Comment on Curr Biol. 2022 Apr 25;32(8):1788-1797.e5.

Comment on Curr Biol. 2022 Apr 25;32(8):1837-1842.e3.

Dataset described in Curr Biol. 2022 Apr 25;32(8):1798-1811.e8.

Comment on Curr Biol. 2022 Apr 25;32(8):1675-1688.e7.

Pim Bongaerts introduces mesophotic, lower-light coral ecosystems.

Plant secondary growth, which is the basis of wood formation, includes the production of secondary xylem, which is derived from meristematic cambium cells embedded in vascular tissue. Here, we identified an important role for the Arabidopsis thaliana (Arabidopsis) AT-HOOK MOTIF CONTAINING NUCLEAR LOCALIZED 15 (AHL15) transcriptional regulator in controlling vascular cambium activity. The limited secondary xylem development in inflorescence stems of herbaceous Arabidopsis plants was significantly reduced in ahl15 loss-of-function mutants, whereas constitutive or vascular meristem-specific AHL15 overexpression produced woody inflorescence stems. AHL15 was required for enhanced secondary xylem formation in the woody suppressor of overexpression of constans 1 (soc1) fruitfull (ful) double loss-of-function mutant. Moreover, we found that AHL15 induces vascular cambium activity downstream of the repressing SOC1 and FUL transcription factors, most likely similar to how it enhances lateral branching by promoting biosynthesis of the hormone cytokinin. Our results uncover a novel pathway driving cambium development, in which AHL15 expression levels act in parallel to and are dependent on the well-established TDIF-PXY-WOX pathway to differentiate between herbaceous and woody stem growth.

Comment in Curr Biol. 2022 Apr 25;32(8):R365-R367.

Comment in Curr Biol. 2022 Apr 25;32(8):R360-R362.

The lateral habenula (LHb) supports learning processes enabling the prediction of upcoming rewards. While reward-related stimuli decrease the activity of LHb neurons, whether this anchors on synaptic inhibition to guide reward-driven behaviors remains poorly understood. Here, we combine in vivo two-photon calcium imaging with Pavlovian conditioning in mice and report that anticipatory licking emerges along with decreases in cue-evoked calcium signals in individual LHb neurons. In vivo multiunit recordings and pharmacology reveal that the cue-evoked reduction in LHb neuronal firing relies on GABAA-receptor activation. In parallel, we observe a postsynaptic potentiation of GABAA-receptor-mediated inhibition, but not excitation, onto LHb neurons together with the establishment of anticipatory licking. Finally, strengthening or weakening postsynaptic inhibition with optogenetics and GABAA-receptor manipulations enhances or reduces anticipatory licking, respectively. Hence, synaptic inhibition in the LHb shapes reward anticipation.

The textbook view of cell division terminates with the final separation of the two daughter cells in the process called abscission. However, in contrast to this classical view, a variety of cell types in multicellular organisms are connected through cytoplasmic bridges, which most often form by incomplete abscission or - more rarely - by local fusion of plasma membranes. In this review, we survey the distribution, function, and formation of cytoplasmic bridges across the eukaryotic tree of life. We find that cytoplasmic bridges are widespread, and were likely ancestrally present, in almost all lineages of eukaryotes with clonal multicellularity - including the five 'complex multicellular' lineages: animals, fungi, land plants, red algae, and brown algae. In animals, cytoplasmic bridges resulting from incomplete abscission are ubiquitous in the germline and common in pluripotent cell types. Although cytoplasmic bridges have been less studied than other structural mediators of multicellularity (such as adhesion proteins and extracellular matrix), we propose that they have played a pivotal role in the repeated evolution of eukaryotic clonal multicellularity - possibly by first performing a structural role and later by allowing exchange of nutrients and/or intercellular communication, which notably buffered cell-cell competition by averaging gene expression. Bridges were eventually lost from many animal tissues in concert with the evolution of spatial cell differentiation, cell motility within the organism, and other mechanisms for intercellular distribution of signals and metabolites. Finally, we discuss the molecular basis for the evolution of incomplete abscission and examine the alternative hypotheses of single or multiple origins.

Comment on Nature. 2022 Feb;602(7897):455-460.

Comment on Curr Biol. 2022 Apr 25;32(8):1852-1860.e5.

Robinson and colleagues respond to the points raised about their paper by Bakker et al.

Comment on Curr Biol. 2021 Jul 12;31(13):2939-2946.e5.

In the animal world, numerous mechanisms have been described that allow for extremely fast actions or reactions via the slow storage of energy, typically in elastic structures, which is then nearly instantly released1-4, similar to the operation of a catapult. Many of these mechanisms are employed for prey capture1,2 or for predator avoidance3,4; however, such superfast actions have not yet been reported as a means to dodge sexual cannibalism. Here, we unveil a novel mechanism in a communal orb-weaving spider Philoponella prominens (Uloboridae) (Figure S1), whereby males undertake a split-second catapult action immediately after mating, thereby fleeing their partner (Video S1). We demonstrate that males achieve their superfast action (up to 88.2 cm/s) by extending the tibia-metatarsus joint of their first leg pair via hydraulic pressure in a joint that is known to lack extensor muscles in spiders. This rapid expansion greatly reduces the likelihood of the male being sexually cannibalized.

Comment in Curr Biol. 2022 Apr 25;32(8):R380-R382.

The functional properties of neocortical pyramidal cells (PCs), such as direction and orientation selectivity in visual cortex, predominantly derive from their excitatory and inhibitory inputs. For layer 2/3 (L2/3) PCs, the detailed relationship between their functional properties and how they sample and integrate information across cortical space is not fully understood. Here, we study this relationship by combining functional in vivo two-photon calcium imaging, in vitro functional circuit mapping, and dendritic reconstruction of the same L2/3 PCs in mouse visual cortex. Our work reveals direct correlations between dendritic morphology and functional input connectivity and the orientation as well as direction tuning of L2/3 PCs. First, the apical dendritic tree is elongated along the postsynaptic preferred orientation, considering the representation of visual space in the cortex as determined by its retinotopic organization. Additionally, sharply orientation-tuned cells show a less complex apical tree compared with broadly tuned cells. Second, in direction-selective L2/3 PCs, the spatial distribution of presynaptic partners is offset from the soma opposite to the preferred direction. Importantly, although the presynaptic excitatory and inhibitory input distributions spatially overlap on average, the excitatory input distribution is spatially skewed along the preferred direction, in contrast to the inhibitory distribution. Finally, the degree of asymmetry is positively correlated with the direction selectivity of the postsynaptic L2/3 PC. These results show that the dendritic architecture and the spatial arrangement of excitatory and inhibitory presynaptic cells of L2/3 PCs play important roles in shaping their orientation and direction tuning.

Comment in Curr Biol. 2022 Apr 25;32(8):R362-R365.

Comment in Curr Biol. 2022 Apr 25;32(8):R367-R370.

Adequate nutrition is essential for normal reproductive function, which is vital for species to survive. In humans and other mammals, starvation and undernutrition deplete fat reserves and cause weight loss, attenuating the function of the reproductive axis and causing hypogonadism.1-4 Thirteen-lined ground squirrels (Ictidomys tridecemlineatus) spend 7 months of every year in hibernation without food and water. Hibernating squirrels alternate between periods of torpor and interbout arousal (IBA), when animals temporarily return to an active-like state.5 The physiological significance of IBA is unclear, but it is thought to be essential for hibernation in animals that drop their body temperature to 2°C-4°C during torpor. Here, we report that juvenile male ground squirrels initiate reproductive maturation during their first hibernation season, despite prolonged undernutrition and profound weight loss. We show that the hypothalamic reproductive axis undergoes activation during interbout arousals in the middle of hibernation, triggering production of luteinizing hormone and testosterone, and promoting testicular growth. Initiation of sexual maturation is circannually entrained and is independent of physiological state, ambient temperature, and food availability. Our study suggests a role for interbout arousals during hibernation and uncovers the neurophysiological mechanism of reproductive axis activation during conditions of extreme negative energy balance. VIDEO ABSTRACT.

Comment on Curr Biol. 2022 Apr 25;32(8):1776-1787.e4.

Dataset use reported in Curr Biol. 2022 Apr 25;32(8):R370-R372.

Many animals have evolved a migratory lifestyle as an adaptation to seasonality,1,2 ranging from insects3 to fish,4 terrestrial and marine mammals,5-7 and birds.8 Old World swifts have evolved an extraordinary aerial non-breeding life phase lasting for 6-10 months.9-11 Swifts exploit the aerosphere in search of insects to meet the high energy demands of flight.12 During this period they roost and likely also sleep in the open airspace. Nocturnal insectivores with restricted foraging time may use moonlight to increase energy intake.13 Using multisensor data loggers that record light for geolocation, acceleration for flight activity, and pressure for flight altitude, we investigated if Northern black swifts, Cypseloides niger borealis, breeding in North America, also lead an aerial lifestyle similar to their Old World relatives. Individual flight activity showed they are airborne >99% of the time, with only occasional landings during their 8-month non-breeding period. Unexpectedly, during periods around the full moon, they conducted regular nocturnal ascents to altitudes up to >4,000 m (mean 2,000 m). A lunar eclipse triggered a synchronized descent, showing a direct effect of moonlight on flight altitude. This previously unknown behavior of nocturnal ascents during moonlight nights could be either a response to predator avoidance or that moonlight provides a foraging opportunity. Observed elevated nocturnal flight activity during periods of moonlight compared to dark nights suggests swifts were hawking for prey. Our finding of this novel behavior provides new perspectives on nocturnal flight behavior during periods surrounding the full moon.

Conservation strategies are rarely systematically evaluated, which reduces transparency, hinders the cost-effective deployment of resources, and hides what works best in different contexts. Using data on the iconic and critically endangered orangutan (Pongo spp.), we developed a novel spatiotemporal framework for evaluating conservation investments. We show that around USD 1 billion was invested between 2000 and 2019 into orangutan conservation by governments, nongovernmental organizations, companies, and communities. Broken down by allocation to different conservation strategies, we find that habitat protection, patrolling, and public outreach had the greatest return on investment for maintaining orangutan populations. Given the variability in threats, land-use opportunity costs, and baseline remunerations in different regions, there were differential benefits per dollar invested across conservation activities and regions. We show that although challenging from a data and analysis perspective, it is possible to fully understand the relationships between conservation investments and outcomes and the external factors that influence these outcomes. Such analyses can provide improved guidance toward a more effective biodiversity conservation. Insights into the spatiotemporal interplays between the costs and benefits driving effectiveness can inform decisions about the most suitable orangutan conservation strategies for halting population declines. Although our study focuses on the three extant orangutan species of Sumatra and Borneo, our findings have broad application for evidence-based conservation science and practice worldwide.

To find food efficiently, a hungry animal engages in goal-directed behaviors that rely on nucleus accumbens (NAc) circuits. Synaptic alterations within these circuits underlie shifts in behavior across motivational states. Here, we show that hunger dampens an NAc to lateral hypothalamus (LH) circuit to promote persistent food seeking. BigLEN, a hunger-driven neuropeptide, acts through its receptor GPR171 to inhibit glutamate transmission onto NAc shell Drd1+ LH-projecting medium spiny neurons by suppressing cholinergic signaling. The antagonism of GPR171 in food-deprived animals reduces persistent unrewarded food-seeking behavior but does not alter effortful food seeking or overall food intake. The chemogenetic upregulation of the NAc to LH circuit reduces this persistent unrewarded responding in hungry animals. These results describe how hunger-driven neuromodulation targets a distinct dimension of motivated behavior by shaping information flow through anatomically defined circuit elements.

Pan-neuronally expressed genes, such as genes involved in the synaptic vesicle cycle or in neuropeptide maturation, are critical for proper function of all neurons, but the transcriptional control mechanisms that direct such genes to all neurons of a nervous system remain poorly understood. We show here that six members of the CUT family of homeobox genes control pan-neuronal identity specification in Caenorhabditis elegans. Single CUT mutants show barely any effects on pan-neuronal gene expression or global nervous system function, but such effects become apparent and progressively worsen upon removal of additional CUT family members, indicating a critical role of gene dosage. Overexpression of each individual CUT gene rescued the phenotype of compound mutants, corroborating that gene dosage, rather than the activity of specific members of the gene family, is critical for CUT gene family function. Genome-wide binding profiles, as well as mutation of CUT homeodomain binding sites by CRISPR/Cas9 genome engineering show that CUT genes directly control the expression of pan-neuronal features. Moreover, CUT genes act in conjunction with neuron-type-specific transcription factors to control pan-neuronal gene expression. Our study, therefore, provides a previously missing key insight into how neuronal gene expression programs are specified and reveals a highly buffered and robust mechanism that controls the most critical functional features of all neuronal cell types.

Comment in Curr Biol. 2022 Apr 25;32(8):R375-R377.

Comment in Curr Biol. 2022 Apr 25;32(8):R378-R379.

Comment on Curr Biol. 2022 Apr 25;32(8):1843-1851.e2.

Comment on Curr Biol. 2022 Apr 25;32(8):1869-1874.e4.

Comment on Curr Biol. 2022 Apr 25;32(8):1728-1742.e6.

Near-ground growth offers low-statured plants many benefits but also exposes them to the risk of being overtopped and losing access to sunlight. Plant community development is often portrayed as a process of serial dominance by successively taller species, but here we describe a mechanism by which a low-growing rosette species alters community spatial structure. Elephantopus elatus (Asteraceae), an herbaceous savanna plant with low-growing leaves that emerge radially from a central bud, pushes neighboring plants away and thereby avoids being overtopped. Active pushing is possible because the leaves have stout petioles that are basally anchored rather than attached to flexible twigs or stems. This growth-mediated leaf pushing introduces a novel example of active plant interactions that is likely important for other rosette plants.

The prefrontal cortex is a well-studied but, in terms of understanding what it is for, deeply divisive part of the brain located at the front of the head. Perhaps the least controversial feature of the prefrontal cortex is its complexity. The prefrontal cortex is anatomically, functionally, and computationally complex. It is anatomically complex, containing a number of subregions each sending and receiving projections to a unique set of other cortical and subcortical areas. This interconnectivity presents a serious challenge to efforts to localize function to prefrontal cortex, because it can seem as though information flows everywhere all at once in prefrontal networks. Perhaps as a result, prefrontal cortex is also computationally complex: working memory, abstraction, sensory attention, value-based decision making, planning, and motor control are all functions that have been attributed to the prefrontal cortex. This diversity of functions is likely to reflect the diversity of brain regions that prefrontal cortex communicates with while carrying out the computations it performs to influence behavior.

Ingested nutrients are proposed to control mammalian behavior by modulating the activity of hypothalamic orexin/hypocretin neurons (HONs). Previous in vitro studies showed that nutrients ubiquitous in mammalian diets, such as non-essential amino acids (AAs) and glucose, modulate HONs in distinct ways. Glucose inhibits HONs, whereas non-essential (but not essential) AAs activate HONs. The latter effect is of particular interest because its purpose is unknown. Here, we show that ingestion of a dietary-relevant mix of non-essential AAs activates HONs and shifts behavior from eating to exploration. These effects persisted despite ablation of a key neural gut → brain communication pathway, the cholecystokinin-sensitive vagal afferents. The behavioral shift induced by the ingested non-essential AAs was recapitulated by targeted HON optostimulation and abolished in mice lacking HONs. Furthermore, lick microstructure analysis indicated that intragastric non-essential AAs and HON optostimulation each reduce the size, but not the frequency, of consumption bouts, thus implicating food palatability modulation as a mechanism for the eating suppression. Collectively, these results suggest that a key purpose of HON activation by ingested, non-essential AAs is to suppress eating and re-initiate food seeking. We propose and discuss possible evolutionary advantages of this, such as optimizing the limited stomach capacity for ingestion of essential nutrients.

Gastrulation movements in all animal embryos start with regulated deformations of patterned epithelial sheets, which are driven by cell divisions, cell shape changes, and cell intercalations. Each of these behaviors has been associated with distinct aspects of gastrulation1-4 and has been a subject of intense research using genetic, cell biological, and more recently, biophysical approaches.5-14 Most of these studies, however, focus either on cellular processes driving gastrulation or on large-scale tissue deformations.15-23 Recent advances in microscopy and image processing create a unique opportunity for integrating these complementary viewpoints.24-28 Here, we take a step toward bridging these complementary strategies and deconstruct the early stages of gastrulation in the entire Drosophila embryo. Our approach relies on an integrated computational framework for cell segmentation and tracking and on efficient algorithms for event detection. The detected events are then mapped back onto the blastoderm shell, providing an intuitive visual means to examine complex cellular activity patterns within the context of their initial anatomic domains. By analyzing these maps, we identified that the loss of nearly half of surface cells to invaginations is compensated primarily by transient mitotic rounding. In addition, by analyzing mapped cell intercalation events, we derived direct quantitative relations between intercalation frequency and the rate of axis elongation. This work is setting the stage for systems-level dissection of a pivotal step in animal development.

Sexually dimorphic courtship behaviors in Drosophila melanogaster develop from the activity of the sexual differentiation genes, doublesex (dsx) and fruitless (fru), functioning with other regulatory factors that have received little attention. The dissatisfaction (dsf) gene encodes an orphan nuclear receptor homologous to vertebrate Tlx and Drosophila tailless that is critical for the development of several aspects of female- and male-specific sexual behaviors. Here, we report the pattern of dsf expression in the central nervous system and show that the activity of sexually dimorphic abdominal interneurons that co-express dsf and dsx is necessary and sufficient for vaginal plate opening in virgin females, ovipositor extrusion in mated females, and abdominal curling in males during courtship. We find that dsf activity results in different neuroanatomical outcomes in females and males, promoting and suppressing, respectively, female development and function of these neurons depending upon the sexual state of dsx expression. We posit that dsf and dsx interact to specify sex differences in the neural circuitry for dimorphic abdominal behaviors.

Comment in Curr Biol. 2022 Apr 25;32(8):R373-R375.

Comment on Curr Biol. 2022 Apr 11;32(7):1457-1469.e4.

Comment on Curr Biol. 2022 Mar 14;32(5):999-1009.e9.

Mlynarek introduces the important ecological and agricultural role of flies as pollinators.

Comment in Curr Biol. 2022 Apr 11;32(7):R324-R327.

Comment in Curr Biol. 2022 Apr 11;32(7):R320-R322.

Limb phase, the timing of the footfalls in quadrupedal locomotion that describes common gaits such as the trot and the pace gait,1,2 is widely believed to be difficult or even impossible to estimate for extinct tetrapods.3-5 We here present a fundamentally new approach that allows for estimating limb phase based on variation patterns in long trackways. The approach is tested on trackways of modern mammals, where the estimates generally correspond well with the actually employed limb phase. We then estimate limb phases of giant wide-gauged sauropod dinosaurs based on three long trackways from the Lower Cretaceous of Arkansas, US.6,7 Gait selection at the largest body sizes is of considerable interest given the lack of modern analogs. Contrary to previous assumptions,8,9 our estimates suggest lateral sequence diagonal couplet walks, in which the footfalls of the diagonal limb pairs (e.g., right hind and left fore) are more closely related in time than those of the same side of the body (e.g., right hind and right fore). Such a gait selection allows for efficient walking while maintaining diagonal limb support throughout the step cycle, which is important for a giant, wide-gauged trackmaker.10 Estimations of limb phase may help to constrain other gait parameters, body size and shape, and, finally, potential trackmaker taxa.

During motor learning,1 as well as during neuroprosthetic learning,2-4 animals learn to control motor cortex activity in order to generate behavior. Two different populations of motor cortex neurons, intra-telencephalic (IT) and pyramidal tract (PT) neurons, convey the resulting cortical signals within and outside the telencephalon. Although a large amount of evidence demonstrates contrasting functional organization among both populations,5,6 it is unclear whether the brain can equally learn to control the activity of either class of motor cortex neurons. To answer this question, we used a calcium-imaging-based brain-machine interface (CaBMI)3 and trained different groups of mice to modulate the activity of either IT or PT neurons in order to receive a reward. We found that the animals learned to control PT neuron activity faster and better than IT neuron activity. Moreover, our findings show that the advantage of PT neurons is the result of characteristics inherent to this population as well as their local circuitry and cortical depth location. Taken together, our results suggest that the motor cortex is more efficient at controlling the activity of pyramidal tract neurons, which are embedded deep in the cortex, and relaying motor commands outside the telencephalon.

Comment in Curr Biol. 2022 Apr 11;32(7):R331-R333.

Comment on Curr Biol. 2022 Apr 11;32(7):1523-1533.e6.

Comment on Curr Biol. 2022 Mar 14;32(5):1206-1210.e3.

Comment on Curr Biol. 2022 Apr 11;32(7):1534-1547.e9.

In the vertebrate eye, photoreceptors are covered beneath a thick sheet of neural retina and face away from the light. This seemingly awkward arrangement has led to the popular notion that our retinas are upside down, implying a deep design flaw. Baden and Nilsson argue that, from an evolutionary perspective, an inverted design actually offers many notable benefits that might have never been exploited if things had started off the other way round.

Interview with Richard Losick, who investigates cell fate determination and decision-making in bacteria at Harvard University.

Mitochondrial damage (MtD) represents a dramatic change in cellular homeostasis, necessitating metabolic changes and stimulating mitophagy. One rapid response to MtD is a rapid peri-mitochondrial actin polymerization termed ADA (acute damage-induced actin). The activation mechanism for ADA is unknown. Here, we use mitochondrial depolarization or the complex I inhibitor metformin to induce ADA. We show that two parallel signaling pathways are required for ADA. In one pathway, increased cytosolic calcium in turn activates PKC-β, Rac, WAVE regulatory complex, and Arp2/3 complex. In the other pathway, a drop in cellular ATP in turn activates AMPK (through LKB1), Cdc42, and FMNL formins. We also identify putative guanine nucleotide exchange factors for Rac and Cdc42, Trio and Fgd1, respectively, whose phosphorylation states increase upon mitochondrial depolarization and whose suppression inhibits ADA. The depolarization-induced calcium increase is dependent on the mitochondrial sodium-calcium exchanger NCLX, suggesting initial mitochondrial calcium efflux. We also show that ADA inhibition results in enhanced mitochondrial shape changes upon mitochondrial depolarization, suggesting that ADA inhibits these shape changes. These depolarization-induced shape changes are not fragmentation but a circularization of the inner mitochondrial membrane, which is dependent on the inner mitochondrial membrane protease Oma1. ADA inhibition increases the proteolytic processing of an Oma1 substrate, the dynamin GTPase Opa1. These results show that ADA requires the combined action of the Arp2/3 complex and formin proteins to polymerize a network of actin filaments around mitochondria and that the ADA network inhibits the rapid mitochondrial shape changes that occur upon mitochondrial depolarization.

Developing animals absorb nutrients either through the placenta or from ingested food; however, the mechanisms by which embryos use external nutrients for individual organ morphogenesis remain to be elucidated. In this study, we assessed nutrient-dependent thyroid follicle morphogenesis in Xenopus laevis and investigated the role of secreted gastrointestinal (GI) hormones post-feeding. We found that feeding triggers thyroid follicle formation, and the thyroid cells showed transient inactivation of cell proliferation after feeding. In addition, the thyroid cells with multi-lumina were frequently observed in the fed tadpoles. The expression of the particular GI hormone incretin, glucose-dependent insulinotropic polypeptide (GIP), responded to feeding in the intestines of Xenopus tadpoles. Inhibition of dipeptidyl peptidase 4 (Dpp4), a degradative enzyme of incretin, increased the size of the thyroid follicles by facilitating follicular lumina connection, whereas inhibition of the sodium-glucose cotransporter (SGLT) reversed the effects of Dpp4 inhibition. Furthermore, injection of GIP peptide in unfed tadpoles initiated thyroid follicle formation-without requiring feeding-and injection of an incretin receptor antagonist suppressed follicle enlargement in the fed tadpoles. Lastly, GIP receptor knockout in neonatal mice showed smaller follicles in the thyroid, suggesting that the GI hormone-dependent thyroid morphogenesis is conserved in mammals. In conclusion, our study links external nutrients to thyroid morphogenesis and provides new insights into the function of GI hormone as a regulator of organ morphology in developing animals.

Comment in Curr Biol. 2022 Apr 11;32(7):R316-R317.

Postrhinal cortex (POR) and neighboring lateral visual association areas are necessary for identifying objects and interpreting them in specific contexts, but how POR neurons encode the same object across contexts remains unclear. Here, we imaged excitatory neurons in mouse POR across tens of days prior to and throughout initial cue-reward learning and reversal learning. We assessed responses to the same cue when it was rewarded or unrewarded, during both locomotor and stationary contexts. Surprisingly, a large class of POR neurons were minimally cue-driven prior to learning. After learning, distinct clusters within this class responded selectively to a given cue when presented in a specific conjunction of reward and locomotion contexts. In addition, another class contained clusters of neurons whose cue responses were more transient, insensitive to reward learning, and adapted over thousands of presentations. These two classes of POR neurons may support context-dependent interpretation and context-independent identification of sensory cues.

The instructive role of mechanical cues during morphogenesis is increasingly being recognized in all kingdoms. Patterns of mechanical stress depend on shape, growth and external factors. In plants, the cell wall integrates these three parameters to function as a hub for mechanical feedback. Plant cells are interconnected by cell walls that provide structural integrity and yet are flexible enough to act as both targets and transducers of mechanical cues. Such cues may act locally at the subcellular level or across entire tissues, requiring tight control of both cell-wall composition and cell-cell adhesion. Here we focus on how changes in cell-wall chemistry and mechanics act in communicating diverse cues to direct growth asymmetries required for plant morphogenesis. We explore the role of cellulose microfibrils, microtubule arrays and pectin methylesterification in the transduction of mechanical cues during morphogenesis. Plant hormones can affect the mechanochemical composition of the cell wall and, in turn, the cell wall can modulate hormone signaling pathways, as well as the tissue-level distribution of these hormones. This also leads us to revisit the position of biochemical growth factors, such as plant hormones, acting both upstream and downstream of mechanical signaling. Finally, while the structure of the cell wall is being elucidated with increasing precision, existing data clearly show that the integration of genetic, biochemical and theoretical studies will be essential for a better understanding of the role of the cell wall as a hub for the mechanical control of plant morphogenesis.

Comment on Curr Biol. 2022 Apr 11;32(7):1511-1522.e6.

Comment on Curr Biol. 2022 Apr 11;32(7):R309-R310.

Comment on Curr Biol. 2022 Apr 11;32(7):1593-1598.e3.

Comment on Curr Biol. 2022 Apr 11;32(7):1470-1484.e12.

Vocal interactions are intrinsic features of social groups and can play a pivotal role in social bonding.1,2 Dunbar's social bonding hypothesis posits that vocal exchanges evolved to "groom at a distance" when social groups became too large or complex for individuals to devote time to physical bonding activities.1,3 Tests of this hypothesis in non-human primates, however, suggest that vocal exchanges occur between more strongly bonded individuals that engage in higher grooming rates4-7 and thus do not provide evidence for replacement of physical bonding. Here, we combine data on social bond strength, whistle exchange frequency, and affiliative contact behavior rates to test this hypothesis in wild male Indo-Pacific bottlenose dolphins, who form multi-level alliances that cooperate over access to females.8-10 We show that, although whistle exchanges are more likely to occur within the core alliance, they occur more frequently between those males that share weaker social bonds, i.e., between core allies that spend less time together, while the opposite occurs for affiliative physical contact behavior. This suggests that vocal exchanges function as a low-cost mechanism for male dolphins that spend less time in close proximity and engage in fewer affiliative contact behaviors to reinforce and maintain their valuable alliance relationships. Our findings provide new evidence outside of the primate lineage that vocal exchanges serve a bonding function and reveal that, as the social bonding hypothesis originally suggested, vocal exchanges can function as a replacement of physical bonding activities for individuals to maintain their important social relationships.

Nutrition is one of the most important influences on growth and the timing of maturational transitions including mammalian puberty and insect metamorphosis. Childhood obesity is associated with precocious puberty, but the assessment mechanism that links body fat to early maturation is unknown. During development, the intake of nutrients promotes signaling through insulin-like systems that govern the growth of cells and tissues and also regulates the timely production of the steroid hormones that initiate the juvenile-adult transition. We show here that the dietary lipid cholesterol, which is required as a component of cell membranes and as a substrate for steroid biosynthesis, also governs body growth and maturation in Drosophila via promoting the expression and release of insulin-like peptides. This nutritional input acts via the nutrient sensor TOR, which is regulated by the Niemann-Pick-type-C 1 (Npc1) cholesterol transporter, in the glia of the blood-brain barrier and cells of the adipose tissue to remotely drive systemic insulin signaling and body growth. Furthermore, increasing intracellular cholesterol levels in the steroid-producing prothoracic gland strongly promotes endoreduplication, leading to an accelerated attainment of a nutritional checkpoint that normally ensures that animals do not initiate maturation prematurely. These findings, therefore, show that a Npc1-TOR signaling system couples the sensing of the lipid cholesterol with cellular and systemic growth control and maturational timing, which may help explain both the link between cholesterol and cancer as well as the connection between body fat (obesity) and early puberty.

Paleontological evidence reveals that the rapid growth characteristic of living birds evolved close to the origin of the crown-group Neornithes, as more stemward birds experienced protracted growth until becoming fully grown.1 Research on Mesozoic confuciusornithids, the earliest divergence of fully beaked birds, has revealed a complex life cycle in which these birds experienced multiple growth phases.2-4 Such a life-history pattern calls for the exploration of the role that ontogenetic niche shifts may have played in size-structuring confuciusornithid populations.5,6 Here, by analyzing the skeletal morphometrics of a dense sample of fossil individuals of Confuciusornis sanctus (n = 171, all fledged), we show that the youngest individuals of this confuciusornithid species experienced a precocious burst of beak growth, probably facilitating access to novel food resources that helped them meet the high energetic demands of their initial growth spurt. Such an early burst of facial (i.e., snout) growth resembles that of young crocodilians.7 However, in these reptiles, facial growth slows down soon thereafter, and the matching of snout scaling between mid-sized and larger individuals instigates demographic competence and the dispersion of the former.8 In contrast, our results reveal that beak growth in C. sanctus continued steadily. We hypothesized that the protracted facial growth of older individuals led to ontogenetic niche shifts by dietary segregation among size classes within populations. Our study thus confirms that the life cycle of C. sanctus was notably different from that of modern birds, and it reveals that beak size allometry may have facilitated population cohesiveness between coinhabiting age classes.

Comment in Curr Biol. 2022 Jun 6;32(11):R528-R530.

Comment on Curr Biol. 2022 Apr 11;32(7):1650-1656.e3.

Comment in Curr Biol. 2022 Apr 11;32(7):R318-R320.

Respiratory syncytial virus (RSV) is an enveloped non-segmented negative sense RNA virus that belongs to Orthopneumovirus genus of the Pneumoviridae family in the order Mononegavirales. The virus is the leading cause of severe respiratory disease in children under two years of age and is responsible for substantial disease burden in infants and elder people in both developed and developing countries1,2. RSV is only known to circulate among humans, though it was first isolated from chimpanzees3. The virus can experimentally infect mice, rats, cotton rats, ferrets, and hamsters, but does not naturally circulate in these animal populations4. We found that Malayan pangolins (Manis javanica) were naturally infected with RSVs that have 99.4-99.8% genomic identity with strains circulating in humans. Phylogenetic analyses revealed that five RSVs in pangolins were RSV-A ON1 and seven were RSV-B BA genotypes, both of which are currently prevalent in humans worldwide. These findings suggest that humans might transmit their viruses to endangered wildlife.

Understanding determinants of differential reproductive success is at the core of evolutionary biology because of its connection to fitness. Early work has linked variation in reproductive success to differences in age,1 rank,2 or size,3,4 as well as habitat characteristics.5 More recently, studies in group-living taxa have revealed that social relationships also have measurable effects on fitness.6-8 The influence of social bonds on fitness is particularly interesting in males who compete over reproductive opportunities. In Shark Bay, Western Australia, groups of 4-14 unrelated male bottlenose dolphins cooperate in second-order alliances to compete with rival alliances over access to females.9-12 Nested within second-order alliances, pairs or trios of males, which can vary in composition, form first-order alliances to herd estrus females. Using 30 years of behavioral data, we examined how individual social factors, such as first-order alliance stability, social connectivity, and variation in social bond strength within second-order alliances, affect male fitness. Analyzing the reproductive careers of 85 males belonging to 10 second-order alliances, we found that the number of paternities a male achieved was positively correlated with his cumulative social bond strength but negatively correlated with his variation in bond strength. Thus, well-integrated males with more homogeneous social bonds to second-order allies obtained most paternities. Our findings provide novel insights into the fitness benefits of polyadic cooperation among unrelated males and highlight the adaptive value of social bonds in this context.

Comment in Curr Biol. 2022 Apr 11;32(7):R329-R331.

Comment in Curr Biol. 2022 Apr 11;32(7):R327-R328.

Inbreeding often imposes net fitness costs,1-5 leading to the expectation that animals will engage in inbreeding avoidance when the costs of doing so are not prohibitive.4-9 However, one recent meta-analysis indicates that animals of many species do not avoid mating with kin in experimental settings,6 and another reports that behavioral inbreeding avoidance generally evolves only when kin regularly encounter each other and inbreeding costs are high.9 These results raise questions about the processes that separate kin, how these processes depend on kin class and context, and whether kin classes differ in how effectively they avoid inbreeding via mate choice-in turn, demanding detailed demographic and behavioral data within individual populations. Here, we address these questions in a wild mammal population, the baboons of the Amboseli ecosystem in Kenya. We find that death and dispersal are very effective at separating opposite-sex pairs of close adult kin. Nonetheless, adult kin pairs do sometimes co-reside, and we find strong evidence for inbreeding avoidance via mate choice in kin classes with relatedness ≥0.25. Notably, maternal kin avoid inbreeding more effectively than paternal kin despite having identical coefficients of relatedness, pointing to kin discrimination as a potential constraint on effective inbreeding avoidance. Overall, demographic and behavioral processes ensure that inbred offspring are rare in undisturbed social groups (1% of offspring). However, in an anthropogenically disturbed social group with reduced male dispersal, we find inbreeding rates 10× higher. Our study reinforces the importance of demographic and behavioral contexts for understanding the evolution of inbreeding avoidance.9.

Erratum in Curr Biol. 2022 Mar 28;32(6):1454-1455.

There is an urgent need to halt and reverse loss of mangroves and seagrass to protect and increase the ecosystem services they provide to coastal communities, such as enhancing coastal resilience and contributing to climate stability.1,2 Ambitious targets for their recovery can inspire public and private investment in conservation,3 but the expected outcomes of different protection and restoration strategies are unclear. We estimated potential recovery of mangroves and seagrass through gains in ecosystem extent to the year 2070 under a range of protection and restoration strategies implemented until the year 2050. Under a protection-only scenario, the current trajectories of net mangrove loss slowed, and a minor net gain in global seagrass extent (∼1%) was estimated. Protection alone is therefore unlikely to drive sufficient recovery. However, if action is taken to both protect and restore, net gains of up to 5% and 35% of mangroves and seagrasses, respectively, could be achieved by 2050. Further, protection and restoration can be complementary, as protection prevents losses that would otherwise occur post-2050, highlighting the importance of implementing protection measures. Our findings provide the scientific evidence required for setting strategic and ambitious targets to inspire significant global investment and effort in mangrove and seagrass conservation.

The strong air temperature warming between the 1950s and 2016 in the Antarctic Peninsula region1 exceeded the global average warming2,3 with evident impacts on terrestrial ecosystems and the two native Antarctic vascular plants Deschampsia antarctica Desv. and Colobanthus quitensis (Kunth) Bartl.4-10 Subsequently, a short but intense cooling occurred from the Antarctic Peninsula to the South Orkney Islands (1999-2016),1,11-13 impacting terrestrial ecosystems, with reduced lichen growth14 and no further expansion of D. antarctica in the Argentine Islands.5 The strong warming trend is predicted to resume15 with expansion of ice-free areas and continued impacts on the abiotic and biotic components of terrestrial ecosystems including the ingression of non-native species3,8,16,17 as recently recorded at Signy Island (South Orkney Islands).18-20 In this study we document acceleration in the expansion of D. antarctica and C. quitensis in the last decade (2009-2018) at Signy Island, where the air temperature warming trend resumed in summer after 2012. We hypothesize that the striking expansion of these plants is mainly triggered by summer air warming and release from the limitation of fur seal disturbance. We also hypothesize that the "pulse" climatic event of the strong air cooling detected in 2012 did not appear to influence the vegetation community dynamics on this island. This is the first evidence in Antarctica for accelerated ecosystem responses to climate warming, confirming similar observations in the Northern Hemisphere. Our findings support the hypothesis that future warming will trigger significant changes in these fragile Antarctic ecosystems.

Animals possess neuronal circuits inducing stress to avoid or cope with threats present in their surroundings, for instance, by promoting behaviors, such as avoidance and escape. However, mechanisms must exist to tightly control responses to stressors, since overactivation of stress circuits is deleterious for the wellbeing of an organism. The underlying neuronal dynamics responsible for controlling behavioral responses to stress have remained unclear. Here, we describe a neuronal circuit in the hypothalamus of zebrafish larvae that inhibits stress-related behaviors and prevents excessive activation of the neuroendocrine pathway hypothalamic-pituitary-interrenal axis. Central components of this circuit are neurons secreting the neuropeptide Galanin, as ablation of these neurons led to abnormally high levels of stress. Surprisingly, we found that Galanin has a self-inhibitory action on Galanin-producing neurons. Our results suggest that hypothalamic Galanin-producing neurons play an important role in fine-tuning stress responses by preventing potentially harmful overactivation of stress-regulating circuits.