes are present at ∼107 per cell. We begin this primer by exploring the tight relationship between ribosome production and cell growth, which has important implications not just for the cell's global protein expression profile and maximum growth rate, but also for the molecular composition of the ribosome itself. We then discuss how and to what extent the expression of the RNA and protein components of ribosomes is fine-tuned to match the cell's needs and minimise waste. Finally, we highlight the importance of coordinated ribosomal RNA (rRNA) and ribosomal protein expression in eukaryotes and explore how defects in this process are associated with proteotoxicity and disease. A central underlying question addressed throughout is whether regulation of ribosome biogenesis has evolved to optimise energy efficiency or is instead (or in addition) driven by other goals, such as maximising cell growth rate, promoting adaptation to changing environmental conditions, or maintaining the stability of the cellular proteome.

Vanderschuren and Agusti introduce plant storage roots.

Comment on Nat Commun. 2022 Mar 18;13(1):1460.

Interview with Asifa Majid, who studies language, culture and cognition at the University of Oxford.

Eukaryotic genomes can acquire bacterial DNA via lateral gene transfer (LGT).1 A prominent source of LGT is Wolbachia,2 a widespread endosymbiont of arthropods and nematodes that is transmitted maternally through female germline cells.3,4 The DNA transfer from the Wolbachia endosymbiont wAna to Drosophila ananassae is extensive5-7 and has been localized to chromosome 4, contributing to chromosome expansion in this lineage.6 As has happened frequently with claims of bacteria-to-eukaryote LGT, the contribution of wAna transfers to the expanded size of D. ananassae chromosome 4 has been specifically contested8 owing to an assembly where Wolbachia sequences were classified as contaminants and removed.9 Here, long-read sequencing with DNA from a Wolbachia-cured line enabled assembly of 4.9 Mbp of nuclear Wolbachia transfers (nuwts) in D. ananassae and a 24-kbp nuclear mitochondrial transfer. The nuwts are <8,000 years old in at least two locations in chromosome 4 with at least one whole-genome integration followed by rapid extensive duplication of most of the genome with regions that have up to 10 copies. The genes in nuwts are accumulating small indels and mobile element insertions. Among the highly duplicated genes are cifA and cifB, two genes associated with Wolbachia-mediated Drosophila cytoplasmic incompatibility. The wAna strain that was the source of nuwts was subsequently replaced by a different wAna endosymbiont. Direct RNA Nanopore sequencing of Wolbachia-cured lines identified nuwt transcripts, including spliced transcripts, but functionality, if any, remains elusive.

The cortical endoplasmic reticulum (cER) is a reticulated network closely attached to the plasma membrane (PM). In the fission yeast Schizosaccharomyces pombe (S. pombe), ER-PM contacts have been suggested to restrict both the allocation and compaction of large-sized actomyosin assemblies along the lateral cell cortex. However, how cells orchestrate ER-PM contact remodeling in accordance with actomyosin coalescence for contractile ring assembly is unclear. Here, we reveal that actomyosin compaction directs the remodeling of the free tubular cER edges, whereas active exocytosis subsequently promotes the reorganization of the eisosome-bound cER rims by weakening their association or repatterning the eisosome-coated PM furrows. cER-eisosome contacts also act to reserve tubular cER edges and, hence, the ER shaping machinery at the lateral cell cortex. By manipulating or rerouting exocytosis in mutants with compromised actomyosin compaction, due to either the loss of myosin II activity or sheet-like cER morphology, we show that exocytosis facilitates ring formation likely by creating free tubular cER rims allowing robust cER remodeling. We thus propose that coordinated cER remodeling driven by both actomyosin forces and active exocytosis ensures proper contractile ring assembly. Our work also provides mechanistic insights into cER-related modulation in actomyosin ring assembly.

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Long-term memory has clear advantages for animals but also has neurological and behavioral costs1-3. Encoding memories is metabolically expensive1. Older memories can interfere with retrieval of more recent memories3, prolong decision-making and reduce cognitive flexibility2,3. Given these opposing selection pressures, understanding how long memories last can shed light on how memory enhances or constrains animals' abilities to exploit their niches. Although testing memory retention in wild animals is difficult, it is important because captive conditions do not reflect the complex cognitive demands of wild environments, and long-term captivity changes the brain4 (Data S1A). Here, we trained wild-caught frog-eating bats (Trachops cirrhosus) to find prey by flying to a novel acoustic cue. After they learned the rewarded sound, we released them back into the wild, and then re-captured some of them one to four years later. When re-tested, all eight 'experienced' bats that previously learned the novel prey sounds flew to those sounds within seconds, whereas 17 naïve bats tested with the same sounds showed weak responses. Experienced bats also showed behavior indicating generalization of memories between novel sounds and rewards over time. The frog-eating bat's remarkably long memory indicates that an ability to remember rarely encountered prey may be advantageous for this predator and suggests hitherto unknown cognitive abilities in bats.

Cancer cell migration during metastasis is mediated by a highly polarized cytoskeleton. MARK2 and its invertebrate homolog Par1B are kinases that regulate the microtubule cytoskeleton to mediate polarization of neurons in mammals and embryos in invertebrates. However, the role of MARK2 in cancer cell migration is unclear. Using osteosarcoma cells, we found that in addition to its known localizations on microtubules and the plasma membrane, MARK2 also associates with the actomyosin cytoskeleton and focal adhesions. Cells depleted of MARK proteins demonstrated that MARK2 promotes phosphorylation of both myosin II and the myosin phosphatase targeting subunit MYPT1 to synergistically drive myosin II contractility and stress fiber formation in cells. Studies with isolated proteins showed that MARK2 directly phosphorylates myosin II regulatory light chain, while its effects on MYPT1 phosphorylation are indirect. Using a mutant lacking the membrane-binding domain, we found that membrane association is required for focal adhesion targeting of MARK2, where it specifically enhances cell protrusion by promoting FAK phosphorylation and formation of focal adhesions oriented in the direction of migration to mediate directionally persistent cell motility. Together, our results define MARK2 as a master regulator of the actomyosin and microtubule cytoskeletal systems and focal adhesions to mediate directional cancer cell migration.

In classical neuroscience experiments, neural activity is measured across many identical trials of animals performing simple tasks and is then analyzed, associating neural responses to pre-defined experimental parameters. This type of analysis is not suitable for patterns of behavior that unfold freely, such as play behavior. Here, we attempt an alternative approach for exploratory data analysis on a single-trial level, applicable in more complex and naturalistic behavioral settings in which no two trials are identical. We analyze neural population activity in the prefrontal cortex (PFC) of rats playing hide-and-seek and show that it is possible to discover what aspects of the task are reflected in the recorded activity with a limited number of simultaneously recorded cells (≤ 31). Using hidden Markov models, we cluster population activity in the PFC into a set of neural states, each associated with a pattern of neural activity. Despite high variability in behavior, relating the inferred states to the events of the hide-and-seek game reveals neural states that consistently appear at the same phases of the game. Furthermore, we show that by applying the segmentation inferred from neural data to the animals' behavior, we can explore and discover novel correlations between neural activity and behavior. Finally, we replicate the results in a second dataset and show that population activity in the PFC displays distinct sets of states during playing hide-and-seek and observing others play the game. Overall, our results reveal robust, state-like representations in the rat PFC during unrestrained playful behavior and showcase the applicability of population analyses in naturalistic neuroscience.

Archaeological consideration of maritime connectivity has ranged from a biogeographical perspective that considers the sea as a barrier to a view of seaways as ancient highways that facilitate exchange. Our results illustrate the former. We report three Late Neolithic human genomes from the Mediterranean island of Malta that are markedly enriched for runs of homozygosity, indicating inbreeding in their ancestry and an effective population size of only hundreds, a striking illustration of maritime isolation in this agricultural society. In the Late Neolithic, communities across mainland Europe experienced a resurgence of hunter-gatherer ancestry, pointing toward the persistence of different ancestral strands that subsequently admixed. This is absent in the Maltese genomes, giving a further indication of their genomic insularity. Imputation of genome-wide genotypes in our new and 258 published ancient individuals allowed shared identity-by-descent segment analysis, giving a fine-grained genetic geography of Neolithic Europe. This highlights the differentiating effects of seafaring Mediterranean expansion and also island colonization, including that of Ireland, Britain, and Orkney. These maritime effects contrast profoundly with a lack of migratory barriers in the establishment of Central European farming populations from Anatolia and the Balkans.

Every spring a 600 lb Atlantic bluefin tuna travels over 3000 miles from Newfoundland to its spawning grounds in the Gulf of Mexico. That it does so on a meal of a couple of bluefish is nothing short of remarkable. Humans will likely never engineer such an efficient swimming machine. Of course, that has not stopped us from trying. We have achieved remarkable progress by following a strategy of inspiration by nature. At the same time, our fish-like robots often fall short of matching fish performance by a considerable margin. Despite our advances, we are still left asking the question: How do fish swim so well?

When faced with limited resources, organisms evolve ways to conserve. In this editorial, Martin introduces a special issue devoted to economies in biology and highlights key issues, including some interesting examples of conservation and how fixed resource budgets force tradeoffs in life history traits.

Comment on Science. 2022 Mar 25;375(6587):eabg7985.

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Comparisons of genomes of different species are used to identify lineage-specific genes, those genes that appear unique to one species or clade. Lineage-specific genes are often thought to represent genetic novelty that underlies unique adaptations. Identification of these genes depends not only on genome sequences, but also on inferred gene annotations. Comparative analyses typically use available genomes that have been annotated using different methods, increasing the risk that orthologous DNA sequences may be erroneously annotated as a gene in one species but not another, appearing lineage specific as a result. To evaluate the impact of such "annotation heterogeneity," we identified four clades of species with sequenced genomes with more than one publicly available gene annotation, allowing us to compare the number of lineage-specific genes inferred when differing annotation methods are used to those resulting when annotation method is uniform across the clade. In these case studies, annotation heterogeneity increases the apparent number of lineage-specific genes by up to 15-fold, suggesting that annotation heterogeneity is a substantial source of potential artifact.

Comment in Curr Biol. 2022 Jun 20;32(12):R567-R569.

Numerous studies have proposed that our adaptive motor behaviors depend on learning a map between sensory information and limb movement,1-3 called an "internal model." From this perspective, how the brain represents internal models is a critical issue in motor learning, especially regarding their association with spatial frames processed in motor planning.4,5 Extensive experimental evidence suggests that during planning stages for visually guided hand reaching, the brain transforms visual target representations in gaze-centered coordinates to motor commands in limb coordinates, via hand-target vectors in workspace coordinates.6-9 While numerous studies have intensively investigated whether the learning for reaching occurs in workspace or limb coordinates,10-20 the association of the learning with gaze coordinates still remains untested.21 Given the critical role of gaze-related spatial coding in reaching planning,22-26 the potential role of gaze states for learning is worth examining. Here, we show that motor memories for reaching are separately learned according to target location in gaze coordinates. Specifically, two opposing visuomotor rotations, which normally interfere with each other, can be simultaneously learned when each is associated with reaching to a foveal target and peripheral one. We also show that this gaze-dependent learning occurs in force-field adaptation. Furthermore, generalization of gaze-coupled reach adaptation is limited across central, right, and left visual fields. These results suggest that gaze states are available in the formation and recall of multiple internal models for reaching. Our findings provide novel evidence that a gaze-dependent spatial representation can provide a spatial coordinate framework for context-dependent motor learning.

Comment in Curr Biol. 2022 Jun 20;32(12):R574-R577.

Reef-building corals are endangered animals with a complex colonial organization. Physiological mechanisms connecting multiple polyps and integrating them into a coral colony are still enigmatic. Using live imaging, particle tracking, and mathematical modeling, we reveal how corals connect individual polyps and form integrated polyp groups via species-specific, complex, and stable networks of currents at their surface. These currents involve surface mucus of different concentrations, which regulate joint feeding of the colony. Inside the coral, within the gastrovascular system, we expose the complexity of bidirectional branching streams that connect individual polyps. This system of canals extends the surface area by 4-fold and might improve communication, nutrient supply, and symbiont transfer. Thus, individual polyps integrate via complex liquid dynamics on the surface and inside the colony.

Comment in Curr Biol. 2022 Jun 20;32(12):R583-R585.

Biddick and Van Stan II introduce how certain plant species harvest rain.

Pra et al. provide an overview of ground squirrels and the physiological adaptations these animals have evolved to contend with harsh climates.

Bacteria have evolved numerous strategies to use resources efficiently. However, bacterial economies depend on both the physiological context of the organisms as well as their growth state - whether they are growing, non-growing or reinitiating growth. In this essay, we discuss some of the features that make bacteria efficient under these different conditions and during the transitions between them. We also highlight the many outstanding questions regarding the physiology of non-growing bacterial cells. Lastly, we examine how efficiency is apparent in both the mode and tempo of bacterial evolution.

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It has become increasingly clear that the microbiome plays a critical role in shaping the host organism's response to disease. There also exists mounting evidence that an organism's ploidy level is important in their response to pathogens and parasites. However, no study has determined whether or how these two factors influence one another. We investigate the effect of whole-genome duplication in Arabidopsis thaliana on the above-ground (phyllosphere) microbiome and determine the interacting impacts of ploidy and microbiome on disease outcome. Using seven independently derived synthetic autotetraploid Arabidopsis accessions and a synthetic leaf-associated bacterial community, we confirm that polyploids are generally more resistant to the model pathogen Pseudomonas syringae pv. Tomato DC3000. Polyploids fare better against the pathogen than diploids do, regardless of microbial inoculation, whereas diploids harboring an intact microbiome have lower pathogen densities than those without. In addition, diploids have elevated numbers of defense-related genes that are differentially expressed in the presence of their phyllosphere microbiota, whereas polyploids exhibit some constitutively activated defenses, regardless of colonization by the synthetic community. These results imply that whole-genome duplication can enhance immunity, resulting in a decreased dependence on the microbiome for protection against pathogens.

All visual animals experience optic flow-global visual motion across the retina, which is used to control posture and movement.1 The midbrain circuitry for optic flow is highly conserved in vertebrates,2-6 and these neurons show similar response properties across tetrapods.4,7-16 These neurons have large receptive fields and exhibit both direction and velocity selectivity in response to large moving stimuli. Hummingbirds deviate from the typical vertebrate pattern in several respects.17,18 Their lentiformis mesencephali (LM) lacks the directional bias seen in other tetrapods and has an overall bias for faster velocities. This led Ibbotson19 to suggest that the hummingbird LM may be specialized for hovering close to visual structures, such as plants. In such an environment, even slight body motions will translate into high-velocity optic flow. A prediction from this hypothesis is that hummingbird LM neurons should be more responsive to large visual features. We tested this hypothesis by measuring neural responses of hummingbirds and zebra finches to sine wave gratings of varying spatial and temporal frequencies. As predicted, the hummingbird LM displayed an overall preference for fast optic flow because neurons were biased to lower spatial frequencies. These neurons were also tightly tuned in the spatiotemporal domain. We found that the zebra finch LM specializes along another domain: many neurons were initially tuned to high temporal frequencies followed by a shift in location and orientation to slower velocity tuning. Collectively, these results demonstrate that the LM has distinct and specialized tuning properties in at least two bird species.

Age-related deficits in pattern separation have been postulated to bias the output of hippocampal memory processing toward pattern completion, which can cause deficits in accurate memory retrieval. Although the CA3 region of the hippocampus is often conceptualized as a homogeneous network involved in pattern completion, growing evidence demonstrates a functional gradient in CA3 along the transverse axis, as pattern-separated outputs (dominant in the more proximal CA3) transition to pattern-completed outputs (dominant in the more distal CA3). We examined the neural representations along the CA3 transverse axis in young (Y), aged memory-unimpaired (AU), and aged memory-impaired (AI) rats when different changes were made to the environment. Functional heterogeneity in CA3 was observed in Y and AU rats when the environmental similarity was high (altered cues or altered environment shapes in the same room), with more orthogonalized representations in proximal CA3 than in distal CA3. In contrast, AI rats showed reduced orthogonalization in proximal CA3 but showed normal (i.e., generalized) representations in distal CA3, with little evidence of a functional gradient. Under experimental conditions when the environmental similarity was low (different rooms), representations in proximal and distal CA3 remapped in all rats, showing that CA3 of AI rats is able to encode distinctive representations for inputs with greater dissimilarity. These experiments support the hypotheses that the age-related bias toward hippocampal pattern completion is due to the loss in AI rats of the normal transition from pattern separation to pattern completion along the CA3 transverse axis.

Comment in Curr Biol. 2022 Jun 20;32(12):R569-R571.