Current Biology

Eye loss has long fascinated evolutionary biologists and occurs across the animal kingdom. Spiders have two parallel visual systems -- two primary and six secondary eyes -- but eye losses, leaving six, four, two, or no eyes, have occurred in multiple lineages. Despite their significance, reports of eye loss are scattered, limiting broader analysis. Here we present the first comprehensive analysis of eye loss across all known spider lineages. We show that eye loss occurs in [~]12% of extant species, mainly within the clade Synspermiata. Six-eyed spiders are most common (>5,300 species), while four-eyed, two-eyed, and eyeless forms are rarer and often linked to troglobitic lifestyles. Principal eye loss is widespread, occurring in 49 families across nearly all major lineages. Using a recent phylogeny of the order Araneae, we demonstrate a strong correlation between eye loss and occupancy of low-light environments, but this is complicated by differential effects across eye types and phylogenetic groups through geological time. These findings reveal striking lability in eye number and lay groundwork for future research into ecological, developmental, and neurological drivers of eye loss. [hidden Markov models, ancestral state reconstruction, Araneae, discrete character evolution, principal eyes, secondary eyes, low light environments].

Acoustic communication signals often contain complex temporal structure, yet the features underlying signal recognition remain poorly understood, particularly in eavesdropping receivers. The parasitoid fly Ormia ochracea localises host crickets by eavesdropping on their calling songs. In Florida, preferred host songs consist of sound pulses repeated at ~50 pulses/s, and flies exhibit matching preferences. However, it remains unclear whether this preference reflects sensitivity to individual temporal features (e.g., pulse duration, interpulse interval) or to derived temporal relationships (e.g., pulse rate, pulse period, duty cycle) that emerge from their combination. We independently varied pulse duration and interpulse interval across a broad stimulus space and quantified tethered-walking phonotaxis using a switch-following paradigm. Behavioural responses formed a structured tuning surface, with high performance along a diagonal corresponding to 50 pulses/s, as well as elevated responses for a restricted range of pulse durations across a wide range of interpulse intervals. Responses failed to collapse across stimuli sharing the same pulse rate or pulse period, indicating that these features alone do not determine recognition. Instead, behaviour was best explained by the interacting effects of pulse duration and interpulse interval. These results demonstrate that song recognition in O. ochracea is multidimensional, with pulse rate tuning emerging from an underlying feature space rather than a single encoded parameter.

The evolutionary origin of nervous systems in animals remains elusive and is largely hidden from the fossil record. Ctenophores, one of the earliest-branching animals possessing neurons, are instrumental to our understanding of nervous system origin, and a few rare ctenophore fossils preserve traces of nervous tissue as carbonaceous remains. Cambrian ctenophores appear to exhibit a more diverse neuroanatomy than that of modern species, suggesting secondary loss in extant ctenophores. However, much remains unknown about the origin and ontogeny giving rise to the structural organization of modern ctenophore nervous systems. Here, by investigating the neural anatomy of the ctenophore Mnemiopsis leidyi during development, we identified a ladder-like nerve net (LNN) beneath the comb rows that converges into condensed neurites and connects to the aboral organ. Examination of carbon-rich areas of Ctenorhabdotus capulus, an extinct ctenophore from the Burgess Shale, reveals a pattern similar to that of M. leidyi, consistent with a shared neural organization. Furthermore, M. leidyi exhibits a condensed comb nerve, resembling the longitudinal nerve preserved in the Cambrian ctenophore Fasciculus vesanus and the giant axon of extant Euplokamis dunlapae. Our study reveals conserved evolutionary constraints shaping nervous system architectures linked to locomotory organs and indicates that the different modes of nervous system organization observed in Cambrian ctenophores are variably retained in modern species.

Repeated execution of individual behavioural units is a common feature of many learned motor behaviours such as dance, music, and birdsong. Little is known about the neuronal control of such learned motor sequences, and specifically, how the number of variable repetitions is determined. The songs of Bengalese finches (Lonchura striata domestica) consist of individual syllables which can repeat a variable number of times (repeat number) to form a repeat phrase. Like vocal sequences in other animals, Bengalese finch song syntax is typically modelled as a Markov chain, where the choice to repeat the same syllable type or switch to a different one is made stochastically after each syllable, before the next syllable is produced. Here, we report that repeat numbers of adjacent and distant repeat phrases in the song can be correlated across specific pairs of phrases. These hidden links between distinct phrases challenge existing models of song syntax where the number of repetitions is independently determined for each syllable type. Instead, they suggest an organisation where a joint factor can control multiple nonadjacent phrases in a song. Repeat phrases in Bengalese finches may therefore be particularly suited to study the neuronal mechanisms underlying long-range dependencies in complex vocal sequences.

Heterotrimeric kinesin 2 is the canonical motor protein for anterograde intraflagellar transport (IFT), driving movement of protein complexes towards the tip of cilia and flagella. Here, we show that all members of the Euglenozoa group lack genes for heterotrimeric kinesins and instead possess a variable number of genes for two homodimeric kinesins termed KIN2A and KIN2B. When expressed in vitro, both Trypanosoma brucei kinesins form homodimers and move processively along brain microtubules, KIN2A being faster than KIN2B. Studies in T. brucei and Leishmania mexicana show anterograde and retrograde IFT of both kinesins, with KIN2A travelling throughout the whole length of the flagellum, while KIN2B is concentrated at its base. In the proximal portion of the flagellum, most KIN2B molecules travel without IFT proteins, except for a few particles that are associated with IFT proteins and reach the tip. Surprisingly, the absence of KIN2A has mild effects on IFT and flagellum assembly, whereas KIN2B is essential for both. Investigation of trypanosome flagella deprived of KIN2B revealed that IFT proteins do not access these flagella but that KIN2A can still circulate. These results support a division-of-labour model where KIN2B is responsible for the import of IFT proteins while KIN2A is responsible for most of the anterograde transport.

A central challenge in characterizing species niches is ensuring that foraging data accurately capture both the resources used and their relative importance, and the role of resource abundance in shaping foraging patterns. Most studies infer diet breadth and resource-use patterns from observational records, yet such data can mask resource-specific decisions when animals forage with different goals. Here, we test this experimentally using individually identifiable bees in controlled resource communities to quantify foraging decisions between nectar (for sustenance) and pollen (for offspring provisioning). Combining observations, pollen DNA metabarcoding, and pollen microscopy, we show that observed visitation patterns misrepresent the floral resources most important for offspring provisioning, which ultimately determines offspring survival and population persistence. We further show that interaction patterns are structured from processes beyond resource abundance. Our results demonstrate that commonly used observational approaches can mischaracterize diet breadth, potentially challenging conclusions about species generalization.

Dumbbell-shaped stomata in grasses represent an evolutionary novelty, as their distinctive guard cell morphology is absent from most plant lineages. Stomata exhibit two major morphological forms: the kidney-shaped type found in most plants, and the dumbbell-shaped type that evolved in grasses. Dumbbell-like forms occur in sedges (Cyperaceae), providing an opportunity to examine how changes in developmental trajectories contribute to morphological evolution. By integrating analyses of cellulose microfibril organization, guard cell length to width ratio, and nuclear morphology, we demonstrate partial convergence between sedge and grass stomatal development. Specifically, cellulose microfibril organization in sedges represents an intermediate developmental state between kidney-shaped stomata and the grass dumbbell-shaped stomata. We further document differences in nuclear architecture: in contrast to kidney-shaped stomata, which have rounded nuclei in central guard cell regions, sedge nuclei are partially elongated and localize within bulbous regions, whereas grass nuclei exhibit fully elongated shapes along the cell axis. Notably, we identified secondary plasmodesmata between guard cells in one sedge species, suggesting a convergent route to symplastic communication achieved through secondary plasmodesmata formation rather than the incomplete cytokinesis characteristic of grasses. Together, these findings reveal convergent developmental solutions underlying similar stomatal morphologies.

Hybridisation between species was once considered a relatively uncommon occurrence but is now recognised to occur frequently across many different taxa. It can result in homogenisation of previously distinct forms, a potential conservation issue, but can also act as a catalyst for diversification through introgression and sharing of favourable genes. Repeated rounds of island colonisation followed by speciation result in secondary sympatry, with the potential for hybridisation between early and late arrivers. In the southwest Pacific, this situation has arisen in the avian family Zosteropidae (the white-eyes). Here we use whole genome sequencing of live birds and historical specimens to characterise hybridisation between three white-eye species on Norfolk Island: two island endemics, Zosterops tenuirostris and the now-extinct Zosterops albogularis, and Zosterops lateralis, which colonised the island in 1904. Despite over two million years of divergence between Z. lateralis and the two endemics, we provide genomic evidence of their hybridisation. First, we confirm the identities of three Z. lateralis x Z. tenuirostris hybrids and additionally identify one Z. lateralis x Z. albogularis hybrid. We also report asymmetric, genome-wide introgression from both endemics into Z. lateralis, with introgressed regions enriched for a range of potential functions. However, despite this introgression, species boundaries have been maintained, and the extant endemic Z. tenuirostris does not appear to be at risk of genetic extinction. Our work additionally demonstrates an unusual case of recent ghost introgression from the extinct Z. albogularis into Z. lateralis. This study sheds light on the genomic outcomes of secondary sympatry and its potential consequences for single-island endemics.

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.

The Dinaric karst of Croatia encompasses a network of over 10,000 caves and represents one of the worlds most important subterranean biodiversity hotspots. It is inhabited by remarkably diverse and often endemic species, including planarian flatworms, which are among the rarest macroinvertebrates encountered in cave habitats. Although the presence of cave planarians has long been known, no integrative research on this group has been conducted to date, and the evolutionary relationships between these animals and their surface water counterparts are currently unresolved. To address these gaps, we combined field sampling, phylogenetic analysis based on COI and 18S genes, and phenotypic characterization. Our results show that cave planariids in Croatia belong to at least three genera and are more widespread and diverse across both Croatia, and the broader Dinaric karst, than previously assumed. We increased the number of cave records in the Dinaric karst from 26 to 37 and documented cf. Atrioplanaria and Phagocata in Croatian caves for the first time. Phylogenetic reconstructions suggest numerous independent cave colonization events, including multiple instances within the genera Crenobia and cf. Atrioplanaria. Variation in pigmentation and eye reduction, both within and between populations, further reveal heterogeneous evolutionary trajectories of cave-associated phenotypes. The biogeographical patterns and high genetic diversity we report here point to a complex evolutionary history of planariids in the Dinarides. Our newly generated molecular phylogenies and systematic documentation of trait variability establish Planariidae as a valuable model for studying mechanisms underlying convergent evolution of pigment loss and eye reduction in cave 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

An object on immediate collision course generates a rapidly expanding visual stimulus on the retina, which will typically trigger a fast, evasive behavior. In hoverflies, for example, such visual looming stimuli may be generated if the insect is about to collide with a stationary object in the surround, by an approaching predator, or by conspecifics during territorial interactions. Thus, similar looming cues can evoke distinct behavioral outputs depending on their source. Supporting this diverse range of appropriate behavioral responses are a multitude of different looming sensitive descending neurons that project information from the head to the thoracic ganglia. We here show that the looming receptive fields of looming sensitive descending neurons are predominantly located in the ventral visual field. To investigate if this is matched by behavior, we recorded how tethered hoverflies responded to looming stimuli displayed either in the dorsal or ventral part of a visual monitor, at four different speeds (l/|v| of 10 - 667 ms), covering a naturalistic range. We found that ventral stimuli, especially at intermediate speeds (l/|v| = 50 - 200 ms), triggered much stronger behavioral responses than dorsally displayed stimuli. The behavioral data thus not only match the receptive fields of the neurons likely to support the behavior, but also highlight that behavioral output is not entirely reflexive but is strongly modulated by stimulus speed and elevation. Significance StatementIf someone throws a ball at you, this generates a rapidly expanding object across your visual field, which will make you react before you have even had time to think. You may for example duck, dip or dive to avoid the ball, or bring your hands up to grab it. Similarly, many insects respond to rapidly approaching objects. We here show that hoverfly reactions to such looming stimuli depend on stimulus speed and elevation, with the strongest reaction to stimuli approaching from below. We further demonstrate that the neurons likely supporting these behaviors show highest sensitivity in the ventral visual field, suggesting a close match between neural tuning and behavioral output.

Parents across diverse taxa modify the biotic or abiotic environments of their offspring. Such modifications may constitute ecological inheritance and are central to developmental niche construction, whereby organisms shape developmental conditions and selective pressures experienced by the next generation. Despite its theoretical importance, parental niche construction is often studied under simplified conditions or by focusing on single components of care, limiting our understanding of how multiple parental modifications interact in ecologically relevant contexts and shape offspring development and evolutionary trajectories. Using the burying beetle Nicrophorus vespilloides, we investigated how parents jointly modify chemical and microbial properties of vertebrate carcasses, a highly contested resource on which the beetles larvae develop. We show that under natural microbial and competitive conditions, pre-hatch parental care enhances larval survival and growth, alters cadaveric volatile emissions, and reduces carcass attractiveness to competitors. While soil type initially shapes carcass-associated microbial communities, parental care buffers these environmental effects, creating a more consistent microbiome and thereby increasing larval survival by reducing environmentally induced mortality. Larvae of the related species Ptomascopus morio, which lacks pre-hatch carcass preparation, showed no difference in survival between prepared and unmodified carcasses, whereas N. vespilloides larvae showed reduced survival on unmodified carcasses. This contrast suggests that N. vespilloides larvae have evolved a reliance on a parentally constructed developmental environment. Together, these findings show that parental care can constitute an integrated form of niche construction that reshapes developmental environments, enhances offspring performance, and can promote evolutionary feedbacks leading to increased offspring dependence on parental care.

Motivation to engage in goal-directed actions is crucial for survival and well-being. Dopaminergic and serotonergic systems have been the focus of efforts to understand neurobiological etiologies of normative and disrupted motivation. Understanding how the brain incorporates salient sensory cues into motivational drive outside of these neuromodulatory systems is less appreciated. We posited that given their afferent and efferent connections, GABAergic cells in the zona incerta (ZI) are ideally positioned to perform this function. Combining behavioral tasks in mice with chemogenetics we show that GABAergic ZI neurons are capable of modulating effort-based motivation and that chemogenetic activation of this cell population can rescue motivational deficits induced by chronic stress - without affecting attention, memory, locomotion, or appetite. Next, using fiber photometry we report that GABAergic cells in the ZI robustly respond to sensory cues and their response to a cue increases as reward-predictive associations are formed. Inhibiting GABAergic cells in the ZI did not abolish cue-associated motivational behavior while cue-locked optogenetic activation of these cells robustly enhanced cue-associated motivated behavior demonstrating that these cells are not necessary but sufficient to allow for sensory cues to influence action selection. These findings establish GABAergic cells in the ZI as modulators of motivation and afford us a neuroanatomical hub that could be targeted to potentially remedy treatment-resistant deficits in motivation.

Pollen development and fertilization are considered the most heat-sensitive stages of plant reproduction. While heat stress severely impairs pollen germination and tube growth, the physiological diversity within a single flowers pollen load suggests that subpopulations may exhibit differential climate resilience. In this study, we tested the hypothesis that this heterogeneity reflects a dormancy-based reserve mechanism that preserves fertilization under heat stress. Using flow cytometry and fluorescence-activated cell sorting in Arabidopsis thaliana and Solanum lycopersicum (MicroTom), we resolved pollen subpopulations by reactive oxygen species (ROS) status and examined their behavior under increasing heat stress. In both species, ROS-defined metabolic state was tightly associated with pollen size: high-ROS pollen was larger and readily germination-competent, whereas low-ROS pollen was smaller and showed low basal germination, consistent with dormancy. Heat stress preferentially depleted the high-ROS fraction, whereas the low-ROS fraction persisted and, under heat stress, increased metabolic activity and size. By isolating low-ROS and high-ROS pollen, we further show that a brief heat treatment suppresses germination of active high-ROS pollen but promotes germination of dormant low-ROS pollen. These findings provide direct evidence that heat can release dormancy in low-ROS pollen and support a conserved model in which dormant pollen serves as a heat-resilient reproductive reserve.

To avoid image blurring, the vestibulo-ocular (VOR) and the optokinetic (OKR) reflexes stabilize gaze. In all vertebrates, the VOR is mediated via direct projections from the vestibular nuclei to the motor nuclei that control the extraocular muscles. Lampreys show three vestibular nuclei that are well characterized in terms of their projections and sensory inputs, but much less is known about their inputs from other brain regions and the connectivity between them. Using tracer injections and electrophysiological recordings, we show that the lamprey vestibular nuclei are largely interconnected, while their inputs from other brain regions are scarce. The main rostral areas projecting to the vestibular nuclei are the pretectum and the ventral tier of the thalamus, which send ipsilateral inputs to the three vestibular nuclei.

Social interactions establish reproductive hierarchies and regulate division of labor in eusocial insect colonies. In the ant Harpegnathos saltator, queen loss induces a subset of workers to transition into reproductive pseudo-queens, known as gamergates, through a ritualized antennal-dueling tournament that can last for more than a month. Gamergate transition is associated with sustained dueling engagement, yet the interaction networks and social dynamics that shape reproductive hierarchy formation remain unclear. Here, we combine long-term automated tracking with behavioral classifiers to systematically quantify social interactions, including antennal dueling and two distinct biting behaviors: aggressive grooming and mandible locking. We find that antennal dueling is organized into two activity states, an engaged state and a disengaged state, and that persistent maintenance of the engaged state, rather than transient entry into it, predicts successful transition to gamergate fate. Early access to abundant food shapes dueling activity and biases ants toward entry into the engaged state. Moreover, engaged-state individuals exhibit a strong assortative preference for dueling with one another and cluster spatially within the colony. We further show that mandible locking precedes transitions out of the engaged state, whereas aggressive grooming reinforces the disengaged state, together contributing to stabilization of worker fate. Our findings reveal how structured social interactions organize reproductive hierarchy formation by regulating stable behavioral states associated with caste fate.

Centromeres are epigenetically specified chromosomal sites that support kinetochore assembly and often embedded within large satellite DNA arrays. Recent telomere to telomere genome assemblies have revealed extensive variation in centromeric satellite arrays between chromosomes and between individuals, but the functional significance of this variation remains unclear. To determine how satellite array size influences centromere function, we generated hybrid mouse models in which homologous chromosomes with different array sizes are paired in meiosis I, creating array size asymmetry across each meiotic bivalent. When an extremely small array is paired with a moderate size array, we find that array size asymmetry leads to functional asymmetry in both centromere chromatin and interactions with spindle microtubules, lagging chromosomes in anaphase I, and increased aneuploidy in MII eggs. In contrast, pairing an extremely large array with a moderate array does not lead to functional centromere asymmetry. Together, these results suggest a threshold model in which centromere array size is tolerated across a broad range, but minimal arrays become functionally limiting when paired with larger arrays in meiosis.

How plants allocate carbon determines their productivity, responses to stress, and interactions with other organisms. A substantial amount of plant carbon is stored as non-structural carbohydrates (NSC), which sustain turgor via osmoregulation and fuel metabolism when carbon is limited. NSC also support root-colonizing mycorrhizal fungi, thus we hypothesized that under carbon-limiting conditions such as drought, a trade-off between feeding mycorrhizal fungi and maintaining turgor may arise. We reduced carbon allocation to ectomycorrhizal (EcM) networks by girdling Pinus ponderosa trees exposed to drought or ambient conditions and manipulated putative fungal connections between trees by trenching. We show that, in droughted plots, trees putatively connected to girdled trees by EcM networks had 33 % less needle NSC and >10% less turgor than those connected to ungirdled trees. Trees disconnected from the mycorrhizal network by trenching had increased NSC likely from the increased water availability with girdling, but these gains were offset in the presence of networks. Our results demonstrate that the increased carbon demand by EcM fungi in response to reduced carbon inputs from some trees can deplete NSC in neighboring trees via shared mycorrhizal networks. At least in the short term, allocation trade-offs under carbon-limiting conditions may expose networked trees to carbon deficits. This may increase vulnerability to drought, which may be particularly acute given shifts in climate.

Powered flight is a critical innovation associated with the evolutionary transition from non-avialan theropods to birds, yet how early feathers gave rise to modern pennaceous feather structures with optimized aerodynamic performance remains unclear. Here we report a three-dimensionally preserved pennaceous feather from the Burmese amber ([~]99 Ma) that exceeds 105 mm in preserved length, representing the longest known feather preserved in amber. It shows symmetrical vanes with densely packed barbs, indicating a derived pennaceous branching architecture, but lacks interlocking barbules and exhibits incompletely differentiated rachis and barbs, implying limited aerodynamic performance. This combination of advanced branching organization and incomplete tissue differentiation indicates asynchronous evolution of pennaceous feathers, in which branching organization, elongation and vane organization preceded the acquisition of interlocking barbules and fully differentiated cortical and medullary tissues required for aerodynamic function. These findings provide direct fossil evidence for stepwise, modular evolution of pennaceous feathers. They suggest that aerodynamic optimization of flight-related feather structures may not have been the primary driver of pennaceous feather branching. Significance statementHow pennaceous feathers became mechanically specialized for powered flight remains poorly understood. Here we report that the longest known three-dimensionally preserved pennaceous feather from Burmese amber ([~]99 Ma) exhibits a symmetrical but non-interlocking vane and limited tissue differentiation in the rachis and barbs, capturing a previously undocumented transitional stage in pennaceous feather evolution. This structural mosaic provides direct fossil evidence that aerodynamic performance was optimized through stepwise, modular evolution of pennaceous feather structures.