Current Biology

Cryptic female choice - female-mediated bias in fertilization after mating - is well established in animals and can also occur in plants when multiple pollens compete on the same pistil. However, whether interactions between pollen and pistil tissues after pollen deposition contribute to this process remains unknown. Here, we experimentally test whether such interactions mediate cryptic female choice in the angiosperm Brassica rapa. We quantified fertilization success of pollen donors competing on the same pistil using paternity analyses, and in parallel, made semi-in vivo assays to measure pollen tubes trajectories emerging from the excised styles and growing toward unfertilized ovules for each donor-recipient pair. We show that pollen tube growth towards ovules predicts higher fertilization success under pollen competition. Thus, we document a previously unobserved mechanism of cryptic female choice based on physical interactions between male and female components of reproduction. In addition, different recipient plants favour different pollen donors, consistent with non-directional female choice. Plants with longer styles bias paternities more strongly towards the most successful pollen donor. Overall, our study demonstrates that interactions between pollen tubes and pistil tissues after pollen germination enable plants to bias paternity toward particular donors.

Mammalian circadian rhythms are primarily entrained by light, but nonphotic cues can also reorganize behavioral timing through mechanisms that remain poorly understood. Nocturnal foot shocks delivered to rodents while they forage away from the safety of their nesting area have been shown to entrain circadian behavioral rhythms and shift foraging and feeding to the daytime. To identify the neural circuits underlying this nonphotic fear entrainment, we optogenetically stimulated tachykinin 1-expressing neurons in the parabrachial nucleus (Tac1PBN) during the subjective night while the animals foraged outside of their nest, which recapitulated the total activity-rest phase switch in circadian behaviors induced by foot shocks. Furthermore, selective stimulation of Tac1PBN projections to the central amygdala (CeA) produced a significant but reduced phase shift compared to direct stimulation of Tac1PBN cell bodies. When Bmal1, a core clock gene, was conditionally deleted from the CeA, mice failed to fear-entrain, implicating the CeA molecular clock as a necessary component for fear entrainment. Together, these experiments demonstrate that activation of a defined neuronal population outside of the suprachiasmatic nucleus (SCN) can reorganize circadian behavior by engaging a non-SCN circadian oscillator network that requires an intact CeA molecular clock.

Freshwater biodiversity is disproportionally high relative to the limited availability of freshwater habitats. This pattern is exemplified by freshwater fishes. Over 50% of freshwater fish species are concentrated in a single clade, Ostariophysi, including the 5000 species of minnows, carps, and loaches, the 4500 species of catfishes, and the over 2000 species of tetras, pirahnas, and characins. However, the relationships and ages of ostariophysans remain uncertain. We show that the initial diversification of ostariophysans involved only two freshwater invasions and was driven by the strikingly rapid origination of major crown clades, including Neotropical electric fishes, lutefishes, and multiple major living clades of catfishes, carps and minnows, and tetras and characins, within five million years of the Cretaceous-Paleogene mass extinction. This result is congruent with the record of well-preserved body fossils of ostariophysans, but contrasts with the controversial assignment of isolated teeth and bones from the Cretaceous to nested lineages of this set of freshwater fish radiations. Although we confirm that Alepocephaliformes, an obscure marine lineage, is the living sister to Ostariophysi, our results demonstrate that the former clade only recently invaded the deep ocean, a transition that involved the loss of structures essential for enhanced auditory capabilities in ostariophysans and the related herrings and anchovies. These results establish a surprisingly young age for the major lineages of living freshwater fishes.

Halteres, the miniaturized hindwings of flies, function as biological gyroscopes that encode angular velocity during flight. Although their established role is to detect flight perturbations and trigger compensatory manoeuvers, here we show that halteres also function as a gyrocompass, maintaining an accurate estimate of heading during rapid turns. To overcome the incompatibility between rapid body rotations and two-photon imaging, we exploited the physics of haltere mechano-transduction to reproduce the inertial forces acting on the halteres during rapid body rotations using micron-scale oscillations of the thorax. Our experiments demonstrate that flies update their internal compass during rapid turns by integrating inertial measurements with predictions derived from efference copy signals. Because body saccades exceed the temporal bandwidth of visual motion processing, this inertial computation allows flies to maintain an accurate internal compass throughout these rapid manoeuvres. This capability may enable flies to compute critical parameters such as wind direction and ground speed by comparing measurements made before and after each saccade. Our findings suggest that an ancestral flight-stabilization system was evolutionarily co-opted into a biological gyrocompass, a new function that may have contributed to the adaptive radiation of flies.

When humans speak, we use rhythmic hand and head gestures that are closely coordinated with the temporal structure of speech to emphasize words and phrases. Similarly, human singing is often accompanied by rhythmic body movements that are aligned with the timing and prosodic structure of the vocal sequence. This rhythmic synchronization of bodily gesture with vocal production is thought to be a shared feature of vocal-learning species. How do these two sensorimotor systems develop, coordinate, and synchronize with precise timing to support multimodal communication? The mechanisms underlying this rhythmic entrainment remain poorly understood, and no established animal model to date captures the human combination of speech and co-speech gesture. Here, we show that a vocal-learning songbird, the zebra finch, has evolved song-entrained head gestures. These co-song gestures rhythmically align with acoustically complex song syllables and are developed and produced independently of other innate, stereotyped, song-entangled courtship displays. Even when the song remains largely the same, co-song gestures can be dynamically modulated in rhythm, form, and/or extent across different social contexts. The rhythmic alignment requires auditory feedback, is under the control of a premotor song nucleus, and gradually develops during the sensitive period of vocal learning. Females respond differently when songs and co-song gestures are misaligned, suggesting a social function. This dynamic modulation of co-song gestures provides a behavioral window into brain and cognitive states, making the zebra finch a promising model for understanding the mechanisms underlying rhythmic synchronization of multi-sensorimotor systems and the origin and evolution of co-speech gestures in humans.

The symbiosis with photosynthetic dinoflagellate algae enables corals to build and sustain reef ecosystems. Individual coral polyps hold algal symbionts in their epithelial endoderm cells and lose them under environmental stress, leading to coral bleaching. How the host integrates symbionts into its body plan is not well understood. Here, using a combination of high-resolution imaging, quantitative analysis, and environmental perturbations in the sea anemone Exaiptasia diaphana (Aiptasia) and reef-building coral Pocillopora damicornis, we uncover a spatial organisation of symbionts along the aboral-oral axis of cnidarian polyps that emerges under the long-range translocation of symbionts between host cells through a fluid-filled cavity. The symbiont distribution becomes specifically enriched in the tentacle bud endoderm during Aiptasia polyp morphogenesis. This pattern can form in darkness and with algae-sized inert spheres, suggesting an innate host-intrinsic mechanism. Symbiont-occupied host cells are mechanically constrained within the endoderm and thus unable to rearrange; instead, they go through cycles of symbiont expulsion and re-uptake via the host gastric cavity, with regionally biased rates of these behaviours providing a route to enrich symbionts in the tentacles. Symbiont organisation is remodelled under increased light in adult coral polyps, with a characteristic pattern of reduced tentacle enrichment, lateral clustering and retention in the body column emerging over a timescale of days. Together, our findings reveal that the spatial organisation of symbionts is dynamically regulated in cnidarian host tissues, a capacity that may shape both the establishment of symbiosis and its resilience under environmental change.

The evolution of new traits can drive species diversification by facilitating the use of new resources, but environmental change may turn these same adaptations into liabilities.Trait loss is also often associated with the origin of new ecologies, but how losses modulate diversification remains unclear. The swim bladder allows ray-finned fishes to regulate their buoyancy and exploit ecosystems throughout the water column, yet this organ has been lost many times among species-rich lineages. Here, we show that timing and ecological context control the macroevolutionary effects of swim bladder loss. Many lineages of fishes lost the swim bladder over the last 66 million years as they specialized for benthic habitats where buoyancy regulation is unnecessary. Swim bladder loss enabled the descendants of these benthic fishes to diversify in the deep sea where extreme pressure makes its inflation untenable, and in the frigid, oxygen-saturated Southern Ocean, where loss of the oxygen delivery mechanisms required for swim bladder inflation carries little physiological cost. Yet, we detect a selective filter associated with swim bladder loss during extreme global warming 56 to 50 million years ago, when its absence limited the capacity of fishes to escape ecological disruptions on the ocean floor. These contrasting patterns explain how the loss of a complex trait promoted major ecological transitions without increasing overall diversification through deep time. As human activity drives rapid global warming, the evolutionary legacies of swim bladder loss may again shape the fate of marine fish diversity.

Animals can adapt their behavioral responses to environmental cues by learning from experience. This ability relies on the formation and recall of memories that are shaped by beneficial or detrimental consequences and regulated by the dopaminergic system, which is highly conserved across insect species. In the Drosophila melanogaster larva, eight of total [~]120 dopaminergic neurons (DANs) innervate the mushroom body (MB), a key center for associative memory. This subset of DANs can be anatomically grouped into two clusters of four cells: the primary protocerebral anterior medial (pPAM) cluster, associated with reward signaling, and the dorsolateral 1 (DL1) cluster, associated with punishment. Such a functional dichotomy is observed in larval and adult Drosophila and reflects a fundamental organizational principle of reinforcement learning across invertebrate and even vertebrate species. Aversive reinforcement through high-salt exposure is encoded within the DL1 cluster in a combinatorial and heterogeneous manner, critically involving two neurons, DAN-f1 and DAN-g1. Using temporally precise optogenetic activation and inhibition during olfactory conditioning, we show that these neurons can modulate memory strength and valence. Their effects are most often consistent and predictable, enabling accurate computational modeling of DAN-driven teaching signals. By manipulating the intrinsic physiology of DAN-f1 and DAN-g1 and altering the valence of gustatory input, we are beginning to understand at the single-cell level how dopaminergic activity is systematically adjusted to control memory formation.

Siphonophores are colonial hydrozoans with unprecedented differentiation and specialization, in which individual zooids are transformed into functional organs rather than autonomous polyps capable of feeding. As a result, the entire colony acts as a single, modular-individual with the highest level of coordination and integration, from development through behavior. Deciphering these integrative mechanisms requires understanding the microanatomical organization of the nervous system in all elements of the colony. Here, using two immunohistochemical markers (anti-tubulin and anti-RFamide antibodies), we systematically characterize the neural systems across the entire Nanomia colony, encompassing pneumatophore, stem and all zooid classes (nectophores, gastrozooids, palpons, male and female gonophores, and protective zooids). The use of two neuronal markers enables visualization of distinct neural subpopulations, some of which are not revealed by a single marker. We provide evidence of neuroanatomical interactions within all elements of the colony, including contributions of giant axons, stem polygonal networks, and RFamide-ir neural rings at the base of each zooid, as well as describe different subpopulations of neural networks in the body of various zooids. The presented mapping facilitates identification of novel conductive and signaling pathways for future analysis of the cellular basis of behavioral integration within decentralized, broadly distributed networks and non-neuronal elements of these unique superorganisms.

Highly diversified specialized metabolism enables plant communication with pollinators, herbivores, and protectors1-4. Its chemodiversity, under which evenness, richness and variation is summarized5-7, includes many compounds without known function1-4 and presents an evolutionary conundrum about how and what is selected for8,9. Due to its complexity, it is frequently unknown how it is encoded in genomes. To produce population level chemodiversity, the traits need to allow for highly chemodiverse and highly specific individuals in the same population. Here we use metabolomics, transcriptomics, and genomics combined with field analyses and functional assays of monoterpene synthases in the Asteraceae Tanacetum vulgare (tansy) and identify forces which produce high population level chemodiversity: selection for product specificity in enzymes, loss-of-expression alleles, absence variation, and specialized metabolism islands drive individuals towards low chemodiversity while unlinked enzyme loci, expression variation alleles, presence variation, and de novo enzyme evolution enable high individual chemodiversity. Since the molecular data suggests selection for mechanisms that increase chemodiversity itself at the population level, the screening hypothesis which posited plants produce a reservoir of diverse chemicals prior to selection8 should be replaced by a chemodiversity selection hypothesis. The results demonstrate that, in addition to plant protection via individual chemicals with known targeting mechanisms for predators, being different from your neighbors even if you are closely related is likely an important element in plant protection.

The claustrum is a broadly connected subcortical structure proposed to coordinate distributed cortical activity. Claustral neurons are recruited during synchronized brain states and contribute to sleep-dependent memory consolidation, primarily through effects on cortical dynamics. Yet the claustrum also innervates the subicular complex, a major hippocampal output node, raising the possibility that it may regulate both cortical state and hippocampo-cortical dialogue during sleep. Here, we identify a projection-defined population of claustral neurons targeting the subicular complex, CLAsc, that is preferentially recruited during slow-wave sleep and tracks cortical and subicular sleep dynamics. Optogenetic activation of CLAsc neurons during post-learning sleep enhanced spatial memory consolidation without detectable changes in ripple occurrence or slow-oscillation-spindle coupling. Instead, CLAsc activation imposed a stereotyped cortical-subicular motif: a brief gamma-rich Up state followed by a coordinated Down state across prefrontal, retrosplenial and subicular regions. Within this gamma-rich Up state, interareal coherence increased, gamma bursts became synchronized, and lagged directed interactions were transiently reorganized, including an enhanced prefrontal-to-subicular component. Together, these findings identify the claustrum as a state-dependent coordinator that transforms ongoing cortical and hippocampal-output activity into coordinated network transitions during sleep, providing a circuit mechanism through which distributed brain states may support memory consolidation.

Heterochromatin replication isnt random or uniform, but occurs in a characteristic spatial and temporal pattern. Previous studies produced conflicting models for pericentric heterochromatin (PCH) replication, suggesting either that heterochromatic sequences translocate to the domain surface for replication, or that replication can also occur internally through localized decondensation. To distinguish true overlap from peripheral enrichment around an irregular PCH domain, we developed FOC-Map, a colocalization analysis approach that combines segmentation of one channel with binning of the other. Applying FOC-Map to three-dimensional Airyscan imaging of cultured Drosophila cells, we find that replication foci at the onset of late S-phase are confined to the outer boundary of the PCH domain, forming a shell-like pattern with little overlap into the HP1a-rich interior. As late S-phase progresses, replication foci are observed within the domain, localizing to low-HP1a regions interspersed between more condensed regions. We then assessed the distribution of CDC45, a rate-limiting replication initiation factor, and found that CDC45 foci are depleted from the PCH domain throughout the cell cycle. We propose that low levels of CDC45 within HP1a-rich PCH limit replication initiation to the domain periphery, giving rise to the shell-like pattern of replication foci that progressively works inward until PCH replication is complete.

Early animal embryos undergo rapid cleavages that partition cytoplasmic volumes orders of magnitude larger than those of somatic cells1. Each division must reposition nuclei and centrosomes and distribute organelles within minutes, over distances up to hundreds of micrometers2. Cleavage furrows are positioned by microtubule asters3,4, but the mechanical mechanism for long-range transport of cytoplasmic components before cytokinesis was unknown. Here, we show that cytoplasm behaves as a locally switchable active material. Fluidization at the midplane allows bulk actomyosin to convert a local mechanical asymmetry into directed global flows of all components as a composite material. Using an actin-intact cycling Xenopus egg extract together with Xenopus and medaka embryos, we find that F-actin mechanically couples microtubule asters, organelles, nuclei and centrosomes into a gel-like composite that propagates forces over hundreds of micrometers. After mitosis, Aurora B kinase patterns a locally fluidized midplane, from which myosin-II contractility drives coherent cytoplasmic flows. A fluid dynamics model accounts for the observed flow geometry and rates. Our results reveal how local control of the material state of cytoplasm converts mitotic symmetry breaking into long-range intracellular transport and identify bulk actomyosin as the active stress generator that partitions embryonic cytoplasm as a composite gel.

Active sensing systems are known to adapt the structure of sensory signals. Whether they can improve perception by controlling when sensory information is acquired remains unclear. We show that echolocating fruit bats exposed to rhythmic noise preferentially emit calls during recurring low-noise periods, a behaviour we term "dip echolocation". Dip echolocation occurred in laboratory and wild bats and represents an active-sensing analogue of dip listening in humans. A normative model showed that temporal positioning of calls emerges from a trade-off between sensory information and energetic cost, alongside concurrent adaptations of call structure. Pharmacological inactivation of the frontal auditory field disrupted precise temporal control, implicating a role for frontal cortical circuits in adaptive vocal timing. These findings identify adaptive vocal timing as an active-sensing strategy for overcoming acoustic interference.

Across species, sleep amount and timing are tightly linked to the nutritional environment. While early life sleep and sleep in mature organisms are both dramatically influenced by reductions in the dietary environment, the mechanisms linking nutritional cues to conserved sleep-regulatory circuitry are not well understood. Using both early 3rd instar (L3) Drosophila larvae and adults, we examined the plasticity of sleep responses under shifting nutrient environments across the lifespan. We find that L3 larvae and adults exhibit changes in sleep duration in low sugar environments with L3 showing a loss of sleep-wake rhythms that can be rescued with additional nutrients. We show that larval and adult sleep plasticity is regulated by CCHamide-1 signaling between DN1a and Dh44 neurons and glucose metabolic genes in Dh44 neurons. Additionally, our data indicate that sleep plasticity is not dependent on anatomical and functional connectivity between clock-arousal circuitry, suggesting that peptidergic signaling alone is sufficient for diet-dependent sleep regulation. Finally, we demonstrate that Dh44 neurons in both L3 larvae and adults adjust mRNA levels of CCHamide-1 receptor (CCHa1-R) in response to changes in dietary sugar. Together, our findings suggest that organisms utilize conserved molecular signaling pathways across the lifespan to dynamically regulate their sleep in a changing environment.

Fluid behavior requires temporal coordination across brain systems that orchestrate movement. A clear example is locomotion, in which left and right turns are not only precisely coordinated with the ongoing stepping rhythm but occur at opposite phases of the stepping cycle. The circuits underlying this coordination remain poorly understood. We discover that neuronal activity in the mouse superior colliculus, a conserved midbrain structure involved in turning behavior, is tightly phase-locked to the stepping rhythm. Notably, neurons selective for left and right turns fire at opposite phases of the stepping cycle. Moreover, this phase opposition is already evident during straight locomotion, before the animal initiates a turn. By aligning the activity of left and right turn neurons to opposite phases of the stepping cycle, the superior colliculus may create alternating windows of opportunity for left and right turns, facilitating the seamless execution of turns during locomotion.

Denisovans, originally identified from ancient genome from Denisova Cave in Altai, were a sister group to the Neanderthals and were once widely distributed across diverse terrains in the north and south of eastern Asia1-5. Genomic studies suggest that there were multiple events of interbreeding between modern humans (Homo sapiens) and Denisovans somewhere in Asia6. However, little is known about Denisovan living environments, diet, ecological niche, the timing of their disappearance, and the possible coexistence with modern humans in different regions. Here we report the radiocarbon age and stable isotopic signature of Penghu 3, a large Denisovan tibia from Penghu Channel, Taiwan7. The results showed that Penghu 3 dates to approximately 45,000 years ago, the time when modern humans were already widespread in southern parts of Asia. This Denisovan individual inhabited a C4-dominated ecosystem, open environments such as savannahs and floodplains, or a mixture of both, and consumed a high proportion of animal protein similar to some European Neanderthals8-10, with no clear evidence for the use of aquatic resources. These findings have implications for the behavioral flexibility, large body size7, and eventual disappearance of the Denisovans.

Previous molecular archaeological research has made the surprising discovery that almost all studied European walrus finds dating between the 11th and 14th centuries CE seemed to be traded from the Norse colony of Greenland. But why has almost no walrus ivory from the Barents Sea region been detected in medieval Europe, despite its closer proximity and being mentioned in historical accounts? Here, we show that the full spatial extent of medieval Atlantic walrus hunting has been underestimated in previous analyses that targeted modified walrus skulls (rostra) with which pairs of attached tusks were traded, because destructive sampling of ivory artefacts is not always practicable. By analysing workshop offcuts from medieval Sigtuna, Sweden, we directly compare the geographical sources of walrus ivory with rostra, and show that isolated tusks were traded in different ways. We first resolve the genome-wide trans-Atlantic walrus population structure, discovering significant genome-wide nuclear differentiation between western and eastern Atlantic walrus populations. By employing spatially diagnostic nuclear SNPs (n = 144,986), we then use low-coverage sequence data to classify historical walrus rostrum and tusk specimens to either western or eastern Atlantic origin, and thus overcome previous limitations when provenancing walruses based on mitochondrial DNA alone. We find that all medieval walrus rostra are assigned exclusively towards the western Atlantic. In contrast, half of the medieval ivory specimens from Sigtuna are assigned to eastern Atlantic sources including Iceland and the Barents Sea region. Moreover, the objects of eastern origin precede those from Norse Greenland in time, suggesting sequential exploitation. Our observations resolve a discrepancy between earlier molecular inference and historical evidence and imply a significantly broader extent and impact of medieval ecological globalisation in the Arctic.

The positioning of the mitotic spindle controls the size, content, and position of daughter cells within embryos and tissues. A major spindle positioning mechanism is cortical pulling whereby the membrane-bound complex LGN/NuMA/Dynein captures astral microtubules and pulls centrosomes toward the cell cortex. Cytoplasmic dynein and astral growth tend to counteract cortical pulling and position spindles at the cell center. It remains unclear how these opposing forces cooperate. Here we examine the ascidian embryo, where spindles of two germ line cells rotate toward one another causing divisions which are both mirror symmetric and unequal. We find that this spindle behavior is governed by transient enrichment of LGN and NuMA and enhanced cortical pulling at the shared cell contact. Inhibition of the LGN/NuMA complex disrupts spindle alignment, unequal cleavage, and mirror symmetry. Temporal analysis shows that cortical pulling force initates at anaphase when there is a sharp increase in astral microtubule length. These results point towards two phases of spindle positioning forces, with cytoplasmic pulling and cortical pulling operating sequentially during early and late mitosis.

In temperate regions around the world, bats travel long distances every winter to gather at hibernation sites. A longstanding hypothesis is that each new generation of bats learns about the locations of these sites (called hibernacula) from older individuals, yet clear and compelling evidence demonstrating social transmission of this knowledge has been lacking. Here, we compiled 30,882 observations from 1985 to 2023 of 13,852 Greater mouse-eared bats (Myotis myotis) that were banded and observed at summer roosts, winter hibernacula, or both. Our analyses revealed four lines of evidence that Greater mouse-eared bats find suitable hibernacula using social information acquired at summer roosts. First, naive yearlings were more likely to be seen sharing their first hibernacula with adults from their summer birth colony relative to a null model where bats moved independently. Second, adult bats were also more likely to co-switch together into the same hibernacula across winters than expected from independent movements. Third, bats that roosted together in the summer were more likely to share a different site as a hibernaculum during the winter: being observed together during a summer changed the probability of a pair being observed together during a winter from 5% to 12%. Finally, high-resolution tracking revealed an instance of tandem flights to hibernacula sites during the summer, demonstrating that yearlings can learn from experienced adult bats months before hibernation. Together, our findings show that maternity colonies serve as "information centers" where females acquire knowledge of suitable hibernation sites throughout their long lives.