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For more than a century, the origin and evolution of the arthropod head and brain have eluded a unifying rationale reconciling divergent morphologies and phylogenetic relationships. Here, clarification is provided by the fossilized nervous system of the lower Cambrian lobopodian

In 1882, the Italian embryologist Giuseppe Bellonci introduced a nomenclature for structures in the stomatopod crustacean Squilla mantis that he claimed correspond to insect mushroom bodies, today recognized as cardinal centers that in insects mediate associative memory. The use of Bellonci's terminology has, through a series of misunderstandings and entrenched opinions, led to contesting views regarding whether centers in crustacean and insect brains that occupy corresponding locations and receive comparable multisensory inputs are homologous or homoplasic. The following describes the fate of terms used to denote sensory association neuropils in crustacean species and relates how those terms were deployed in the 1920s and 1930s by the Swedish neuroanatomist Bertil Hanström to claim homology in insects and crustaceans. Yet the same terminology has been repurposed by subsequent researchers to promote the very opposite view: that mushroom bodies are a derived trait of hexapods and that equivalent centers in crustaceans evolved independently.

Many biological systems across scales of size and complexity exhibit a time-varying complex network structure that emerges and self-organizes as a result of interactions with the environment. Network interactions optimize some intrinsic cost functions that are unknown and involve for example energy efficiency, robustness, resilience, and frailty. A wide range of networks exist in biology, from gene regulatory networks important for organismal development, protein interaction networks that govern physiology and metabolism, and neural networks that store and convey information to networks of microbes that form microbiomes within hosts, animal contact networks that underlie social systems, and networks of populations on the landscape connected by migration. Increasing availability of extensive (big) data is amplifying our ability to quantify biological networks. Similarly, theoretical methods that describe network structure and dynamics are being developed. Beyond static networks representing snapshots of biological systems, collections of longitudinal data series can help either at defining and characterizing network dynamics over time or analyzing the dynamics constrained to networked architectures. Moreover, due to interactions with the environment and other biological systems, a biological network may not be fully observable. Also, subnetworks may emerge and disappear as a result of the need for the biological system to cope with for example invaders or new information flows. The confluence of these developments renders tractable the question of how the structure of biological networks predicts and controls network dynamics. In particular, there may be structural features that result in homeostatic networks with specific higher-order statistics (e.g., multifractal spectrum), which maintain stability over time through robustness and/or resilience to perturbation. Alternative, plastic networks may respond to perturbation by (adaptive to catastrophic) shifts in structure. Here, we explore the opportunity for discovering universal laws connecting the structure of biological networks with their function, positioning them on the spectrum of time-evolving network structure, that is, dynamics of networks, from highly stable to exquisitely sensitive to perturbation. If such general laws exist, they could transform our ability to predict the response of biological systems to perturbations—an increasingly urgent priority in the face of anthropogenic changes to the environment that affect life across the gamut of organizational scales.

Summary Fossils provide insights into how organs may have diversified over geological time.1 However, diversification already accomplished early in evolution can obscure ancestral events leading to it. For example, already by the mid-Cambrian period, euarthropods had condensed brains typifying modern mandibulate lineages.2 However, the demonstration that extant euarthropods and chordates share orthologous developmental control genes defining the segmental fore-, mid-, and hindbrain suggests that those character states were present even before the onset of the Cambrian.3 Fossilized nervous systems of stem Euarthropoda might, therefore, be expected to reveal ancestral segmental organization, from which divergent arrangements emerged. Here, we demonstrate unsurpassed preservation of cerebral tissue in Kaili leanchoiliids revealing near-identical arrangements of bilaterally symmetric ganglia identified as the proto-, deuto-, and tritocerebra disposed behind an asegmental frontal domain, the prosocerebrum, from which paired nerves extend to labral ganglia flanking the stomodeum. This organization corresponds to labral connections hallmarking extant euarthropod clades4 and to predicted transformations of presegmental ganglia serving raptorial preocular appendages of Radiodonta.5 Trace nervous system in the gilled lobopodian Kerygmachela kierkegaardi6 suggests an even deeper prosocerebral ancestry. An asegmental prosocerebrum resolves its location relative to the midline asegmental sclerite of the radiodontan head, which persists in stem Euarthropoda.7 Here, data from two Kaili Leanchoilia, with additional reference to Alalcomenaeus,8,9 demonstrate that Cambrian stem Euarthropoda confirm genomic and developmental studies10–15 claiming that the most frontal domain of the euarthropod brain is a unique evolutionary module distinct from, and ancestral to, the fore-, mid-, and hindbrain.

In one species of shore crab (Brachyura, Varunidae), a center that supports long-term visual habituation and that matches the reniform body's morphology has been claimed as a homolog of the insect mushroom body despite lacking traits that define it as such. The discovery in a related species of shore crab of a mushroom body possessing those defining traits renders that interpretation unsound. Two phenotypically distinct, coexisting centers cannot both be homologs of the insect mushroom body. The present commentary outlines the history of research leading to misidentification of the reniform body as a mushroom body. One conclusion is that if both centers support learning and memory, this would be viewed as a novel and fascinating attribute of the pancrustacean brain.

Neural organization of mushroom bodies is largely consistent across insects, whereas the ancestral ground pattern diverges broadly across crustacean lineages resulting in successive loss of columns and the acquisition of domed centers retaining ancestral Hebbian-like networks and aminergic connections. We demonstrate here a major departure from this evolutionary trend in Brachyura, the most recent malacostracan lineage. In the shore crabHemigrapsus nudus, instead of occupying the rostral surface of the lateral protocerebrum, mushroom body calyces are buried deep within it with their columns extending outwards to an expansive system of gyri on the brain’s surface. The organization amongst mushroom body neurons reaches extreme elaboration throughout its constituent neuropils. The calyces, columns, and especially the gyri show DC0 immunoreactivity, an indicator of extensive circuits involved in learning and memory.

Experience alters brain structure, but the underlying mechanism remained unknown. Structural plasticity reveals that brain function is encoded in generative changes to cells that compete with destructive processes driving neurodegeneration. At an adult critical period, experience increases fiber number and brain size in Drosophila. Here, we asked if Toll receptors are involved. Tolls demarcate a map of brain anatomical domains. Focusing on Toll-2, loss of function caused apoptosis, neurite atrophy and impaired behaviour. Toll-2 gain of function and neuronal activity at the critical period increased cell number. Toll-2 induced cycling of adult progenitor cells via a novel pathway, that antagonized MyD88-dependent quiescence, and engaged Weckle and Yorkie downstream. Constant knock-down of multiple Tolls synergistically reduced brain size. Conditional over-expression of Toll-2 and wek at the adult critical period increased brain size. Through their topographic distribution, Toll receptors regulate neuronal number and brain size, modulating structural plasticity in the adult brain., eLife digest Everything that you experience leaves its mark on your brain. When you learn something new, the neurons involved in the learning episode grow new projections and form new connections. Your brain may even produce new neurons. Physical exercise can induce similar changes, as can taking antidepressants. By contrast, stress, depression, ageing and disease can have the opposite effect, triggering neurons to break down and even die. The ability of the brain to change in response to experience is known as structural plasticity, and it is in a tug-of-war with processes that drive neurodegeneration. Structural plasticity occurs in other species too: for example, it was described in the fruit fly more than a quarter of a century ago. Yet, the molecular mechanisms underlying structural plasticity remain unclear. Li et al. now show that, in fruit flies, this plasticity involves Toll receptors, a family of proteins present in the brain but best known for their role in the immune system. Fruit flies have nine different Toll receptors, the most abundant being Toll-2. When activated, these proteins can trigger a series of molecular events in a cell. Li et al. show that increasing the amount of Toll-2 in the fly brain makes the brain produce new neurons. Activating neurons in a brain region has the same effect, and this increase in neuron number also depends on Toll-2. By contrast, reducing the amount of Toll-2 causes neurons to lose their projections and connections, and to die, and impairs fly behaviour. Li et al. also show that each Toll receptor has a unique distribution across the fly brain. Different types of experiences activate different brain regions, and therefore different Toll receptors. These go on to trigger a common molecular cascade, but they modulate it such as to result in distinct outcomes. By working together in different combinations, Toll receptors can promote either the death or survival of neurons, and they can also drive specific brain cells to remain dormant or to produce new neurons. By revealing how experience changes the brain, Li et al. provide clues to the way neurons work and form; these findings may also help to find new treatments for disorders that change brain structure, such as certain psychiatric conditions. Toll-like receptors in humans could thus represent a promising new target for drug discovery.

Stomatopods have an elaborate visual system served by a retina that is unique to this class of pancrustaceans. Its upper and lower eye hemispheres encode luminance and linear polarization while an equatorial band of photoreceptors termed the midband detects color, circularly polarized light and linear polarization in the ultraviolet. In common with many malacostracan crustaceans, stomatopods have stalked eyes, but they can move these independently within three degrees of rotational freedom. Both eyes separately use saccadic and scanning movements but they can also move in a coordinated fashion to track selected targets or maintain a forward eyestalk posture during swimming. Visual information is initially processed in the first two optic neuropils, the lamina and the medulla, where the eye's midband is represented by enlarged regions within each neuropil that contain populations of neurons, the axons of which are segregated from the neuropil regions subtending the hemispheres. Neuronal channels representing the midband extend from the medulla to the lobula where populations of putative inhibitory glutamic acid decarboxylase-positive neurons and tyrosine hydroxylase-positive neurons intrinsic to the lobula have specific associations with the midband. Here we investigate the organization of the midband representation in the medulla and the lobula in the context of their overall architecture. We discuss the implications of observed arrangements, in which midband inputs to the lobula send out collaterals that extend across the retinotopic mosaic pertaining to the hemispheres. This organization suggests an integrative design that diverges from the eumalacostracan ground pattern and, for the stomatopod, enables color and polarization information to be integrated with luminance information that presumably encodes shape and motion.

Crustaceans and insects share many similarities of brain organization suggesting that their common ancestor possessed some components of those shared features. Stomatopods (mantis shrimps) are basal eumalacostracan crustaceans famous for their elaborate visual system, the most complex of which possesses 12 types of color photoreceptors and the ability to detect both linearly and circularly polarized light. Here, using a palette of histological methods we describe neurons and their neuropils most immediately associated with the stomatopod retina. We first provide a general overview of the major neuropil structures in the eyestalks lateral protocerebrum, with respect to the optical pathways originating from the six rows of specialized ommatidia in the stomatopod's eye, termed the midband. We then focus on the structure and neuronal types of the lamina, the first optic neuropil in the stomatopod visual system. Using Golgi impregnations to resolve single neurons we identify cells in different parts of the lamina corresponding to the three different regions of the stomatopod eye (midband and the upper and lower eye halves). While the optic cartridges relating to the spectral and polarization sensitive midband ommatidia show some specializations not found in the lamina serving the upper and lower eye halves, the general morphology of the midband lamina reflects cell types elsewhere in the lamina and cell types described for other species of Eumalacostraca.

The insect central complex and vertebrate basal ganglia are forebrain centres involved in selection and maintenance of behavioural actions. However, little is known about the formation of the underlying circuits, or how they integrate sensory information for motor actions. Here, we show that paired embryonic neuroblasts generate central complex ring neurons that mediate sensory-motor transformation and action selection in Drosophila. Lineage analysis resolves four ring neuron subtypes, R1-R4, that form GABAergic inhibition circuitry among inhibitory sister cells. Genetic manipulations, together with functional imaging, demonstrate subtype-specific R neurons mediate the selection and maintenance of behavioural activity. A computational model substantiates genetic and behavioural observations suggesting that R neuron circuitry functions as salience detector using competitive inhibition to amplify, maintain or switch between activity states. The resultant gating mechanism translates facilitation, inhibition and disinhibition of behavioural activity as R neuron functions into selection of motor actions and their organisation into action sequences.

Significance Comparative developmental genetics indicate insect and mammalian forebrains form and function in comparable ways. However, these data are open to opposing interpretations that advocate either a single origin of the brain and its adaptive modification during animal evolution; or multiple, independent origins of the many different brains present in extant Bilateria. Here, we describe conserved regulatory elements that mediate the spatiotemporal expression of developmental control genes directing the formation and function of midbrain circuits in flies, mice, and humans. These circuits develop from corresponding midbrain-hindbrain boundary regions and regulate comparable behaviors for balance and motor control. Our findings suggest that conserved regulatory mechanisms specify cephalic circuits for sensory integration and coordinated behavior common to all animals that possess a brain., Corresponding attributes of neural development and function suggest arthropod and vertebrate brains may have an evolutionarily conserved organization. However, the underlying mechanisms have remained elusive. Here, we identify a gene regulatory and character identity network defining the deutocerebral–tritocerebral boundary (DTB) in Drosophila. This network comprises genes homologous to those directing midbrain-hindbrain boundary (MHB) formation in vertebrates and their closest chordate relatives. Genetic tracing reveals that the embryonic DTB gives rise to adult midbrain circuits that in flies control auditory and vestibular information processing and motor coordination, as do MHB-derived circuits in vertebrates. DTB-specific gene expression and function are directed by cis-regulatory elements of developmental control genes that include homologs of mammalian Zinc finger of the cerebellum and Purkinje cell protein 4. Drosophila DTB-specific cis-regulatory elements correspond to regulatory sequences of human ENGRAILED-2, PAX-2, and DACHSHUND-1 that direct MHB-specific expression in the embryonic mouse brain. We show that cis-regulatory elements and the gene networks they regulate direct the formation and function of midbrain circuits for balance and motor coordination in insects and mammals. Regulatory mechanisms mediating the genetic specification of cephalic neural circuits in arthropods correspond to those in chordates, thereby implying their origin before the divergence of deuterostomes and ecdysozoans.

Mantis shrimps (Stomatopoda) possess in common with other crustaceans, and with Hexapoda, specific neuroanatomical attributes of the protocerebrum, the most anterior part of the arthropod brain. These attributes include assemblages of interconnected centers called the central body complex and in the lateral protocerebra, situated in the eyestalks, paired mushroom bodies. The phenotypic homologues of these centers across Panarthropoda support the view that ancestral integrative circuits crucial to action selection and memory have persisted since the early Cambrian or late Ediacaran. However, the discovery of another prominent integrative neuropil in the stomatopod lateral protocerebrum raises the question whether it is unique to Stomatopoda or at least most developed in this lineage, which may have originated in the upper Ordovician or early Devonian. Here, we describe the neuroanatomical structure of this center, called the reniform body. Using confocal microscopy and classical silver staining, we demonstrate that the reniform body receives inputs from multiple sources, including the optic lobe's lobula. Although the mushroom body also receives projections from the lobula, it is entirely distinct from the reniform body, albeit connected to it by discrete tracts. We discuss the implications of their coexistence in Stomatopoda, the occurrence of the reniform body in another eumalacostracan lineage and what this may mean for our understanding of brain functionality in Pancrustacea.

Brain centers possessing a suite of neuroanatomical characters that define mushroom bodies of dicondylic insects have been identified in mantis shrimps, which are basal malacostracan crustaceans. Recent studies of the caridean shrimp Lebbeus groenlandicus further demonstrate the existence of mushroom bodies in Malacostraca. Nevertheless, received opinion promulgates the hypothesis that domed centers called hemiellipsoid bodies typifying reptantian crustaceans, such as lobsters and crayfish, represent the malacostracan cerebral ground pattern. Here, we provide evidence from the marine hermit crab Pagurus hirsutiusculus that refutes this view. P. hirsutiusculus, which is a member of the infraorder Anomura, reveals a chimeric morphology that incorporates features of a domed hemiellipsoid body and a columnar mushroom body. These attributes indicate that a mushroom body morphology is the ancestral ground pattern, from which the domed hemiellipsoid body derives and that the “standard” reptantian hemiellipsoid bodies that typify Astacidea and Achelata are extreme examples of divergence from this ground pattern. This interpretation is underpinned by comparing the lateral protocerebrum of Pagurus with that of the crayfish Procambarus clarkii and Orconectes immunis, members of the reptantian infraorder Astacidea. (Less)

A prevailing opinion since 1926 has been that optic lobe organization in malacostracan crustaceans and insects reflects a corresponding organization in their common ancestor. Support for this refers to malacostracans and insects both possessing three, in some instances four, nested retinotopic neuropils beneath their compound eyes. Historically, the rationale for claiming homology of malacostracan and insect optic lobes referred to those commonalities, and to comparable arrangements of neurons. However, recent molecular phylogenetics has firmly established that Malacostraca belong to Multicrustacea, whereas Hexapoda and its related taxa Cephalocarida, Branchiopoda, and Remipedia belong to the phyletically distinct clade Allotriocarida. Insects are more closely related to remipedes than are either to malacostracans. Reconciling neuroanatomy with molecular phylogenies has been complicated by studies showing that the midbrains of remipedes share many attributes with the midbrains of malacostracans. Here we review the organization of the optic lobes in Malacostraca and Insecta to inquire which of their characters correspond genealogically across Pancrustacea and which characters do not. We demonstrate that neuroanatomical characters pertaining to the third optic lobe neuropil, called the lobula complex, may indicate convergent evolution. Distinctions of the malacostracan and insect lobula complexes are sufficient to align neuroanatomical descriptions of the pancrustacean optic lobes within the constraints of molecular-based phylogenies.

Just one superorder of insects is known to possess a neuronal network that mediates extremely rapid reactions in flight in response to changes in optic flow. Research on the identity and functional organization of this network has over the course of almost half a century focused exclusively on the order Diptera, a member of the approximately 300-million-year-old clade Holometabola defined by its mode of development. However, it has been broadly claimed that the pivotal neuropil containing the network, the lobula plate, originated in the Cambrian before the divergence of Hexapoda and Crustacea from a mandibulate ancestor. This essay defines the traits that designate the lobula plate and argues against a homologue in Crustacea. It proposes that the origin of the lobula plate is relatively recent and may relate to the origin of flight.

The middle Cambrian taxon Waptia fieldensis offers insights into early evolution of sensory arrangements that may have supported a range of actions such as exploratory behavior, burrowing, scavenging, swimming, and escape, amongst others. Less elaborate than many modern pancrustaceans, specific features of Waptia that suggest a possible association with the pancrustacean evolutionary trajectory, include mandibulate mouthparts, a single pair of antennae, reflective triplets on the head comparable to ocelli, and traces of brain and optic lobes that conform to the pancrustacean ground pattern. This account revisits an earlier description of Waptia to further interpret the distribution of its overall morphology and receptor arrangements in the context of plausible behavioral repertoires.

Paired centers in the forebrain of insects, called the mushroom bodies, have become the most investigated brain region of any invertebrate due to novel genetic strategies that relate unique morphological attributes of these centers to their functional roles in learning and memory. Mushroom bodies possessing all the morphological attributes of those in dicondylic insects have been identified in mantis shrimps, basal hoplocarid crustaceans that are sister to Eumalacostraca, the most species-rich group of Crustacea. However, unless other examples of mushroom bodies can be identified in Eumalacostraca, the possibility is that mushroom body-like centers may have undergone convergent evolution in Hoplocarida and are unique to this crustacean lineage. Here, we provide evidence that speaks against convergent evolution, describing in detail the paired mushroom bodies in the lateral protocerebrum of a decapod crustacean, Lebbeus groenlandicus, a species belonging to the infraorder Caridea, an ancient lineage of Eumalacostraca.

Occasionally, fossils recovered from lower and middle Cambrian sedimentary rocks contain the remains of nervous system. These residues reveal the symmetric arrangements of brain and ganglia that correspond to the ground patterns of brain and ventral ganglia of four major panarthropod clades existing today: Onychophora, Chelicerata, Myriapoda, and Pancrustacea. Comparative neuroanatomy of living species and studies of fossils suggest that highly conserved neuronal arrangements have been retained in these four lineages for more than a half billion years, despite some major transitions of neuronal architectures. This chapter will review recent explorations into the evolutionary history of the arthropod brain, concentrating on the subphylum Pancrustacea, which comprises hexapods and crustaceans, and on the subphylum Chelicerata, which includes horseshoe crabs, scorpions, and spiders. Studies of Pancrustacea illustrate some of the challenges in ascribing homology to centers that appear to have corresponding organization, whereas Chelicerata offers clear examples of both divergent cerebral evolution and convergence.

SummaryThe record of arthropod body fossils is traceable back to the “Cambrian explosion,” marked by the appearance of most major animal phyla. Exceptional preservation provides crucial evidence for panarthropod early radiation. However, due to limited representation in the fossil record of internal anatomy, particularly the CNS, studies usually rely on exoskeletal and appendicular morphology. Recent studies [1–3] show that despite extreme morphological disparities, euarthropod CNS evolution appears to have been remarkably conservative. This conclusion is supported by descriptions from Cambrian panarthropods of neural structures that contribute to understanding early evolution of nervous systems and resolving controversies about segmental homologies [4–12]. However, the rarity of fossilized CNSs, even when exoskeletons and appendages show high levels of integrity, brought into question data reproducibility because all but one of the aforementioned studies were based on single specimens [13]. Foremost among objections is the lack of taphonomic explanation for exceptional preservation of a tissue that some see as too prone to decay to be fossilized. Here we describe newly discovered specimens of the Chengjiang euarthropod Fuxianhuia protensa with fossilized brains revealing matching profiles, allowing rigorous testing of the reproducibility of cerebral structures. Their geochemical analyses provide crucial insights of taphonomic pathways for brain preservation, ranging from uniform carbon compressions to complete pyritization, revealing that neural tissue was initially preserved as carbonaceous film and subsequently pyritized. This mode of preservation is consistent with the taphonomic pathways of gross anatomy, indicating that no special mode is required for fossilization of labile neural tissue.

Animals that have true color vision possess several spectral classes of photoreceptors. Pancrustaceans (Hexapoda + Crustacea) that integrate spectral information about their reconstructed visual world do so from photoreceptor terminals supplying their second optic neuropils, with subsequent participation of the third (lobula) and deeper centers (optic foci). Here we describe experiments and correlative neural arrangements underlying convergent visual pathways in two species of branchiopod crustaceans that have to cope with a broad range of spectral ambience and illuminance in ephemeral pools, yet possess just two optic neuropils, the lamina and optic tectum. Electroretinographic recordings and multimodel inference based on modeled spectral absorptance were used to identify the most likely number of spectral photoreceptor classes in their compound eyes. Recordings from the retina provide support for four color channels. Neuroanatomical observations resolve arrangements in their laminas that suggest signal summation at low light intensities, incorporating chromatic channels. Neuroanatomical observations demonstrate that spatial summation in the lamina of the two species are mediated by quite different mechanisms, both of which allow signals from several ommatidia to be pooled at single lamina monopolar cells. We propose that such summation provides sufficient signal for vision at intensities equivalent to those experienced by insects in terrestrial habitats under dim starlight. Our findings suggest that despite the absence of optic lobe neuropils necessary for spectral discrimination utilized by true color vision, four spectral photoreceptor classes have been maintained in Branchiopoda for vision at very low light intensities at variable ambient wavelengths that typify conditions in ephemeral fresh water habitats.

SummaryExcept in species that have undergone evolved loss, paired lobed centers referred to as “mushroom bodies” occur across invertebrate phyla [1–5]. Unresolved is the question of whether these centers, which support learning and memory in insects, correspond genealogically or whether their neuronal organization suggests convergent evolution. Here, anatomical and immunohistological observations demonstrate that across phyla, mushroom body-like centers share a neuroanatomical ground pattern and proteins required for memory formation. Paired lobed or dome-like neuropils characterize the first brain segment (protocerebrum) of mandibulate and chelicerate arthropods and the nonganglionic brains of polychaete annelids, polyclad planarians, and nemerteans. Structural and cladistic analyses resolve an ancestral ground pattern common to all investigated taxa: chemosensory afferents supplying thousands of intrinsic neurons, the parallel processes of which establish orthogonal networks with feedback loops, modulatory inputs, and efferents. Shared ground patterns and their selective labeling with antisera against proteins required for normal mushroom body function in Drosophila are indicative of genealogical correspondence and thus an ancestral presence predating arthropod and lophotrochozoan origins. Implications of this are considered in the context of mushroom body function and early ecologies of ancestral bilaterians.

A 1915 monograph by the Nobel Prize–winning neuroanatomist Santiago Ramón y Cajal and Domingo Sánchez y Sánchez, describing neurons and their organization in the optic lobes of insects, is now standard fare for those studying the microcircuitry of the insect visual system. The work contains prescient assumptions about possible functional arrangements, such as lateral interactions, centrifugal pathways, and the convergence of neurons onto wider dendritic trees, to provide central integration of information processed at peripheral levels of the system. This chapter will consider further indications of correspondence between the insect-crustacean and the vertebrate visual systems, with particular reference to the deep organization of the optic lobe’s third optic neuropil, the lobula, and part of the lateral forebrain (protocerebrum) that receives inputs from it. Together, the lobula and lateral protocerebrum suggest valid comparison with the visual cortex and olfactory centers.

Mushroom bodies are the iconic learning and memory centers of insects. No previously described crustacean possesses a mushroom body as defined by strict morphological criteria although crustacean centers called hemiellipsoid bodies, which serve functions in sensory integration, have been viewed as evolutionarily convergent with mushroom bodies. Here, using key identifiers to characterize neural arrangements, we demonstrate insect-like mushroom bodies in stomatopod crustaceans (mantis shrimps). More than any other crustacean taxon, mantis shrimps display sophisticated behaviors relating to predation, spatial memory, and visual recognition comparable to those of insects. However, neuroanatomy-based cladistics suggesting close phylogenetic proximity of insects and stomatopod crustaceans conflicts with genomic evidence showing hexapods closely related to simple crustaceans called remipedes. We discuss whether corresponding anatomical phenotypes described here reflect the cerebral morphology of a common ancestor of Pancrustacea or an extraordinary example of convergent evolution., eLife digest With more than four million species, arthropods are the largest and most diverse group of animals on the planet and include, for example, crustaceans, insects and spiders. They are defined by their segmented bodies, hard outer skeletons and jointed limbs. All arthropods share a common ancestor that lived more than 550 million years ago. Exactly how this ancestral arthropod gave rise to the myriad species that exist today is unclear but we know that at some point the arthropod family tree split into branches, one of which went on to become the crustaceans. The crustacean branch then split again, giving rise to a line of descendants that would become the insects. But although insects evolved from crustaceans, the brains of insects possess structures that those of crustaceans do not. Known as mushroom bodies, these structures help to form and store memories. Their absence in crustaceans has therefore been an enduring mystery. Wolff et al. now add a piece to the puzzle by showing that one group of modern-day crustaceans, the mantis shrimps, does in fact possess mushroom bodies. By visualizing cells and pathways within the brains of mantis shrimps, and also a number of closely related species, Wolff et al. show that only these shrimps possess true mushroom bodies. However, some of the mantis shrimp’s close relatives possess a few attributes of these structures. This suggests that mushroom bodies are evolutionarily ancient structures that arose in a common ancestor of insects and crustaceans, before being lost or radically modified in most of the crustaceans. So why did this happen? Mantis shrimps are top predators with excellent vision that hunt over considerable distances, requiring them to evaluate and memorize complex features of their environment. These cognitive demands, which might not be shared by other crustaceans, may have led to the mantis shrimps retaining their mushroom bodies. Further research into the brains and behavior of the mantis shrimp may provide insights into how mushroom bodies construct memories of a complex sensory world.

One approach to investigating functional attributes of the central complex is to relate its various elaborations to pancrustacean phylogeny, to taxon-specific behavioral repertoires and ecological settings. Here we review morphological similarities between the central complex of stomatopod crustaceans and the central complex of dicondylic insects. We discuss whether their central complexes possess comparable functional properties, despite the phyletic distance separating these taxa, with mantis shrimp (Stomatopoda) belonging to the basal branch of Eumalacostraca. Stomatopods possess the most elaborate visual receptor system in nature and display a fascinating behavioral repertoire, including refined appendicular dexterity such as independently moving eyestalks. They are also unparalleled in their ability to maneuver during both swimming and substrate locomotion. Like other pancrustaceans, stomatopods possess a set of midline neuropils, called the central complex, which in dicondylic insects have been shown to mediate the selection of motor actions for a range of behaviors. As in dicondylic insects, the stomatopod central complex comprises a modular protocerebral bridge (PB) supplying decussating axons to a scalloped fan-shaped body (FB) and its accompanying ellipsoid body (EB), which is linked to a set of paired noduli and other recognized satellite regions. We consider the functional implications of these attributes in the context of stomatopod behaviors, particularly of their eyestalks that can move independently or conjointly depending on the visual scene.

Despite being among the most celebrated taxa from Cambrian biotas, anomalocaridids (order Radiodonta) have provoked intense debate about their affinities within the moulting-animal clade that includes Arthropoda. Current alternatives identify anomalocaridids as either stem-group euarthropods, crown-group euarthropods near the ancestry of chelicerates, or a segmented ecdysozoan lineage with convergent similarity to arthropods in appendage construction. Determining unambiguous affinities has been impeded by uncertainties about the segmental affiliation of anomalocaridid frontal appendages. These structures are variably homologized with jointed appendages of the second (deutocerebral) head segment, including antennae and 'great appendages' of Cambrian arthropods, or with the paired antenniform frontal appendages of living Onychophora and some Cambrian lobopodians. Here we describe Lyrarapax unguispinus, a new anomalocaridid from the early Cambrian Chengjiang biota, southwest China, nearly complete specimens of which preserve traces of muscles, digestive tract and brain. The traces of brain provide the first direct evidence for the segmental composition of the anomalocaridid head and its appendicular organization. Carbon-rich areas in the head resolve paired pre-protocerebral ganglia at the origin of paired frontal appendages. The ganglia connect to areas indicative of a bilateral pre-oral brain that receives projections from the eyestalk neuropils and compound retina. The dorsal, segmented brain of L. unguispinus reinforces an alliance between anomalocaridids and arthropods rather than cycloneuralians. Correspondences in brain organization between anomalocaridids and Onychophora resolve pre-protocerebral ganglia, associated with pre-ocular frontal appendages, as characters of the last common ancestor of euarthropods and onychophorans. A position of Radiodonta on the euarthropod stem-lineage implies the transformation of frontal appendages to another structure in crown-group euarthropods, with gene expression and neuroanatomy providing strong evidence that the paired, pre-oral labrum is the remnant of paired frontal appendages.

Preservation of neural tissue in early Cambrian arthropods has recently been demonstrated, to a degree that segmental structures of the head can be associated with individual brain neuromeres. This association provides novel data for addressing long-standing controversies about the segmental identities of specialized head appendages in fossil taxa. Here we document neuroanatomy in the head and trunk of a 'great appendage' arthropod, Alalcomenaeus sp., from the Chengjiang biota, southwest China, providing the most complete neuroanatomical profile known from a Cambrian animal. Micro-computed tomography reveals a configuration of one optic neuropil separate from a protocerebrum contiguous with four head ganglia, succeeded by eight contiguous ganglia in an eleven-segment trunk. Arrangements of optic neuropils, the brain and ganglia correspond most closely to the nervous system of Chelicerata of all extant arthropods, supporting the assignment of 'great appendage' arthropods to the chelicerate total group. The position of the deutocerebral neuromere aligns with the insertion of the great appendage, indicating its deutocerebral innervation and corroborating a homology between the 'great appendage' and chelicera indicated by morphological similarities. Alalcomenaeus and Fuxianhuia protensa demonstrate that the two main configurations of the brain observed in modern arthropods, those of Chelicerata and Mandibulata, respectively, had evolved by the early Cambrian.

The arthropod central complex and vertebrate basal ganglia derive from embryonic basal forebrain lineages that are specified by an evolutionarily conserved genetic program leading to interconnected neuropils and nuclei that populate the midline of the forebrain-midbrain boundary region. In the substructures of both the central complex and basal ganglia, network connectivity and neuronal activity mediate control mechanisms in which inhibitory (GABAergic) and modulatory (dopaminergic) circuits facilitate the regulation and release of adaptive behaviors. Both basal ganglia and central complex dysfunction result in behavioral defects including motor abnormalities, impaired memory formation, attention deficits, affective disorders, and sleep disturbances. The observed multitude of similarities suggests deep homology of arthropod central complex and vertebrate basal ganglia circuitries underlying the selection and maintenance of behavioral actions.

The discovery of fossilized brains and ventral nerve cords in lower and mid-Cambrian arthropods has led to crucial insights about the evolution of their central nervous system, the segmental identity of head appendages and the early evolution of eyes and their underlying visual systems. Fundamental ground patterns of lower Cambrian arthropod brains and nervous systems correspond to the ground patterns of brains and nervous systems belonging to three of four major extant panarthropod lineages. These findings demonstrate the evolutionary stability of early neural arrangements over an immense time span. Here, we put these fossil discoveries in the context of evidence from cladistics, as well as developmental and comparative neuroanatomy, which together suggest that despite many evolved modifications of neuropil centers within arthropod brains and ganglia, highly conserved arrangements have been retained. Recent phylogenies of the arthropods, based on fossil and molecular evidence, and estimates of divergence dates, suggest that neural ground patterns characterizing onychophorans, chelicerates and mandibulates are likely to have diverged between the terminal Ediacaran and earliest Cambrian, heralding the exuberant diversification of body forms that account for the Cambrian Explosion.

The nervous system provides a fundamental source of data for understanding the evolutionary relationships between major arthropod groups. Fossil arthropods rarely preserve neural tissue. As a result, inferring sensory and motor attributes of Cambrian taxa has been limited to interpreting external features, such as compound eyes or sensilla decorating appendages, and early-diverging arthropods have scarcely been analysed in the context of nervous system evolution. Here we report exceptional preservation of the brain and optic lobes of a stem-group arthropod from 520 million years ago (Myr ago), Fuxianhuia protensa, exhibiting the most compelling neuroanatomy known from the Cambrian. The protocerebrum of Fuxianhuia is supplied by optic lobes evidencing traces of three nested optic centres serving forward-viewing eyes. Nerves from uniramous antennae define the deutocerebrum, and a stout pair of more caudal nerves indicates a contiguous tritocerebral component. Fuxianhuia shares a tripartite pre-stomodeal brain and nested optic neuropils with extant Malacostraca and Insecta, demonstrating that these characters were present in some of the earliest derived arthropods. The brain of Fuxianhuia impacts molecular analyses that advocate either a branchiopod-like ancestor of Hexapoda or remipedes and possibly cephalocarids as sister groups of Hexapoda. Resolving arguments about whether the simple brain of a branchiopod approximates an ancestral insect brain or whether it is the result of secondary simplification has until now been hindered by lack of fossil evidence. The complex brain of Fuxianhuia accords with cladistic analyses on the basis of neural characters, suggesting that Branchiopoda derive from a malacostracan-like ancestor but underwent evolutionary reduction and character reversal of brain centres that are common to hexapods and malacostracans. The early origin of sophisticated brains provides a probable driver for versatile visual behaviours, a view that accords with compound eyes from the early Cambrian that were, in size and resolution, equal to those of modern insects and malacostracans.

Copepods are a diverse and ecologically crucial group of minute crustaceans that are relatively neglected in terms of studies on nervous system organization. Recently, morphological neural characters have helped clarify evolutionary relationships within Arthropoda, particularly among Tetraconata (i.e., crustaceans and hexapods), and indicate that copepods occupy an important phylogenetic position relating to both Malacostraca and Hexapoda. This taxon therefore provides the opportunity to evaluate those neural characters common to these two clades likely to be results of shared ancestry (homology) versus convergence (homoplasy). Here we present an anatomical characterization of the brain and central nervous system of the well-studied harpacticoid copepod species Tigriopus californicus. We show that this species is endowed with a complex brain possessing a central complex comprising a protocerebral bridge and central body. Deutocerebral glomeruli are supplied by the antennular nerves, and a lateral protocerebral olfactory neuropil corresponds to the malacostracan hemiellipsoid body. Glomeruli contain synaptic specializations comparable to the presynaptic "T-bars" typical of dipterous insects, including Drosophila melanogaster. Serotonin-like immunoreactivity pervades the brain and ventral nervous system, with distinctive deutocerebral distributions. The present observations suggest that a suite of morphological characters typifying the Tigriopus brain reflect a ground pattern organization of an ancestral Tetraconata, which possessed an elaborate and structurally differentiated nervous system.

Studying the insect visual system provides important data on the basic neural mechanisms underlying visual processing. As in vertebrates, the first step in visual processing in insects is through a series of retinotopic neurons. Recent studies on flies have found that these converge onto assemblies of columnar neurons in the lobula, the axons of which segregate to project to discrete optic glomeruli in the lateral protocerebrum. This arrangement is much like the fly's olfactory system, in which afferents target uniquely identifiable olfactory glomeruli. Here, whole-cell patch recordings show that even though visual primitives are unreliably encoded by single lobula output neurons because of high synaptic noise, they are reliably encoded by the ensemble of outputs. At a glomerulus, local interneurons reliably code visual primitives, as do projection neurons conveying information centrally from the glomerulus. These observations demonstrate that inDrosophila, as in other dipterans, optic glomeruli are involved in further reconstructing the fly's visual world. Optic glomeruli and antennal lobe glomeruli share the same ancestral anatomical and functional ground pattern, enabling reliable responses to be extracted from converging sensory inputs.

In most insects with olfactory glomeruli, each side of the brain possesses a mushroom body equipped with calyces supplied by olfactory projection neurons. Kenyon cells providing dendrites to the calyces supply a pedunculus and lobes divided into subdivisions supplying outputs to other brain areas. It is with reference to these components that most functional studies are interpreted. However, mushroom body structures are diverse, adapted to different ecologies, and likely to serve various functions. In insects whose derived life styles preclude the detection of airborne odorants, there is a loss of the antennal lobes and attenuation or loss of the calyces. Such taxa retain mushroom body lobes that are as elaborate as those of mushroom bodies equipped with calyces. Antennal lobe loss and calycal regression also typify taxa with short nonfeeding adults, in which olfaction is redundant. Examples are cicadas and mayflies, the latter representing the most basal lineage of winged insects. Mushroom bodies of another basal taxon, the Odonata, possess a remnant calyx that may reflect the visual ecology of this group. That mushroom bodies persist in brains of secondarily anosmic insects suggests that they play roles in higher functions other than olfaction. Mushroom bodies are not ubiquitous: the most basal living insects, the wingless Archaeognatha, possess glomerular antennal lobes but lack mushroom bodies, suggesting that the ability to process airborne odorants preceded the acquisition of mushroom bodies. Archaeognathan brains are like those of higher malacostracans, which lack mushroom bodies but have elaborate olfactory centers laterally in the brain.

Within the Arthropoda, morphologies of neurons, the organization of neurons within neuropils and the occurrence of neuropils can be highly conserved and provide robust characters for phylogenetic analyses. The present paper reviews some features of insect and crustacean brains that speak against an entomostracan origin of the insects, contrary to received opinion. Neural organization in brain centres, comprising olfactory pathways, optic lobes and a central neuropil that is thought to play a cardinal role in multi-joint movement, support affinities between insects and malacostracan crustaceans.

The moth Spodoptera littoralis, is a major pest of agriculture whose olfactory system is tuned to odorants emitted by host plants and conspecifics. As in other insects, the paired mushroom bodies are thought to play pivotal roles in behaviors that are elicited by contextual and multisensory signals, amongst which those of specific odors dominate. Compared with species that have elaborate behavioral repertoires, such as the honey bee Apis mellifera or the cockroach Periplaneta americana, the mushroom bodies of S. littoralis were originally viewed as having a simple cellular organization. This has been since challenged by observations of putative transmitters and neuromodulators. As revealed by immunocytology, the spodopteran mushroom bodies, like those of other taxa, are subdivided longitudinally into discrete neuropil domains. Such divisions are further supported by the present study, which also demonstrates discrete affinities to different mushroom body neuropils by antibodies raised against two putative transmitters, glutamate and gamma-aminobutyric acid, and against three putative neuromodulatory substances: serotonin, A-type allatostatin, and tachykinin-related peptides. The results suggest that in addition to longitudinal divisions of the lobes, circuits in the calyces and lobes are likely to be independently modulated.

SummaryIn the eye, visual information is segregated into modalities such as color and motion, these being transferred to the central brain through separate channels. Here, we genetically dissect the achromatic motion channel in the fly Drosophila melanogaster at the level of the first relay station in the brain, the lamina, where it is split into four parallel pathways (L1-L3, amc/T1). The functional relevance of this divergence is little understood. We now show that the two most prominent pathways, L1 and L2, together are necessary and largely sufficient for motion-dependent behavior. At high pattern contrast, the two pathways are redundant. At intermediate contrast, they mediate motion stimuli of opposite polarity, L2 front-to-back, L1 back-to-front motion. At low contrast, L1 and L2 depend upon each other for motion processing. Of the two minor pathways, amc/T1 specifically enhances the L1 pathway at intermediate contrast. L3 appears not to contribute to motion but to orientation behavior.

Since the 1970s, human subjects that have undergone corpus callosotomy have provided important insights into neural mechanisms of perception, memory, and cognition. The ability to test the function of each hemisphere independently of the other offers unique advantages for investigating systems that are thought to underlie cognition. However, such approaches have been limited to mammals. Here we describe comparable experiments on an insect brain to demonstrate learning-associated changes within one brain hemisphere. After training one half of their bisected brains, cockroaches learn to extend the antenna supplying that brain hemisphere towards an illuminated diode after this has been paired with an odor stimulus. The antenna supplying the naive hemisphere shows no response. Cockroaches retain this ability for up to 24 h, during which, shortly after training, the mushroom body of the trained hemisphere alone undergoes specific post-translational alterations of microglomerular synaptic complexes in its calyces. © 2007 Wiley Periodicals, Inc. Develop Neurobiol, 2007.

Survival and reproduction entail the selection of adaptive behavioural repertoires. This selection manifests as phylogenetically acquired activities that depend on evolved nervous system circuitries. Lorenz and Tinbergen already postulated that heritable behaviours and their reliable performance are specified by genetically determined programs. Here we compare the functional anatomy of the insect central complex and vertebrate basal ganglia to illustrate their role in mediating selection and maintenance of adaptive behaviours. Comparative analyses reveal that central complex and basal ganglia circuitries share comparable lineage relationships within clusters of functionally integrated neurons. These clusters are specified by genetic mechanisms that link birth time and order to their neuronal identities and functions. Their subsequent connections and associated functions are characterized by similar mechanisms that implement dimensionality reduction and transition through attractor states, whereby spatially organized parallel-projecting loops integrate and convey sensorimotor representations that select and maintain behavioural activity. In both taxa, these neural systems are modulated by dopamine signalling that also mediates memory-like processes. The multiplicity of similarities between central complex and basal ganglia suggests evolutionarily conserved computational mechanisms for action selection. We speculate that these may have originated from ancestral ground pattern circuitries present in the brain of the last common ancestor of insects and vertebrates.

Within invertebrate neuroscience, it is without question the nervous system of insects that is most intensely studied. This chapter summarizes our knowledge about structure and function of the insect brain in close comparison with that of the closest insect relatives, the crustaceans. Major subsystems of the insect brain include the visual neuropils, the central olfactory pathways, the central complex and the mushroom bodies. The structures of these subsystems are described in detail, including instructive wiring diagrams summarizing inputs and outputs as well as known interneuronal connections. A detailed knowledge of the insect brain’s architecture provides insights into how these systems may function as a whole to generate coordinated behaviours.

Four types of eyes serve the visual neuropils of extant arthropods: compound retinas composed of adjacent facets; a visual surface populated by spaced eyelets; a smooth transparent cuticle providing inwardly directed lens cylinders; and single-lens eyes. The first type is a characteristic of pancrustaceans, the eyes of which comprise lenses arranged as hexagonal or rectilinear arrays, each lens crowning 8-9 photoreceptor neurons. Except for Scutigeromorpha, the second type typifies Myriapoda whose relatively large eyelets surmount numerous photoreceptive rhabdoms stacked together as tiers. Scutigeromorph eyes are facetted, each lens crowning some dozen photoreceptor neurons of a modified apposition-type eye. Extant chelicerate eyes are single-lensed except in xiphosurans, whose lateral eyes comprise a cuticle with a smooth outer surface and an inner one providing regular arrays of lens cylinders. This account discusses whether these disparate eye types speak for or against divergence from one ancestral eye type. Previous considerations of eye evolution, focusing on the eyes of trilobites and on facet proliferation in xiphosurans and myriapods, have proposed that the mode of development of eyes in those taxa is distinct from that of pancrustaceans and is the plesiomorphic condition from which facetted eyes have evolved. But the recent discovery of enormous regularly facetted compound eyes belonging to early Cambrian radiodontans suggests that high-resolution facetted eyes with superior optics may be the ground pattern organization for arthropods, predating the evolution of arthrodization and jointed post-protocerebral appendages. Here we provide evidence that compound eye organization in stem-group euarthropods of the Cambrian can be understood in terms of eye morphologies diverging from this ancestral radiodontan-type ground pattern. We show that in certain Cambrian groups apposition eyes relate to fixed or mobile eyestalks, whereas other groups reveal concomitant evolution of sessile eyes equipped with optics typical of extant xiphosurans. Observations of fossil material, including that of trilobites and eurypterids, support the proposition that the ancestral compound eye was the apposition type. Cambrian arthropods include possible precursors of mandibulate eyes. The latter are the modified compound eyes, now sessile, and their underlying optic lobes exemplified by scutigeromorph chilopods, and the mobile stalked compound eyes and more elaborate optic lobes typifying Pancrustacea. Radical divergence from an ancestral apposition type is demonstrated by the evolution of chelicerate eyes, from doublet sessile-eyed stem-group taxa to special apposition eyes of xiphosurans, the compound eyes of eurypterids, and single-lens eyes of arachnids. Different eye types are discussed with respect to possible modes of life of the extinct species that possessed them, comparing these to extant counterparts and the types of visual centers the eyes might have served.