Current Biology

The symbiosis between algae and animals represents a relatively recent evolutionary innovation, and exemplified by species in the Cnidaria phylum. Cnidaria can harbor algae within a modified cellular organelle called the symbiosome in a process called endosymbiosis. This animal-algal symbiosis can be facultative or obligate. Algae acquisition occurs either by horizontal transmission, where free-swimming planula gain algae through feeding, or by algae deposition into the developing oocyte in vertical transmission[1-5]. Most studies focus on anthozoans that perform obligate endosymbiosis and transmit algae horizontally. How facultative endosymbiosis in combination with vertical algal transmission impacts the evolutionary adaptation between host and symbiont remains unclear. By studying Hydra viridissima, which performs facultative endosymbiosis and transmits its Chlorella algae vertically, we define different cell types and identify the endoderm cell lineage that gives rise to three major cell types hosting algae. Compared to obligate endosymbiosis[6, 7], Hydra viridissima algal host cells exhibit distinct features, including algal uptake, elevated oxidative phosphorylation and redox activities, and express genes that can provide ammonium for their algal symbionts. We further show when and how the developing Hydra oocytes may take up algae and where oocytes may obtain lipids. Since Hydra is amenable to genetic manipulations, our findings should enable mechanistic studies of how facultative endosymbiosis and vertical transmission evolve and adapt in a changing climate.

Processing rapid motion while maintaining high spatial acuity is a fundamental evolutionary challenge for the vertebrate visual system. Here, we investigated the structural adaptations enabling aerial insectivores - swifts (Apus apus) and swallows (Hirundo rustica, Delichon urbicum) - to track and capture prey at high speeds. We show that these phylogenetically distinct species share highly specialized temporal foveae that provide sharp frontal vision. Strikingly, this avian specialization converges on primate foveal architecture, featuring cones with long axons and a unique cluster of large, orthotopic ganglion cells (soma area [≥] 200 {micro}m{superscript 2}) surrounding a deep foveal pit. By tracking their large axons, we mapped their neural representation within the optic nerve and tectum. Despite the low abundance of these foveal cells, their substantial tectal magnification reflects high processing demands. This cluster of putative motion-sensitive ganglion cells suggests that foveal neural circuitry links high-acuity vision to rapid temporal processing in these birds.

Parasitic nematodes infect over a billion people worldwide and cause some of the most prevalent neglected tropical diseases1-5. Many of these parasites are skin penetrating and have both extra-host life stages that inhabit host feces and surrounding soil, and intra-host life stages that inhabit host niches such as skin, vasculature, and intestine2,6-8. Across life stages, these parasites encounter oxygen (O2) levels that range from ~21% at the soil-air interface to near-anaerobic levels in the host intestine9-12. However, whether parasitic nematodes detect and respond to changes in O2 levels was unknown. Here, we examine O2 sensation in skin-penetrating parasitic nematodes and find that they show robust responses to changes in O2 levels. Moreover, their O2-evoked behaviors differ from those of the free-living nematode Caenorhabditis elegans. We then investigate the molecular and neural mechanisms of O2 sensing in Strongyloides stercoralis, a genetically tractable human-infective nematode, and find that parasite-specific behavioral responses to O2 arise in part from evolutionary changes in their soluble guanylate cyclase repertoire. Finally, we find that neuronal O2 sensing regulates intra-host development in S. stercoralis. Our results demonstrate that skin-penetrating nematodes exhibit neuronally mediated O2 responses that are critical for multiple steps of their parasitic life cycle.

Long-term neuronal plasticity is driven by activity-regulated gene (ARG) expression programs that encode stimulus features in a neuron type-specific manner 1-6. ARG programs are typically characterized by rapid induction of immediate early genes (IEGs) without requiring new protein synthesis, followed by induction of secondary response genes regulated by IEG-encoded transcription factors 2,5,7-14. However, the molecular mechanisms that pattern these programs in specific neuron types in vivo in response to physiological stimuli remain unclear. We previously showed that temperature regulates an ARG program in the C. elegans AFD thermosensory neuron pair to drive behavioral plasticity 3,15,16. Here, by profiling AFD following temperature upshifts of varying durations, we show that ARGs in this neuron exhibit distinct temporal trajectories. Notably, rapidly induced genes do not include known IEGs but are enriched for molecules implicated in signal transduction and navigation. Both rapid and delayed ARG expression require the CMK-1 CaMKI kinase and CRH-1/CREB transcription factor, with CRH-1 acting at both early and late stages. We further define a temporal regulatory cascade in which CREB-dependent induction of the RCAN-1 calcineurin regulator acts in parallel with the MEF-2 transcription factor to repress expression of a delayed ARG at early timepoints. Subsequent downregulation of RCAN-1 likely enables CRH-1-dependent ARG expression at later stages. Our results demonstrate that in addition to classical gene-activating transcriptional cascades, ARG-controlled repressive mechanisms also operate to precisely shape the temporal dynamics of an ARG cascade in a sensory neuron type in vivo, and suggest that distinct cell type-specific regulatory pathways may operate across neuron types to drive ARG expression programs.

Syntax was long considered to distinguish human language from other vocal systems, with parallels in non-human animals historically limited to song. However, song lacks discrete meaning, which is a crucial pre-requisite of linguistic syntax. Over the last two decades evidence of combinatoriality in the discrete, semantic calls of an array of taxa has accumulated, providing the opportunity to investigate potentially closer parallels to language. However, most examples remain limited to small repertoires of simple two-call sequences, preventing evidence of complex internal structuring like that seen in human sentences. The recent discovery that several species produce extensive repertoires of much longer call sequences, has provided the opportunity to investigate the full extent of syntactic structure in non-human call systems. Here we demonstrate that Western Australian magpies (Gymnorhina tibicen dorsalis) use multi-level structured ordering rules within their semantic call sequences and that these ordering rules are learned during development. Specifically, we find that calls within sequences up to 15 calls long depend on the two calls given prior and that independently produced segments ( phonemes), calls, and sequences recombine into longer structures, indicating hierarchical organisation. This represents the first evidence of multi-level non-adjacent organisation and learned syntactic structure in a semantic non-human system.

How animals evaluate reward quality is a fundamental question in neuroscience and behavioral biology. Here we show that in honey bees (Apis mellifera), the value of a sucrose reward is not processed in absolute terms but relative to prior experience, and that this subjective evaluation strongly influences long-term memory formation. Using appetitive olfactory conditioning of the proboscis extension reflex (PER), we demonstrate that memory performance is determined by the contrast between a previously experienced reward and the reward used during training, rather than by the absolute concentration of sucrose received. This effect operates across multiple timescales, from contrasts between successive trials within a single session to differences between rewards experienced 24 hours apart. We further show that prior exposure to sucrose solutions of different concentrations modulates gustatory responsiveness and alters the sensitivity of antennal gustatory receptor neurons, suggesting that peripheral sensory plasticity contributes to experience-dependent changes in reward evaluation. Dissociating pre- and post-ingestive reward components revealed that the contrast between the sucrose concentration sensed by the antennae and the concentration ingested is sufficient to modulate memory formation. Together, our results indicate that bees form an internal expectation of reward quality based on experience, and that this expectation rescales the perceived value of subsequent rewards, thereby shaping associative memory strength. These findings provide a mechanistic framework for understanding how invertebrates perform relative reward comparisons across multiple temporal scales, with implications for flexible foraging strategies in dynamic environments.

O_LIMechanical interaction between guard cells and epidermal pavement cells enables large stomatal apertures and high productivity in angiosperms. We do not know when this response evolved, but over the last 169 years we have found that mechanical advantage has been tested in at least 230 species from 85 families. To date no data on this trait exists among angiosperms outside magnoliids, monocots and eudicots. C_LIO_LITo resolve the evolutionary origins of this critical stomatal response we tested for mechanical advantage across 14 additional species including the earliest diverging lineages of angiosperms. C_LIO_LIWe find that mechanical advantage, while variable in magnitude, is present in all angiosperm species that have been measured, including Amborella trichopoda sister to all angiosperms. C_LIO_LIThis response likely evolved once in flowering plants, in the common ancestor of this clade, remaining widespread across angiosperms today. We hypothesize that angiosperms could not have realized the full potential of physiological innovations in water transport without the evolution of this key trait that increased operational stomatal aperture. C_LI

Animals must adapt locomotion to changing environments, but how the nervous system flexibly select gait remains unclear. Gravity is a powerful natural perturbation altering body loading and limb dynamics. Apollo astronauts often skipped on the Moon, adopting an asymmetric gait rarely used on Earth, yet the motor control basis of this behavior is unknown. Here, by studying the effect of hypogravity on locomotion in humans and mice, we identify a conserved strategy for gait adaptation. Muscle synergy analysis in humans shows that skipping in reduced gravity is generated through flexible reuse of existing motor modules rather than construction of new ones. In mice, lunar gravity elicited a skipping-like asymmetric gait and genetic elimination of muscle proprioceptors abolished it. Thus, hypogravity reveals a proprioception-dependent mechanism for flexible gait selection.

Mosquitoes are classified into two subfamilies, each monophyletic, and typically considered to both be ancient, having diverged more than 100 million years ago based on previous divergence analyses. A recent publication challenged this view with phylogenomic results primarily from the third codon position and UCEs. Utilizing alternative fossil placement and these phylogenomic data, these authors find that the Culicidae and Chaoboridae diverged in the lower Cretaceous, and that one mosquito subfamily, the Anophelinae, is nested within the Culicinae. These results are in stark contrast to previous results from diverse data sources, ranging from other genomic data, to morphology, to fossils. Here, we briefly detail the substantial evidence that supports two monophyletic subfamilies of extant mosquitoes, along with fossil evidence that supports the ancient divergence of these lineages.

In an early phase of life, most animals are behaviorally and physiologically not yet able to reproduce but show adaptations specific to a juvenile state. In Drosophila females, sexual maturation after metamorphosis is achieved by acquiring receptivity to male courtship and completing oogenesis, a transition that is under hormonal control and requires coordinates changes in the nervous system. Here, we show that immature females display a transient signaling behavior during the time window of asexuality by flicking their wings in response to and dependent on male courtship stimuli. Immature wing flicks require the activity of Doublesex (Dsx) expressing central brain pC1a neurons that mediate receptivity in mature virgins. Immature wing flicks generate patterned sound pulse trains that differ from other intraspecific acoustic signals, but resemble pulses produced during mature male agonistic interactions. Courting males exposed to immature flicks shorten courtship singing and abstain from copulation attempts, indicating that immature wing flicks serve as an effective rejection signal of asexual females to minimize futile male mating pursuits.

Acetylcholine (ACh) release from the basal forebrain has traditionally been viewed as a slow, spatially diffuse signal regulating cortical arousal across sleep and wakefulness1-3. Recent characterizations with higher resolution optical sensors have revealed rapid, local cholinergic modulation supporting dynamic changes in sensory processing, associative learning, and behavioral state4-7. However, sensory events that recruit cortical ACh often also change arousal and evoke movements, making it difficult to determine whether ACh transients reflect sensory features of environmental stimuli or the behavioral state changes that accompany sensory stimulation. To separate these contributions, we performed optic fiber recordings of a genetically encoded ACh fluorescent sensor in the auditory, visual, and prefrontal cortex of awake, head-fixed mice while monitoring pupil size and facial movements. Across cortical areas, ACh release tracked spontaneous fluctuations in arousal state, as indexed by pupil dilation and orofacial movements. Sensory stimuli also evoked rapid ACh transients, with sounds producing larger and more widespread responses than visual stimuli. Because sounds also elicited time-locked pupil dilations and facial movements, we used multivariate modeling to estimate the relative contributions of stimulus features, arousal, and behavior to cortical ACh dynamics. We identified a regional dissociation: sound-evoked ACh release in prefrontal cortex was largely explained by arousal- and movement-related variables, whereas auditory cortical ACh release retained a stronger relationship to stimulus features. These findings show that cortical ACh signaling reflects both shared arousal state and area-specific sensory processing and demonstrate that sound is especially effective at recruiting rapid, widespread cholinergic modulation across cortex.

Cells harness the actomyosin contractility of the cell cortex to drive rapid cellular deformations and intracellular flows during cell polarization, migration, and division. To sustain contractile network architectures while allowing for network deformation and remodeling, the balance of actin filament assembly and disassembly must be finely tuned, but how this is coordinated in the cell remains obscure. Here, we combine quantitative measurements and manipulations of filament assembly and disassembly rates with live imaging of network contractility dynamics in the C. elegans zygote to identify co-dependencies between assembly rates, disassembly rates, and large-scale deformations of the cortical actin network. We find that strong reductions in either filament assembly or disassembly rates both result in actin cortex collapse, but each perturbation has distinct effects on actin cortex and cell membrane dynamics. These findings demonstrate that rapid turnover, involving tightly coordinated assembly and disassembly, allows the cortex to maintain a connected architecture while undergoing rapid deformation and coherent flow.

Understanding how cells specialize is essential for reconstructing the diversification of life on earth. Cnidocytes (stinging cells) have a single origin in the stem cnidarian ([~]800mya) and have since specialized into extremes in morphology and function. Using single-cell RNA sequencing and transcriptional lineage reconstruction in a coral and a sea anemone, we show that a single gene (FoxL2) controls a critical switch point in the evolution of cnidocyte diversity: the decision to be a piercing cell or an ensnaring cell. Surprisingly, ensnaring cells are one of the most highly conserved differentiated cell types. This suggests spirocytes reached an adaptive peak early and have changed little during the 600 million years since corals and sea anemones last shared a common ancestor, making them living fossil cells.

Corals form important ecosystems that serve as habitat for numerous marine species. Being sessile, adult corals are exposed to changing environments without the means to relocate. Species dispersal is therefore restricted to the motile larval lifestage. How do microscopic larvae achieve reliable dispersal and conquest of novel habitats under time pressure and unpredictable environmental conditions? Here we show an unexpected diversity of behaviors in the cold-water coral Lophelia pertusa. Anatomical and behavioral changes of coral planula promote a change from neutral, passive buoyancy in the dispersal phase, to active swimming and search behavior during competency. As lipids are metabolized and sensory abilities develop, the coral larvae drastically change their motility patterns. Comparative analysis with a poorly dispersing, lecithotrophic anthozoan larvae reveals that developmentally timed sensory integration is conserved between species, but the behavioral modes and sensory responses are adapted to their particular ecology.

Habits are automatic actions shaped by prior experience, enabling efficient and fast responses in stable environments. While habitual gaze rapidly directs the eyes toward valuable objects, the mechanisms underlying habitual manual choice for reaching and grasping remain unclear. Here we show that macaque monkeys develop habitual manual choices toward previously rewarded objects through multi-day object-value learning, driven by learned value and spatial preferences. This reaching habit persisted without reward and showed shorter latencies than in value-deliberative tasks, consistent with automatic control. Regression analyses further revealed that manual choice was guided by learned object values, whereas visual salience had no effect, unlike gaze habits. Instead, intrinsic spatial preferences continued to bias reaching behavior even after long-term value learning. These findings demonstrate that habitual manual choice arises from the integration of spatial preferences and long-term value memory, defining a distinct mechanism of automatic behavior beyond habitual gaze.

Temporal niche partitioning is a strategy for reducing interspecies competition and strengthening reproductive isolation. It relies on animals confining their daily activity to distinct diurnal, crepuscular, or nocturnal windows. However, a hardwired temporal niche is only advantageous under stable, predictable ecological regimes; surviving dynamic environments demands behavioral flexibility. Yet, it remains unclear how animals override rigid biological constraints to rapidly exploit transiently available fitness-critical time windows. To address this, we leveraged the twilight-active, species-rich Drosophila genus and monitored their daily activity under naturalistic conditions. Here, we show that intense sociosexual interactions rapidly drive a species-specific reformatting of their canonical crepuscular niche. The dominant sensory modality used for sexual communication predicts niche shift direction: reliance on chemosensation for courtship redirects behavioral activity into the night, while visual reliance shifts it into the day. This temporal plasticity bypasses the circadian clock, instead operating via a conserved dopaminergic pathway. Dopamine operates a dual-output brain circuit that simultaneously inhibits sleep and sustains sexual motivation. Our results reveal how mating imperatives decouple behavioral timing from circadian command, enabling conditional colonization of otherwise restricted temporal windows. Ultimately, by driving the divergence of previously overlapping niches, sociosexually induced temporal plasticity provides a powerful mechanism for sympatric coexistence in crowded environments.

For most Drosophila species, the firm surface of intact ripe fruit acts as a physical barrier to oviposition, effectively restricting them to the saprophagous niche. How species overcome such mechanical constraints at the behavioral and sensory levels, and whether doing so leads to niche breadth expansion or niche specialization, remain poorly understood. Here we show across ten Drosophila species that substrate physical hardness is a critical barrier preventing most species from exploiting ripe fruit. Unlike saprophagous species, the pest D. suzukii and the widely distributed D. immigrans have evolved a tolerance for high substrate stiffness to perform puncture oviposition. This behavioral shift is enabled by distinct morphology of saw-like and needle-like ovipositors respectively, which are critical for breaching intact fruit. To uncover the neural basis for this mechanical adaptation, we screened mechanosensory mutants in D. melanogaster and identified the Inactive (IAV) channel as a key sensory gene mediating this behavior. Functional rescue experiments reveal that IAV has diverged in D. suzukii and D. immigrans, mediating a sensory relaxation that permits oviposition on stiff substrates. This mechanical breach confers a direct fitness advantage, allowing only the offspring of these two species to successfully complete larval development in fresh fruit. Finally, field surveys in the wild demonstrate that this modular adaptation facilitates niche overlap and resource partitioning in natural habitats. Overall, this work reveals how the divergence of mechanosensory channels and morphological innovations can overcome physical constraints to drive broad ecological niche expansion.

Songbirds, such as Bengalese finches (Lonchura striata domestica) produce syntactically organized vocal sequences, composed of individual syllables strung together in variable order. Adult birds can learn to modify transition probabilities between syllables through sequence modification training: when punishing one transition with manipulated auditory feedback, birds will gradually reduce the targeted transition. This protocol is thought to rely on a circuit for vocal-auditory monitoring of the birds own song. Despite the overwhelming usefulness of food rewards for other kinds of trained animal behavior, reinforcing birdsong features with food rewards has remained elusive, possibly because the slow timescale of food reward does not match the fast and precise vocal-auditory feedback loops underlying learned birdsong. Here, we use second-order conditioning to selectively increase the frequency of target transitions in song with food rewards. Bengalese finches learned to associate a delayed primary reinforcer (food delivery by an automated feeder after song ends) with a secondary reinforcer (a short click sound). We then reinforced specific target syllables with the click during ongoing song, leading birds to selectively increase the frequency of the targeted syllable transitions. Learned changes were specific to the target and evident in catch trials without reinforcement, indicative of a learning process. Our results demonstrate that song control circuits can learn from different feedback modalities, including learned associations with food reward.

Cnidae are explosive harpoon-like organelles localized within stinging cells, or cnidocytes, of the phylum Cnidaria (jellyfish, hydroids, sea anemones, and corals). These unique Golgi-derived vesicular structures define the phylum and are prominent examples of an evolutionary cellular novelty. While recent studies have focused on the developmental specification and regulation of cnidocytes more broadly, less is understood about gene expression patterns, structural variations, and toxin repertoires within distinct cnidae subtypes. Here, we determine the transcriptional profile of two major cnidae subtypes in the sea anemone Nematostella vectensis, nematocytes and spirocytes, using the cnidae-specific structural family of proteins called minicollagens. We first define the in vivo expression patterns for three known and three uncharacterized minicollagen orthologs. We show that four minicollagens are broadly expressed throughout ectodermal cnidocytes in developing larvae and primary polyps while two others are restricted to tentacular cnidocytes. Leveraging whole adult scRNA-seq data and two novel transgenic reporter lines, we then demonstrate that the tentacle-restricted cnidocytes are developing spirocytes that are distinguished by expression of the minicollagen NvNcol5. To deepen our analysis of cnidocyte gene expression, we used a customized RNA-FACS-seq pipeline to determine global transcriptional differences between these two subtypes. This approach identified a suite of differentially expressed genes, illuminating spatial and temporal gene expression dynamics across both developing nematocytes and spirocytes. Altogether, our experiments provide fundamental and novel insights into the specialization of cnidarian stinging cells while establishing a rich set of resources for further investigation.

Sleep deprivation alters brain activity and impairs performance, yet many aspects of behaviour are preserved in this state. In the cortex for example, sleep deprivation increases neuronal firing rates and low-frequency oscillatory activity, but cortical circuits continue to process information. Recent work has implicated synaptic inhibition in these changes, with sleep deprivation causing cortical GABAA receptor (GABAAR) signalling to become depolarizing due to changes in chloride gradients that determine the GABAAR reversal potential (EGABAAR). The impact in the intact brain remains unclear, however, as both the degree and effects of EGABAAR changes depend on network activity and intrinsic properties of neurons. To address this, we perform in vivo gramicidin recordings from cortical pyramidal neurons in sleep-deprived mice. We reveal that synaptic EGABAAR is depolarised to values sufficient to support bona fide excitatory GABAAR signalling, through combined network-dependent and cell-autonomous effects. In the face of this depolarizing drive, cortical neurons engage spike threshold adaptation mechanisms that limit their excitability. These opposing effects stabilise activity in simulations of sleep-deprived cortical networks and reproduce the increased firing rates and low-frequency oscillatory activity. This interplay between intrinsic and synaptic mechanisms may help maintain network stability during sleep deprivation, while reducing flexibility for subsequent adaptation.