Current Biology

The ability of flying insects to locate distant food and mates by tracking odor plumes through turbulent and unsteady flow represents a remarkable feat of sensorimotor integration. Successful navigation requires not only extracting a reliable directional estimate from an intermittent olfactory signal, but also contending with the challenging dynamics of variable winds. While prior work has established that insects integrate the history of odor encounters to shape search decisions, whether they also retain a working memory of recently experienced wind conditions has remained unknown. Here, we use optogenetics combined with controlled wind perturbations in a free-flight wind tunnel to investigate how wind history modulates the olfactory search behavior of Drosophila melanogaster. By introducing lateral "gust" flow via auxiliary fans and independently delivering olfactory stimuli, we show that the wind experienced during an olfactory stimulus shapes both the immediate surge response and the subsequent spatial search. Flies that received an olfactory stimulus while being displaced by a crosswind gust were significantly more likely to return to the gust zone during the post-stimulus search phase compared to flies that received the same odor cue in steady laminar flow. Meanwhile, surge responses and course directions exhibited during search indicate that moment-to-moment flight kinematics may be driven more by instantaneous flow. These results reveal that wind experience is tracked in addition to olfactory experience, and provide evidence that Drosophila maintain a short-term working memory of ambient wind conditions to guide olfactory navigation.

Pennaceous feathers are fundamental to avian flight, yet their early function in non-volant dinosaurs remains unknown. Early-diverging pennaraptorans had simple pennaceous feathers on proto-wings and tails, which were unsuitable for flight but may have enhanced visual signals. However, the visual display hypothesis has not been empirically tested. To address this, we used computer animations of early pennaraptoran displays to measure responses in a well-established animal model of a visually sensitive neural pathway. We show that pennaceous proto-wings and tails enhance the efficiency of motion-based displays across a range of anatomically plausible movements. Integrating these results with comparative and paleontological evidence, we suggest that early pennaceous feathers functioned in diverse signaling contexts and were subsequently exapted for aerodynamic use.

Many animals navigate their world largely by seeing and feeling it. To disentangle these visual and mechanosensory contributions, we developed a virtual reality assay targeting the optomotor response in adult wild-type zebrafish swimming against flow. By projecting dynamic visual patterns onto the walls of a variable-speed flow tank, we decoupled wide-field optic flow from hydrodynamic velocity. We then tested fish responses to abrupt visual perturbations while they held station in the unsteady wake behind a bluff body. These perturbations reliably elicited compensatory optomotor responses, with fish aligning to the direction of the moving stimulus. Notably, this behavior was absent in uniform flows, suggesting that fish prioritize visual input when predictive lateral line signaling is compromised. We propose that this sensory shift serves to optimize swimming energetics in turbulent wakes. Extending this framework, we further show that zebrafish swimming against flow, whether alone or in groups, exhibit heightened escape responses to looming visual stimuli. Together, our findings reveal that fish sensory strategies are not fixed but dynamically tuned to hydrodynamic context: favoring visual cues in turbulent environments and lateral line input in uniform flows. Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=84 SRC="FIGDIR/small/715425v1_ufig1.gif" ALT="Figure 1"> View larger version (18K): org.highwire.dtl.DTLVardef@1d7ba00org.highwire.dtl.DTLVardef@1f456f1org.highwire.dtl.DTLVardef@7826c4org.highwire.dtl.DTLVardef@391a68_HPS_FORMAT_FIGEXP M_FIG C_FIG

The vascular system is central to plant ecology and evolution. Here, we show that more than 100 species across 27 genera and four subfamilies of Fabaceae have evolved atypical vascular architectures and that these species occur in all biogeographical regions except Antarctica. Because Fabaceae includes many ecologically and economically important species exhibiting these novel vasculatures, the family emerges as an ideal system for assessing the implications of vascular innovation in both fundamental and applied research.

How photosynthetic endosymbionts reorganize host daily regulation remains unclear. Paramecium bursaria displays pronounced day-night behaviors, but whether its algal symbionts drive host temporal programs has been unresolved. We compared host gene expressions across a 24-hour light-dark cycle in symbiotic and aposymbiotic cells. Symbiotic cells exhibit an expanded and highly temporally ordered diel transcriptome compared with aposymbiotic cells. These rhythmic programs encompass motility, signaling, metabolism, and growth regulation, consistent with observed behaviors. Symbiosis-associated rhythmic programs recruit gene families encoding post-translational regulatory domains, including kinases, ubiquitin-related factors, WD40 scaffolds, and calcium-binding proteins, despite lacking recognizable canonical clock genes. Disrupting photosynthesis with paraquat altered these temporal profiles, shifting them toward an aposymbiotic-like state. A distantly related ciliate, Tetrahymena utriculariae, with an independently evolved symbiosis, showed similar symbiosis-associated daily programs, suggesting that photosynthetic endosymbionts can act as important organizers of host daily gene regulation in endosymbiotic protists.

Visual experience is organized in time. When riding the same bus route each day, the visual scene unfolds in a predictable order without requiring active choice. During goal-directed behavior, individuals organize actions into routines, such as repeatedly walking the same route to work even when alternatives are equally efficient. Because experience unfolds across sequences of events, identifying how it reshapes population activity requires examining representations over time. Many studies have shown that repeated experience reduces mean firing rates in visual cortex1-14. While firing rates effectively signal novelty or repetition, they are not well positioned to describe how populations of neurons represent temporal relationships. A growing body of work suggests that the geometry of population activity provides additional insight into how visual information is structured and read out15-26. We examined how experience with temporal structure reshapes the geometry of population activity in visual area V4. We recorded neuronal populations across three contexts that varied in temporal structure and behavioral relevance: repeated presentation of individual images, passive exposure to structured image sequences, and repeated execution of self-chosen visually guided action sequences for reward. Across contexts, experience constrained population responses toward a typical activity pattern. In sequence contexts, experience made temporal position more linearly accessible and, during active practice, increased the separability of task-relevant variables. These findings show that experience reorganizes the geometry of visual population activity to reflect temporal structure, constraining responses and altering how sequence-related information is represented.

Spiders (Araneae) are responsible for one of the most captivating and intricate examples of animal architecture in the natural world: the web. But only certain groups of spiders weave the familiar spiral-shaped orb web, and the evolutionary origin of orb-weaving has left arachnologists tangled in a debate for the past decade. Since phylogenetic studies rejected the long-held belief that orb-weavers were monophyletic, two competing hypotheses have emerged: that the cribellate (dry) and ecribellate (sticky) orb webs arose independently and convergently, or that the ability to weave the orb originated with web-spinning common ancestors of all extant orb-weavers and was subsequently lost in many non-orb-weaving descendants. Attempts to reconstruct the ancestral state of the orb web have reached conflicting conclusions as a result of disagreements about the species phylogeny and the definition of orb-weaving. As a potential solution to this phylogenetic impasse, we tested orthologous genes from across the genomes of 98 species of spiders for evidence of both convergent positive selection and relaxed selection corresponding to the orb-weaving phenotype, the patterns that we would expect to be caused by each of the competing hypotheses on the origins of the orb. Using a permutation-based approach, we also compared the odds of gene loss and duplication between orb-weavers and non-orb-weaving spiders and identified genes whose copy number differ significantly between the two phenotypic groups. Through these analyses, we integrate the evolutionary history and genetic basis of orb web-associated traits, providing unique insights into the emergence of complex behavior.

Smell allows animals to find food, avoid danger, and communicate through the binding of odorants to chemosensory receptors on olfactory sensory neurons. The vision-priority hypothesis predicts an antagonistic relationship between olfaction and vision, in which olfactory ability increases as visual acuity decreases along evolutionary lineages, a tradeoff that often occurs through expansion and contraction of chemosensory receptor gene families. The Mexican tetra (Astyanax mexicanus), a fish species with both sighted surface-dwelling and blind cave-dwelling populations, presents an ideal model for exploring the mechanisms underlying this tradeoff. Here we show that although cavefish can sense odorants at lower concentrations than surface fish, they do not have an expanded repertoire of chemosensory receptors, increased sensory neuron number or density, or enhanced expression of receptors compared to surface fish. Instead, cavefish have physiological adaptations to the olfactory epithelium, including more motile cilia and decreased flow rate through the olfactory pits. Pharmacological attenuation of flow rate in the olfactory pits in surface fish increased visits to the odorant source, suggesting that the reduced flow rate in cavefish is an adaptation leading to better foraging. This unexpected evolutionary path to enhanced olfaction as a compensation for loss of vision underscores the need for mechanistic understanding of comparative genomics.

Medusozoan cnidarians (e.g., jellyfish) metamorphose from a benthic juvenile polyp into a pelagic adult medusa, providing a well-known example of a clade that uses tissue remodeling to create distinct juvenile and adult body plans. Staurozoans (i.e., stalked jellyfish) are an atypical lineage of medusozoans that have lost their medusa stage; thus, their juvenile and adult body plans look remarkably alike. Their limited metamorphosis is characterized by the regression of primary (juvenile) tentacles and the development of secondary (adult) tentacles. In some staurozoan lineages, metamorphosis also involves development of novel adhesive structures (anchors), which are built on top of the regressing primary tentacles. Understanding how cells are partitioned from making juvenile tissues to making adult tissues is important for understanding how animals can make adult structures in the absence of complete metamorphosis. We compared the abundance and distribution of proliferative cells in tissues undergoing regression (primary tentacles) and development (secondary tentacles and anchors) during the juvenile to adult transition in the San Juan Island stalked jellyfish, Haliclystus sanjuanensis. We show that proliferative cells are lost in regressing primary tentacles but are gained in anchors, consistent with a shift in investment from juvenile to adult tissue. Prior to regression, primary and secondary tentacles show similar patterns in their proliferative cell distribution and in the identity of their cnidocytes (stinging cells), indicating that adult tentacles are made by re-deploying a juvenile tentacle program. Finally, we demonstrate that unlike secondary tentacles, primary tentacles cannot regenerate, illustrating that the temporary investment in this tissue is tied to their loss of proliferative cells. Thus, we propose that continued investment in a population of proliferating cells is an important mechanism for segregating temporary tissues (primary tentacles) from long-term tissues (secondary tentacles). These observations of cell dynamics in H. sanjuanensis suggest that temporary investment into juvenile structures may be used to pattern novel adult tissues, providing an important mechanism for diversifying adult body plans.

In afoveate species such as mice, it is accepted that gaze is typically redirected by head movements with a saccade-and-fixate strategy, while the eyes primarily stabilize vision within a limited oculomotor range. This view suggests that the accompanying eye movements are primarily reflexive, driven by mechanisms like the vestibulo-ocular reflex (VOR). However, emerging evidence challenges this assumption, suggesting that eye movements during active head motion may not be purely reflex-driven. Here, we directly test whether eye movements in mice are actively coordinated as part of voluntary gaze redirection rather than being reflexive. By systematically monitoring head and pupil positions during goal-directed orienting in a cohort of male mice, we find that mice generated active saccadic eye movements whose onsets are tightly linked to head movements. Furthermore, these saccadic eye movements occur at markedly shorter latencies than reflexive quick-phase eye movements evoked by comparable passive head rotations. Importantly, the interplay between coordinated eye and head movements during voluntary orienting resemble the predictable, stereotyped gaze patterns seen in foveate animals, such as primates. Our results suggest that mice possess an evolutionarily conserved mechanism for gaze redirection, integrating voluntary eye-head coordination similar to that of foveate vertebrates. These findings reframe the prevailing view by demonstrating an actively coordinated eye-head component to gaze redirection under goal-directed conditions in mice, complementing established reflexive mechanisms.

Microtubule networks are major determinants of cell architecture and logistics. Microtubule organization and density are regulated by severing enzymes, which cut microtubule lattices or affect their growth and shortening. These activities can lead to microtubule amplification or disassembly, depending on the presence of microtubule stabilizers or destabilizers, but the interplay between these factors is poorly understood. Here, we reconstituted in vitro the activity of microtubule severase katanin together with microtubule minus-end stabilizers CAMSAPs, their binding partner WDR47 and microtubule depolymerase kinesin-13/MCAK. We confirmed that katanin can amplify or destroy microtubules in a concentration-dependent manner. CAMSAPs recruit katanin to microtubules and reduce katanin concentration needed for both amplification and destruction, whereas kinesin-13 completely abolishes microtubule amplification. WDR47 binds to microtubules decorated by CAMSAPs and suppresses katanin binding and severing. In addition, both katanin and WDR47 inhibit polymerization of CAMSAP-decorated microtubule minus ends. These data explain how these proteins act together to fine-tune microtubule minus-end stability without strongly increasing microtubule abundance. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=169 SRC="FIGDIR/small/714132v1_ufig1.gif" ALT="Figure 1"> View larger version (20K): org.highwire.dtl.DTLVardef@746fe3org.highwire.dtl.DTLVardef@5dd5a8org.highwire.dtl.DTLVardef@762373org.highwire.dtl.DTLVardef@1192db_HPS_FORMAT_FIGEXP M_FIG Graphical abstract C_FIG

Crop domestication is an evolutionary process that has led to extraordinary plant phenotypic changes in response to artificial selection. The extent to which domestication has altered floral phenotypes and the implications of these changes for plant-pollinator interactions remain unclear. Here, we characterized the floral phenotypes of wild and domesticated species in the genus Cucurbita (squash and pumpkins) and quantified their relative attractiveness to generalist and specialist pollinators. Our results show that functional floral traits change with domestication and that some of these changes impact the visitation of generalist pollinators but not specialists. Crops displayed larger flowers with shorter anthers and wider corollas, lower volatile richness, higher sugar content in pollen, and lower sucrose:glucose ratios in nectar. These trait shifts were associated with pollinator behavior in generalist pollinators, which preferentially visited domesticated flowers. We demonstrate that domestication alters functional plant traits and that these changes affect generalist pollinator preference in agricultural settings.

Hippocampal pyramidal neurons function as place cells, showing location-specific activity during navigation, to form an internal spatial map of the environment. They are hypothesized to be the neural substrate of episodic memory. However, place cell receptive fields tend to drift or have poor tuning in low demand tasks, lacking operant goals such as random foraging, or in sensory context-deprived environments. Through chronic two-photon calcium imaging of hippocampal area CA1, we directly compare stability in a low versus a high demand task within the same animals over the course of learning and recall in the same environment. We find that compared to random foraging, an odor-context based navigational task stabilizes place cell representations and increases place cell quality and quantity. To investigate the circuit mechanism that may support this stability, we manipulated the activity of lateral entorhinal cortex (LEC) excitatory neurons, which provide both indirect and direct multisensory inputs about context, odor, and time to CA1. We chemogenetically suppressed activity of excitatory neurons in LEC during recall of the odor-context based navigation task and found that context discrimination is impaired at both the behavioral and neural level. With LEC silencing, mice had lower behavioral performance, less stable population activity, and greater similarity between opposing trial types. Our study finds that increasing task demand increases CA1 stability and that this stability is partially supported by LEC.

Colonial animals composed of clonally produced units can achieve a high degree of functional integration, challenging the distinction between an individual and a higher-order organism. Siphonophores (Cnidaria: Hydrozoa) exemplify this condition, forming highly organized colonies in which genetically identical zooids are specialized for functions such as locomotion, feeding, and reproduction, and are precisely arranged along a shared stem. All zooids arise from two spatially separated budding zones, the nectosomal and siphosomal growth zones, suggesting that positional information along the stem patterns colony organization at the level of the colony rather than individual zooids. However, the molecular basis of this colony-level axial patterning remains poorly understood. Here, we analyze gene expression along the stem of the siphonophore Agalma okenii using RNA sequencing and in situ hybridization chain reaction (HCR). We show that conserved developmental regulators, including Hox and Wnt pathway genes, exhibit region-specific expression corresponding to distinct budding zones and zooid distributions. These results indicate that canonical axial patterning systems are deployed at the level of the colony axis. Our findings demonstrate that developmental gene networks classically associated with anterior-posterior patterning can operate at a higher level of biological organization, providing a mechanistic framework for the evolution of integrated, superorganism-like body plans in colonial animals.

Understanding the repeatability of evolution requires disentangling the roles of constraint, contingency, and convergence in shaping phenotypic diversity. Mullerian mimicry in Heliconius butterflies offers a powerful natural experiment, with co-occurring species independently evolving similar wing color patterns under shared selective regimes. Here, we integrate high-throughput image-based phenotyping, genome-wide association studies (GWAS), and comparative pan-genomics to investigate the genetic architecture underlying convergent wing pattern evolution across parallel hybrid zones in Heliconius erato and H. melpomene. Using automated computer vision pipelines, we extracted and quantified color pattern variation from over 650 butterfly specimens. Principal component analysis (PCA) of recolorized, landmark-aligned wing images captured biologically meaningful axes of variation, which were used as phenotypes in GWAS. We identified strong associations at known patterning loci--including ivory:mir193 (previously coretex), optix, WntA, and vvl--as well as novel regions, including a chromosome 2 inversion in H. erato and a gustatory receptor gene (Gr21a) in H. melpomene. Comparative analyses using a Heliconius pan-genome revealed that while significant associations mapped to homologous regulatory regions across species, the specific variants were lineage-specific, consistent with parallel evolution via distinct cis-regulatory changes. These findings demonstrate that repeated adaptive outcomes can arise through different genetic paths within conserved regulatory architectures. More broadly, our study highlights the power of integrating machine learning, high-resolution phenotyping, and comparative genomics to dissect the molecular basis of convergent evolution in natural populations.

Septins are cytoskeletal proteins that regulate cytokinesis in fungi and animals, yet their functions in choanoflagellates -- the closest living relatives of animals -- have remained unknown. Salpingoeca rosetta, a choanoflagellate that switches between unicellular and multicellular forms, encodes four septins closely related to animal and fungal septins. CRISPR/Cas9-mediated disruption of S. rosetta septins revealed that a subset regulate cell size, with two mutants exhibiting an elevated frequency of oversized cells and one exhibiting smaller cells. Three of the four septins were required for proper rosette colony development, while two also regulated rosette structural integrity. Characterization of Sros_septA, which showed the strongest phenotype, revealed a role in cytokinesis: mutant cells exhibited late-stage cytokinesis failure, resulting in enlarged, multinucleated cells. Cytokinesis failure rate increased in uninduced Sros_septA mutant cells and was further elevated upon rosette induction, suggesting that the multicellular context places heightened demands on the septin cytoskeleton. Endogenously tagged Sros_SeptA dynamically redistributed from the basal pole in interphase cells to the cleavage furrow and nascent intercellular bridge during cell division. These findings identify septins as regulators of cytokinesis and multicellular development in S. rosetta and offer a framework for exploring how cell division regulation contributed to the emergence of animal multicellularity. Significance StatementO_LISeptins are cytoskeletal proteins that regulate cell division in fungi and animals, but their functions in choanoflagellates - the closest living relatives of animals - were unknown. C_LIO_LIUsing CRISPR/Cas9 gene editing in Salpingoeca rosetta, we show that septins regulate both cell size and multicellular colony development. SeptA, whose gene disruption produced the strongest phenotype, localizes dynamically to the cleavage furrow and regulates cytokinesis, with cell size and division defects that are exacerbated during multicellular rosette development. C_LIO_LIThese findings raise the possibility that elaboration of the extracellular matrix during animal origins imposed new mechanical demands on dividing cells, linking the evolution of cell adhesion to the evolution of cytokinetic regulation. C_LI

Near-extinction events impose severe genomic bottlenecks that can have lasting fitness consequences, yet the specific mechanisms involved remain poorly understood. Alal[a], the endemic Hawaiian crow, narrowly avoided extinction when a conservation breeding program was founded from just nine individuals. Although the breeding program has since recovered to [~]120 birds, it remains plagued by egg hatching failure rates >50%. To investigate the impacts of this bottleneck on hatching failure and other fitness components, we generated a chromosome-level reference genome and resequenced 175 individuals, including 78 deceased embryos. Although long runs of homozygosity (ROH) >1Mb are abundant in Alal[a] (mean FROH=0.32), associations between FROH and measures of survival and reproduction, including egg failure, were weak or nonexistent. Instead, we identify two recessive lethal haplotypes that together account for [~]20% of all hatching failures and have persisted in the population at high frequency (15-25%), hinting at impaired purifying selection. Eco-evolutionary simulation models demonstrate that these limited impacts of ROH and elevated recessive lethal allele frequencies are expected for a species that has endured a severe population bottleneck and exhibits modest levels of non-ROH heterozygosity. Our findings suggest that elevated recessive allele frequencies may be a broadly important consequence of population bottlenecks.

Sexual signals are thought to reflect metabolic capacity, allowing females to assess male genetic quality. In insects, cuticular hydrocarbons (CHCs) are central to mate recognition and sexual signalling, and their biosynthesis is directly tied to mitochondrial metabolism. Because mitochondrial performance requires coordination between the mitochondrial and nuclear genomes, non-compatible genomes may disrupt CHC production and reduce male attractiveness. We tested this prediction using a global Drosophila melanogaster mitonuclear panel comprising 80 cybrid genotypes. Multivariate analyses of male CHC profiles revealed strong nuclear effects, smaller but significant mitochondrial effects, and substantial non-additive mitonuclear interactions that accounted for ~10% of the variance after controlling for body mass. These interactions reorganised CHC blends in genotype-specific ways, with certain hydrocarbons contributing disproportionately to differentiation. In behavioural assays, females preferentially mated with males whose mitonuclear genomes were coadapted. Conversely, coadapted males had higher copulation success than males presenting disrupted combinations to the female. Our results demonstrate that mitonuclear compatibility influences the production of sexual signals and shapes reproductive outcomes, linking genomic interactions to mate choice.

1Fleshy fruits underpin a major mutualistic pathway linking plants and birds in Mediterranean scrublands, yet we still lack a mechanistic understanding of how ecomorphological and digestive traits constrain fruit use, foraging behaviour, and ultimately the effectiveness of avian seed dispersal. Here we assemble an integrative dataset for 146 Iberian bird species combining external morphology, digestive anatomy, diet composition, and fine-grained observations of fruit foraging and handling obtained from standardized focal watches and camera traps at fruiting plants. We classify species into five functional feeding groups (seed dispersers, pulp consumers, pulp consumer-dispersers, pulp consumer-seed predators, non-frugivores) and ask how suites of traits map onto these feeding modes and onto quantitative metrics of frugivory and feeding rate. Across species, the proportion of diet volume made up by fleshy fruits increases with gape width and faster food transit, and decreases with larger gizzards and longer intestines, indicating a tight coupling between frugivory and traits that enable rapid processing of dilute, pulp-rich food. A small subset of traits (body mass, gape width, gizzard mass, transit time) explains over half of the interspecific variation in fruit consumption, with ecomorphological and digestive characters contributing roughly equally to explained variance. Per-visit feeding rates and numbers of fruits ingested per visit scale positively with body mass, and canonical discriminant analysis reveals distinct multivariate trait syndromes separating seed dispersers from pulp consumers, seed predators, and non-frugivores. These trait syndromes, and the associated differences in handling mode and feeding speed, provide a mechanistic link between individual-level foraging decisions and the sparsity, asymmetry, and effectiveness of plant-frugivore interaction networks in Mediterranean systems. Our results highlight how trait-based constraints shape not only who interacts with whom, but also how efficiently seeds are removed and dispersed across a diverse frugivore assemblage.

Acquiring nutrients is a fundamental biological process of all organisms, playing crucial roles in ecological sustainability. Diplonemids are highly abundant heterotrophic unicellular flagellates that are widespread in the worlds ocean. They have a highly complex microtubule-based feeding apparatus (cytostome-cytopharynx complex) located adjacent to the deep flagellar pocket from which two flagella emerge from parallel basal bodies. The apical papilla is a tongue-shaped structure unique to diplonemids that connects the cytopharynx and the flagellar pocket, the latter of which is formed by reinforcing microtubules (MTR) and two flagellar roots called intermediate and dorsal roots. Here we report identification of 17 proteins that localize at the feeding apparatus or flagellar apparatus in Diplonema papillatum. Using ultrastructure expansion microscopy, we show that Mad2 and its interaction partner MBP65 localize at the MTR, intermediate root, and dorsal root. Homologs of proteins that associate with the flagellar apparatus in Trypanosoma brucei (PFR2, KMP11, BILBO1) localize at the feeding apparatus in D. papillatum. We also identify proteins that localize at the apical papilla, MTR, parallel microtubule loop, or cytopharynx. By discovering components of the feeding apparatus for the first time in diplonemids, this work forms the foundation to understand molecular mechanisms of the feeding apparatus in these highly abundant marine plankton.