The Divergent Evolution of Arthropod Brains: Ground Pattern Organization and Stability Through Geological Time
Abstract and Keywords
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.
When we talk about arthropods, if ever we do, most of us refer to exotic animals such as dragonflies; or edible ones like lobsters, or those that elicit more ambivalent reactions such as spiders and scorpions. Scant attention is paid to whether these animals have brains, aside from a vague awareness of some of the most advertised facts of insect behavior: that honeybees communicate with each other by dancing; or that when a female praying mantis devours the head of her copulating partner, she releases more vigorous action by his surviving end. With few exceptions, most of us are oblivious that arthropod behavior is marvelously varied and that this variation derives from brains that are diverse and exquisitely organized—so organized that they may be at least as elaborate in terms of their computational parts as is the brain of a small mammal.
In the 19th and early 20th centuries, some scientists seriously suggested that the brain and its connected ganglia in an annelid or an arthropod, both of which are segmented invertebrates, correspond to the brain and spinal cord of vertebrates, despite that the ganglionic chain in invertebrates is disposed beneath the gut, whereas in vertebrates the spinal cord lies above it. This idea of inverted correspondence, first proposed in 1820 by the French anatomist Geoffroy St. Hilaire as a “unity of plan,” was vehemently contested and those who espoused it were ignored, if not regarded with contempt (Strausfeld, 2010). But the idea that the vertebrate body plan (and hence the nervous system) might be an inverted version of that of the arthropod, or an annelid, is not easily dispelled (De Robertis & Sasai, 1996; Nagao et al., 1998; Tsubouchi et al., 2017). And even though the enormous variation in the disposition of nerve cords amongst invertebrates, particularly in Spiralia (including annelids, mollusks, Platyhelminthes, and Gastrotricha), may speak for convergent evolution of the bilaterian ventral nervous system (Martín-Durán et al., 2017), genetic and developmental studies nevertheless suggest that not only do the brains of arthropods and vertebrates appear to correspond regarding their segmental organization, but that various centers in their forebrains may phenotypically, even genotypically, correspond (Hirth & Reichert, 1999; Hirth et al., 2003; Finkelstein et al., 2005; Tomer et al., 2010; Strausfeld & Hirth, 2013; Joly et al., 2016).
Irrespective of whether such similarities are due to genealogical correspondence or whether they are extraordinary examples of convergent evolution, what matters is that regardless of whether cerebral complexity evolved once or often we should pay attention to the historical record of such evolution. And as the fossil record of arthropod diversification extends so far back in time, it is the arthropods that currently provide a wealth of information, and controversy, associated with explorations of brain evolution at many levels - from how the gross arrangements of brain segments define major arthropod lineages, to whether neural arrangements shared by distantly related species are homologous or examples of convergent evolution (Strausfeld & Hirth, 2013; Edgecombe et al., 2015; Strausfeld et al., 2016a; Wolff & Strausfeld, 2016). This chapter considers some of those explorations.
Arthropods are today referred to as the superphylum Panarthropoda. It consists of Euarthropoda comprising Chelicerata, Myriapoda, and Pancrustacea, all of which have jointed legs, and two related groups sometimes accorded their own status as phyla: Onychophora and Tardigrada, which have unjointed, lobe-like legs (Dunn et al., 2008). Species belonging to Panarthropoda possess a segmented body, paired legs, and a ventral or ventrolateral nervous system originating from a dorsal brain or, as in Tardigrada, an apical “circumpharyngeal” brain, the synaptic neuropil of which encircles the front of the gut (Smith et al., 2017). The status of the tardigrade brain is discussed in the final part of this chapter.
Euarthropods are found in almost every conceivable habitat, from volcanic vents in the ocean to Himalayan glaciers, and as parasites living on or in other organisms. From the lower Cambrian, over 520 million years ago, Euarthropoda has diversified to become the most species-rich animal group, dominated now by its subphylum Pancrustacea comprising about 4 million hexapod species (Hamilton et al., 2010) and about half a million crustacean species. The latter, and their extinct ancestors, have existed far longer than hexapods, which originated from within Crustacea, probably first colonizing land in the Ordovician (Lozano-Fernandez et al., 2016: Rota-Stabelli et al., 2013). Pancrustacea and its sister taxon Myriapoda (which includes centipedes and millipedes) are grouped together as Mandibulata due to their common possession of a specialized cutting surface on the inner edge of the first article (coxa) of their paired second postantennular appendages (Edgecombe, 2017). These originate from the fourth body segment (segment numbers beginning with the most rostral head segment, the protocerebrum, denoted as the first segment). Notably, although many hexapod species obtain nourishment not by cutting but by sucking or piercing, their mandibles are nevertheless key elements for “structural interaction” with other mouthparts to provide the appropriate mechanics (Blanke et al., 2015). Mandibulate arthropods are distinct from the other major euarthropod subphylum Chelicerata, which lack mandibulate mouthparts. Chelicerata consists of Merostomata (four species of Limulidae or “horseshoe crabs”), Pycnogonida (sea spiders), and about 112,000 species of Arachnida (Zhang, 2011). The last includes scorpions, spiders, ticks, and mites in addition to other more exotic animals, such as the acetic-acid-squirting Thelyphonida or “whip scorpions.”
Panarthropods belong to Ecdysozoa, animals that molt, discarding and rebuilding their exoskeletons as they grow (Aguinaldo et al., 1997). That their organs reside inside a supporting skeleton means that under conditions amenable to exceptional preservation fossils can also reveal petrified internal organs, such as digestive tracts, associated glands, reproductive organs, muscles, circulatory systems, and, in the rarest of cases, brains and ventral nervous systems (Parry et al., 2017). It is the latter that provide vital clues about the early divergence of euarthropod brains and about the extent to which such early arrangements have persisted through an immense span of time (Edgecombe et al., 2015; Strausfeld et al., 2016).
Simply viewing the heads of euarthropods informs us about some of their cardinal distinctions. For example, mandibulates differ from chelicerates in that in the former, the second (deutocerebral) segment is equipped with a pair of uniramous antennules: appendages usually consisting of numerous annuli, on which occur porous sensilla containing the dendrites of olfactory receptor neurons. Antennules do not exist in chelicerates; their deutocerebral segment bears a pair of chelicerae, which are the segmental homologues of antennules. But rather than composed of annuli, chelicerae consist of two or three articles (“segments”) ending in a claw or scissor-like configuration. Whereas antennules are odorant-sensing organs, chelicerae are organs used in feeding; terrestrial chelicerates tear apart their prey, dribble digestive juices on the pieces, and ingest the soup. Mandibulates chew or suck. Recently obtained genetic evidence (Sharma et al., 2015; Setton et al., 2017) suggests that antennules originated later in arthropod evolution than the chelicera-like deutocerebral appendages that are a defining feature of stem arthropods called Megacheira, described later.
A further distinction refers to the visual system. Pancrustaceans and myriapods (centipedes and millipedes) possess a single pair of eyes. These comprise many optical units called ommatidia. In Pancrustacea, and in the basal myriapod order Scutigeromorpha (Müller et al., 2003), each ommatidium is surmounted by a lens that is secreted by a quartet of cone cells, a feature bestowing to Mandibulata the alternate name “Tetraconata” (Dohle, 2001). Chelicerates have two pairs of eyes, an arrangement that is not immediately obvious. Horseshoe crabs have a pair of lateral compound eyes and a pair of smaller dorsally disposed single-lens eyes. No other chelicerate has compound eyes, although the now extinct sea scorpions (Eurypterida) did and, as in horseshoe crabs, their compound eyes were situated laterally and the paired single-lens eyes dorsally. In today’s scorpions, the lateral eyes have fragmented into three pairs of single-lens eyes, accompanied by the one pair of frontal eyes (there are also light-sensitive organs on caudal segments). The same configuration is seen on the head of spiders where there is usually a large frontal viewing pair and three smaller lateral pairs (Strausfeld et al., 2016b).
Although chelicerates have evolved a variety of distinctive morphologies that allow most of us to distinguish a spider from a scorpion or its relatives, it is Pancrustacea that has evolved the most stunning morphological diversity, evidenced not only by tagmatization, where trunk segments can be grouped to serve specialized functions, such as the second and third thoracic segments in insects the muscles of which serve flight or, in stomatopod crustaceans, ganglia that are grouped together to serve a set of raptorial and affiliated appendages (Fig. 1, left), but also a huge variety of body shapes, cuticular decorations, and specialized appendages, including the aforementioned key innovation of insects, their wings. The evolutionary exuberance of pancrustacean morphologies, especially in the ocean, reflects not only the ecological radiation of this group but is also relevant to their stunning range of individual and collaborative behaviors (Derby & Thiel, 2014; Matthews & Matthews, 2010). For example, both crustaceans and insects have evolved eusociality with the development of caste systems and caste behaviors. Whereas eusocial crustaceans (species of pistol shrimps, Alpheoidea) convert sponges into group domiciles (Duffy, 1996; Duffy et al., 2000), insects have gone further in constructing their own elaborate architectures, such as the hives of social bees and wasps, the underground metropolises of harvester ants, or the iron-hard towers of certain species of termites (Wilson & Hölldobler, 2005).
Species of both Chelicerata and Pancrustacea can migrate as accurately as do vertebrates, some over great distances (Swan, 2005; Reppert et al., 2016), and they can learn and remember places, events, and directions. As do certain species of paper wasps (Tibbetts & Lindsay, 2008), mantis shrimps remember conspecifics with which they have had aversive or nonaversive encounters (Caldwell, 1992). Crustaceans, and many species of insects, exhibit exquisite motor control in running, climbing, and swimming. Such behaviors require a brain that can process many sensory modalities, some of which are utterly foreign to us (Cronin et al., 2006; Templin et al., 2017). Euarthropod brains are equipped with centers that memorize places, territories and features, conspecifics, and the behavior of others. Predatory behaviors include trap line-foraging, stalking, ambushing, and parasitoidism, in which the huntress is obliged to observe and remember numerous locations of potential hosts on which to lay her eggs (Rosenheim, 1987; Lihoreau et al., 2012; Collett et al., 2013). Across Euarthropoda, the many examples of courtship and rivalry behaviors are endlessly fascinating and diverse, with male salticids (jumping spiders) supreme, having evolved flamboyant visual and percussive displays (Elias et al., 2005; Girard et al., 2011).
How Conserved Are Arthropod Brains?
Behavioral repertoires are driven and controlled by brains. But is such variety of behaviors reflected by as profuse a diversity of brains and nervous systems? To what degree does the brain of a stomatopod crustacean—a raptorial marine predator—resemble or differ from that of a praying mantis, the iconic insect predator; or its cousin the cockroach, a winged terrestrial detritivore? Is the visual system of a salticid spider, which has acute color perception and motion detection, comparable to that of an insect that uses both color perception and the precise registration of visual motion to stabilize its directional flight and locate targets?
A couple of now famous studies published early in the 20th century by two Swedish scientists, Nils Holmgren and Bertil Hanström (Holmgren, 1916; Hanström 1926), were the first to suggest that the arrangement of centers in arthropod brains reflects a surprisingly limited number of divergent motifs and that each motif defines a specific group of arthropods. Such essential arrangements are today referred to as “ground patterns,” a set of plesiomorphic morphological characters traceable through a group’s ancestry (Scholtz, 2004). Holmgren and Hanström anticipated this idea in proposing that arthropod central nervous systems are represented by just a few cerebral characters, each comprising a few prominent centers, the arrangements of which represented divergent evolutionary trajectories: brains of Myriapoda are distinct from those of Crustacea and Hexapoda, for example, yet originate from a common ancestor that was distinct from the ancestor of Chelicerata. The proposition was that five or six ground cerebral patterns typify the major arthropod groups: Onychophora, Chelicerata, and the three mandibulate lineages, Myriapoda, Crustacea and Hexapoda, with trilobites occupying a basal position (Holmgren, 1916). Here, I will consider brain evolution within these clades, reviewing what is currently known about the early divergence of the chelicerate and mandibulate brain with reference to fossil evidence. This has led to the recognition that ancient ground patterns recognized in the brains of today’s arthropods have not essentially changed for over half a billion years (Strausfeld et al., 2016).
The Earliest Arthropods
Together, molecular clock data and paleontological observations that resolve ancient nodes of species divergence place the origin of euarthropods at the end of the Ediacaran or the base of the Cambrian (Rehm et al., 2011; Edgecombe & Legg, 2014). Molecular dating methods estimate dates of divergence of Onychophora and Euarthropoda from a common ancestor as the late Ediacaran (Peterson et al., 2008; Rota-Stabelli et al., 2011; 2013). Although, as yet, no fossils of animals have been found to support the molecular divergence data, trace fossils reveal important aspects of behaviors of animals that, with a few notable exceptions such as the mollusk-like Kimberella (Fedonkin & Waggoner, 1997) or the enigmatic Keretsa brutoni (Ivantson, 2017), were likely to have been simple, and vermiform. As the term suggests, trace fossils are animal tracks resolved as serial indentations, elongated swellings, or grooves preserved on slabs of sedimentary rock (see Buatois & Mángano, 2016). Up to near the end of the Ediacaran such tracks were simple, revealing nothing more interesting than meandering pathways (Jensen, 2003). But quite abruptly, just prior to the beginning of the Cambrian, such tracks assume very different characteristics. They cease to be confined to two dimensions. Animals clearly burrowed, suggesting a radical change from two- to three-dimensional habitats that reflect novel properties of sea bed ecology (Vannier et al., 2010; Budd & Soren, 2017). Some tracks show records of possible predator–prey encounters: one track turning sharply away from a second, suggesting an aversive response. Other tracks reveal that an organism returned to a site it had already visited, suggesting recall of a place. Other fossilized records are indicative of systematic searching, actions that were selected in response to an external or internal stimulus (Raup & Seilacher, 1969). Today, Drosophila larvae foraging on a substrate employ similar strategies.
The larval Drosophila nervous system is equipped with a miniscule brain containing paired centers called “mushroom bodies” that are required for the formation of associative memory (Waddell, 2013; Rohwedder et al., 2016; Saumweber et al., 2018), and a midline center called the central complex that in the adult insect mediates action selection (Guo & Ritzmann, 2013). Those centers, both of which are constrained within the most anterior brain segment, the protocerebrum, are not as intricate in larvae as they are in adults, yet each conforms to a characteristic ground pattern arrangement of neurons that is first expressed in the embryo (Williams et al., 2005; Young & Armstrong, 2010; Eichler et al., 2017). Subjected to genetic manipulation, both centers reveal their participation in foraging behaviors and acquiring memory of a source of nourishment (Varnam et al., 1996; Kaun et al., 2007). In their simplest manifestation, as in the tiny soil inhabiting hexapods called Collembola, such centers can be composed of just a few score neurons (Kollmann et al., 2011). Comparable centers are also found in certain annelids, segmented animals belonging to the superphylum Lophotrochozoa, and in flatworms (also belonging to Spiralia), which are asegmental (Wolff & Strausfeld, 2015a). It is reasonable to postulate that what defined the ancestral apical brain may have been circuits, such as those comprising the simplest central complexes and mushroom bodies that decide what actions are best suited to sensory events, and circuits that learn about them.
The first evidence for what were likely bilaterian animals with jointed appendages is the trace fossil Rusophycus, assumed to be an imprint of a resting trilobite, dated to 528 million years ago (Mya) (Budd & Jensen, 2000; Wolfe et al., 2016). Fossils of recognizably segmented animals with jointed limbs are recovered from sedimentary rocks dating to about 520 Mya. These are indeed trilobites, euarthropods recognized by their characteristic external organization (Lieberman & Karim, 2010): a body divided into a rostral head-like structure called a “cephalon” attached to a robust “thorax,” followed by a set of distinctive terminal segments, the opisthothorax and “pygidium” followed by a single terminal element (Hughes, 2003). The cephalon is characterized by a medially raised part (the glabella) flanked by a system of lobes and sutures and, in many species, compound eyes. The trilobite thorax consists of a series of almost identical segments, the number of which relates to the animal’s age (Hopkins, 2017). The dorsal plate of each segment has a medial hump aligned with the glabella in front. In many species, flange-like “pleura” from each plate taper outward often as spinose extensions. Also, in many species, the dorsal surface of each tergum is decorated with embellishments, mostly spiny and as elaborately contorted as is a Jugendstil wrought iron balcony. These structures and the ability of trilobites to roll up into a defensive posture suggest that throughout their history many trilobite species were subject to intense predation that drove the evolution of such modifications (Esteve et al., 2011; Rustan et al., 2011).
In many respects, trilobites possess the simplest euarthropod body plan (Fig. 1, right). A five-segmented, “head” called the cephalon, carried a pair of lateral compound eyes, the ancestral apposition optics of which subsequently evolved in many trilobite lineages to become very different from those of pancrustaceans (for a description of ancestral – “holochroal” – and derived eye types see: Clarkson et al., 2006; also, Strausfeld et al., 2016b). A single pair of annulated unbranched (uniramous) antennules originated from behind the eyes in the deutocerebral segment and extended forward from beneath the head shield. Immediately following the origin of the antennules there are three pairs of biramous limbs, also under the head shield. These are smaller than, but identical to, those equipping all further segments caudally, diminish in size towards the rear end (Hughes, 2003). The limbs are representative of the euarthropod appendicular ground pattern (Boxshall, 2004): an outer branch, the exopod (which in trilobites is lobate, fringed by lamellate gills); and an inner branch, the telopod which likely acted as the walking appendage. The repeat (homonomous) arrangement of identical limbs is considered the ancestral organization, from which other variants of limb diversification have evolved (Boxshall, 2004). Although trilobites show evidence of local segmental differentiation in the trunk region, revealing they had evolved tagmosis (Hughes, 2003), trilobites may have lacked those elements of genetic networks that, particularly in Pancrustacea, determine the enormous diversity of appendicular morphologies (see Tweedt, 2017). Trilobites existed for about 300 million years from the lower Cambrian until their comprehensive extinction at the end of the Permian.
The Earliest Recognizable Fossil Brains
Despite their plentiful fossil record we know nothing about the trilobite central nervous system. And this is unlikely to change because trilobite exoskeletons were calcareous and robust, thereby inimical to the preservation of soft tissue. It is other euarthropods such as Fuxianhuiidae and Leanchoiliidae, which had soft uncalcified exoskeletons, that provide crucial insights into the early divergence of euarthropod nervous systems (Ma et al., 2012; Tanaka et al., 2013; Yang et al., 2016). The importance of these fossils (Figs. 2–4) is that because their central nervous system ground patterns are so similar to those of extant groups (Fig. 5), it is possible to approximate when the central complex and mushroom bodies likely underwent divergent transformation from an ancestral morphology to one representative of the four major euarthropod lineages alive today.
Claims that arthropod brains could fossilize (Bergström et al., 2008; Strausfeld, 2011; Ma et al., 2012) is not without controversy, the counterclaim being that nervous tissue is, per se, unsuited to preservation. Thus, before continuing with the description of fossil brains, it is appropriate to briefly digress and consider conditions speaking for and against the fossilization of soft tissues, which include neural, circulatory, contractile, and alimentary systems, and to emphasize the importance of symmetry in identifying bone fide organ systems.
The process of fossilization (taphonomy) has attracted numerous studies that assess conditions required for the preservation of structural fidelity, including that of soft tissue (e.g., Allison & Briggs, 1993; Briggs, 2003; Sansom, 2014). However, it has been claimed that in arthropods neural tissues are one of the earliest to decompose (Murdock et al., 2014). Objections to nervous tissue fossilization called on experiments documenting progressive dissolution of arthropod cadavers, including those of Onychophora, that had been placed undisturbed in receptacles containing salt water. These conditions are, however, far removed from reality in that they omit inundation and obrution (rapid burial) of living specimens by particulate matter. Obrution of the living, anoxia or low-oxygen conditions, and surface cementation of the dead contribute to morphological fidelity in Konservat-Lagerstätten (Seilacher et al., 1985; Briggs, 2003), a term referring to exceptionally preserved soft-bodied fossil assemblages (Seilacher, 1970). Decay experiments are informative with regard as to how chemical and bacterial actions relate to the process of taphonomy and, hence, the interpretation of fossil morphologies (Briggs & Kear, 1993; Butler et al., 2015). And, despite their misrepresentation (Sansom, 2016), experiments have provided evidence that burial can advance neural preservation. Entombing living annelid or pancrustacean nervous system in a slurry of mud and sea water that is then gradually compressed over hours or weeks before drying provides a residuum, the shape of which matches that of living nerve cord or brain (Edgecombe et al., 2015). Indeed, the notion that decaying animals lying on the sea floor might eventually fossilize to provide morphologies at variance with those of the living organism, a claim made for vertebrate and invertebrate fossils (Sansom et al., 2011), neglects the propensity of extant arthropods to scavenge cadavers, which in any event comprise an infrequent food source (Britton & Morton, 1994). It is likely that Cambrian necrophagy was as opportunistic and that cataclysmic burial of living biota provided the best chance of preservation (Conway Morris, 1985; Gaines, 2014).
Analyses of fossilized brains from the Chengjiang Lagerstätte demonstrate their primary composition as carbon (Ma et al., 2015). Identical cerebral arrangements are observed in different specimens of the same species (Ma et al., 2015; Ortega-Hernández, 2015; Park et al., 2018). Other modes of nervous system preservation have been identified, as in a fossilized archaeognathan hexapod from the Triassic (Montagna et al., 2017). The match between fossilized nervous systems and those of extant organisms (Strausfeld et al., 2016) further disqualifies objections arising from decay experiments that inexplicably exclude factors favoring the preservational potential of neural tissue (Murdock et al., 2014). Misleading interpretations of taphonomic events have also been recruited to assert that neural or vascular tissue lacks the potential to fossilize, suggesting instead that it is bacterial biofilms that result in “brain-like” deposits in the fuxianhuiid head (Liu et al., 2018). In featuring those deposits as irregular but unique shapes lacking any indication of bilaterality, Liu et al. (2018) disregard that bilateral symmetry is a key feature defining arthropod organs, including ganglia and brains. In the fuxianhuiid head, bilaterally symmetric carbon residues correspond to flatten pancrustacean cerebra, which as described below reveal paired eyestalks, symmetric visual centers, and paired neural tracts reaching into the antennae (Ma et al., 2015). As recently reviewed by Parry et al. (2017), numerous physical and chemical indicators support the now plentiful examples of “exceptional preservation” of soft tissues in fossils, including central nervous system (Tanaka et al., 2013; Cong et al., 2014; Yang et al., 2016; Park et al., 2018).
The brains and ventral nervous systems of Fuxianhuiidae and Leanchoiliidae had obtained their distinctive ground pattern organization already by the lower Cambrian, 518 million years ago. Also identified are other fossil brains from this time; one comparable to the brains of extant Onychophora occurred in Lyrarapex unguispinus, a member of Radiodonta, the Cambrian’s top predatory taxon (Cong et al., 2014), and another in the predatory species Kerygmachela recovered from the Lower Cambrian Sirius Passet Lagerstätte in northern Greenland (Park et al, 2018).
Fossilized brains have been identified in multisegmented stem euarthropods equipped with grasping deutocerebral appendages, similar to those of Leanchoiliidae but in species that possess just one pair of compound eyes (Strausfeld et al., 2016a,b). These last fossils reveal just two nested optic lobes, comparable to the cerebral organization of the living chilopod Scutigera coleoptrata.
The suggestion that preserved neural tissue existed in Fuxianhuia protensa, one of the early Cambrian’s simplest euarthropods, was originally made by the Swedish paleontologist Jan Bergström in 2008 (Bergström et al., 2008). Re-examination of this specimen along with seven additional specimens of the same species resolved the profile of a brain that is typical of a modern pancrustacean (Fig. 2). A pair of articulated stalked eyes extends in front of a pair of annulated antennules. The eyes and antennules are associated with a brain comprising three fused neuromeres (neuronal segmental units) (Ma et al., 2012, 2015). Fuxianhuia’s eyestalks each house three nested centers corresponding to the pancrustacean visual neuropils, called the lamina, medulla, and lobula; together these denote the brain’s protocerebral segment. The second segment (the deutocerebrum) is denoted by paired nerve trunks extending to the paired uniramous antennules. The contiguous third segment of the brain (the tritocerebrum) supplies nerves to a pair of ventrally disposed caliper-like postantennular appendages. In eucrustaceans this segment is associated with the paired biramous appendages referred to as antennae, or second antennae.
Before continuing further, a word of explanation regarding these terms is in order. Morphologists studying hexapods and myriapods usually refer to the first pair of postocular (deutocerebral) uniramous appendages as the antennae, whereas morphologists studying crustaceans refer to these appendages as the antennules, or first antennae. This dichotomous nomenclature was amplified by the erection in 1972 of the artificial and since (in 1992) discredited phylum “Uniramia,” that grouped Onychophora, Myriapoda and Hexapoda (Manton, 1972; but see Kukalová-Peck, 1992). Throughout this chapter the term antennules is used to refer to deutocerebral appendages of both crustaceans and hexapods. The traditional use of the term antennae is maintained to refer to the biramous second antennae originating from the crustacean tritocerebrum (Boxshall & Jaume, 2013).
The suggestion that Fuxianhuia engaged in active predation comes not only from its powerful caliper-like postantennular appendages but also refers to a unique specimen, in which the preserved cardiovascular system (Fig. 5, middle left) reveals a dense network of vessels within the brain’s volume, from which tributaries extend out to the optic neuropils and compound retina (Ma et al., 2014). Such an arrangement suggests an active animal with a brain requiring a ready supply of oxygen. The body of Fuxianhuia was extremely simple, however, being tagmatized into a 16-segmented trunk equipped with as many paired biramous appendages, followed by a tapering 13-segment “abdomen” that terminated as a three-spine telson (Fig. 2). A study of another fuxianhuiid species has identified a serial arrangement of ganglia belonging to a ladder-like ventral nervous system flanked by many hundreds of lateral traces (Yang et al., 2016). The authors proposed these to be the remnants of nerve bundles indicative of an ancestral “orthogon,” an arrangement typical of an aganglionic nervous system in which nerves extending from the ventral (or in some species lateral) cords are arranged as rings encircling the mesoderm. This organization typifies many cycloneuralian ecdysozoans such as priapulids, and it is also found in Onychophora, arthropods characterized by numerous lobed appendages and a lateroventral nervous system lacking discrete ganglia yet possessing discrete sensory-motor domains that obviously reflect the body’s segmentation (Rothe & Schmidt-Rhaesa, 2010; Whitington & Mayer, 2011; Martin et al., 2017).
Fuxianhuiid brains are preserved as dark mirror-symmetrical deposits composed of carbon films that in some specimens are secondarily coated with minute pyrite crystalline assemblages (Ma et al., 2015). Fuxianhuia protensa possesses the cerebral ground pattern of a mandibulate euarthropod (Fig. 2), and related species of Fuxianhuiidae have provided the first evidence in any euarthropod of gnathobasic protopodites (Yang et al., 2018), heralding the characteristic cutting edge that will typify Mandibulata, However, the 10-million-years-younger species Waptia fieldensis dating to 508 Mya, which also possessed traces of a tripartite brain and three nested optic centers, shows clear evidence of paired mandible-like second postantennular appendages (Strausfeld, 2016; Fig. 1 center). So, too, does the more recently described stem euarthropod Tokummia katalepsis (Aria & Caron, 2017). As were trilobites, and as are insects and myriapods, these two species were equipped with a single pair of antennules. This contrasts with all crustaceans, which are defined by the possession of paired antennules (first antennae) and a second pair of biramous antennae (second antennae) arising from the third head segment, the tritocerebrum. Present in all crustacean groups, these serve a great variety of sensory and motor functions (see Boxshall & Jaume, 2013).
Waptia fieldensis is one of many beautifully preserved species of stem euarthropods whose abundance and variety inspired the notion of the “Cambrian explosion” (Erwin & Valentine, 2013), a period of rapid morphological diversification but of uncertain beginning and duration (Budd & Jensen, 2000). The presence of a postantennular (tritocerebral) segment lacking paired appendages in Waptia is a puzzle. Classical morphologists term this appendage-free third segment in insects and myriapods the “intercalary segment,” which in those groups is immediately anterior to the eponymous segment providing the paired mandibles. The transient expression during insect development of the limb-determining gene distal-less defines the intercalary segment as ancestrally appendicular (Diederich et al., 1991). The absence of the second antenna pair in Waptia (Fig. 1, center), and in Tokummia katalepsis, may suggest that the loss of the tritocerebral appendages occurred several times during the Cambrian. Neither Waptia nor the bizarre Tokummia look remotely like hexapods. But this may not have any significance at all. Today, blind, cave-dwelling and homonomously segmented Remipedia (“paddle footed”) are identified by molecular phylogeneticists as the crustacean sister taxon of Hexapoda.
Yet living remipedes can hardly look less like a hexapod; and they are unequivocally crustacean, equipped with biramous antennae and a brain that corresponds to that of a eumalacostracan (Fanenbruck et al., 2004). Molecular dating puts the time of divergence of the remipede and hexapod trajectories in the upper Cambrian (Oakley et al., 2013; Schwentner et al., 2017); but what the ancestor of Remipedia + Hexapoda, or the ancestor of Hexapoda alone looked like is open to conjecture. Possibly, Waptia was less than remotely related to the hexapod stem.
But what about Trilobita? Their paired antennules, one pair of eyes, and homonomous postantennular appendages all support the interpretation that Trilobita and the related Artiopoda belong to the mandibulate stem group (Scholtz & Edgecombe, 2005; Zeng et al., 2017). Furthermore, as described from lower Cambrian trilobites (Zeng et al., 2017), the first article of the trilobite leg (the coxa) is equipped with rigid saw-tooth serrations reminiscent of those of mandibulate mandibles (Edgecombe, 2017). These also define the coxal edge in Triarthrus eatoni (Fig. 1, left), a beautifully pyritized fossil from the Ordovician Martin Quarry Lagerstätte (Whittington & Almond, 1987). These appendicular features clearly distinguish trilobites and other artiopodans from Megacheira, a class of euarthropods equipped with two pairs of eyes and chelate (pincer-like) postocular appendages, to which Leanchoiliidae belong and from which chelicerates most probably derive (Cotton & Braddy, 2004). The Megacheiran neural ground pattern is considered next.
Megacheirans are a class of extinct tagmatized euarthropods common in the lower Cambrian and persisting until at least the mid-Ordovician (Fig. 3). Thus far there is one exceptionally preserved fossil specimen, Alalcomenaeus, which is bulky yet small enough to permit imaging of its internal organization using X-ray computed tomography and energy-dispersive X-ray fluorescence microscopy. These tools resolve brain and the ventral nervous system (Fig. 4), the arrangements of which are entirely distinct from those of Fuxianhuia (Tanaka et al., 2013). The brain of Alalcomenaeus is composed of three fused cerebral segments connected to several contiguous ganglia in the trunk leading to a system of nerves that extend from the terminal thoracic segment down the length of a short abdomen. The entire nervous system closely approximates that of a young horseshoe crab alive today. Like that of the horseshoe crab, the brain of Alalcomenaeus is supplied by two pairs of eyes set flush with the head cuticle. The eyes are compound, but similar to those of Limulus, in which cones extending inward from the cuticle provide the focusing lenses (Exner, 1891; Land, 1979; Strausfeld et al., 2016b). In megacheirans, a pair of elongated grasping appendages comparable to the paired chelicerae of extant arachnids, but tapering to delicate annulated extensions, arises from behind the eyes; in Alalcomenaeus their point of origin is reached by nerves extending from the first postocular segment, the deutocerebrum. That the annulated antennules of Fuxianhuiids and the grasping appendages of megacheirans (referred to by paleontologists as “Great Appendages”) are both innervated from the deutocerebrum demonstrates their segmental homology, even though the fossil brain and nervous system of fuxianhuiids and megacheirans distinguish the pancrustacean from the chelicerate nervous system ground patterns. These ground patterns likewise differentiate today’s pancrustaceans and arachnids (Fig. 5).
Origin and Divergence of Forebrain Centers: Protocerebral Architectures
Molecular phylogenetics has confirmed Hanström’s conclusion, derived exclusively from the study of brains, that insects derive from crustaceans (Hanström, 1926; Regier et al., 2005). Crustacea and Hexapoda are today grouped into one phylum, the Pancrustacea. Hexapoda embraces four classes of six-legged arthropods: Insecta, Collembola, Protura, and Diplura.
Except for Protura, hexapods lacking eyes and antennules and so minute that they have so far defied neuroanatomical analysis, studies across Pancrustacea identify a prominent midline neuropil in the brain’s first segment, the protocerebrum. This neuropil is the central body, which in insects and malacostracans is interconnected with about half a dozen identifiable satellite centers. Together this assemblage comprises the “central complex” (Flögel, 1878; Ito et al., 2012). Also present in the brains of all but one hexapod order are the paired mushroom bodies, which in Drosophila and honeybees are recognized as centers supporting learning and memory (Fahrbach, 2006). The exception is Archaeognatha, a clade of flightless hexapods that is the sister group of all other Insecta. Archaeognathan fossils have been claimed from Devonian deposits, which if verified would suggest this taxon is at least 410 million years old (Labandeira et al., 1988). The lack of mushroom bodies in Archaeognatha has led to the suggestion that mushroom bodies in insects are apomorphic, convergent with morphologically identical centers in other arthropod groups, a subject that will be discussed later.
One challenge to ascribing phenotypic correspondence of brain centers, not merely within, say, Pancrustacea, but across the four major panarthropod lineages, is that each group is distinguished by the configuration of its combined cerebral neuropils (Fig. 6). In Chelicerata and Pancrustacea, discrete synaptic neuropils comprising the first segment of the brain, the protocerebrum, are obviously lateralized, whereas they are not in Myriapoda or Onychophora. In those two groups, protocerebral neuropils are generally organized not as discrete territories but as layers that extend heterolaterally across the midline. On the other hand, the chelicerate brain is distinguished from that of a pancrustacean brain in having discrete but densely packed neuropils but with few prominent fiber bundles connecting them; however, segmental ganglia of chelicerates are supplied by many large ipsi- and heterolateral tracts, and their brains provide prominent pathways that extend to the ganglia (Gronenberg, 1990). Surveys across myriapods, arachnids, and pancrustaceans have also noted that the number and arrangement of motor neurons in a segmental ganglion are characteristic of each group, a feature that has helped to dispel the now recondite notion that Myriapoda may be more closely allied to chelicerates than to Pancrustacea (Harzsch et al., 2005).
The Central Body and Central Complex
Despite these overarching distinctions (the Tardigrada are omitted for the present but will be considered later), all four panarthropod groups manifest the two iconic brain centers named at the beginning of this section: the central body, which with satellite neuropils constitutes the “central complex,” and the paired mushroom bodies. Neuromorphological similarities, physiological and pathological resemblances, and corresponding gene expression have been cited to propose that the hexapod (and by inference the panarthropod) central complex genealogically corresponds to the vertebrate basal ganglia that, like the central complex, is required for the organization and coordination of motor actions (Strausfeld & Hirth, 2013). Using the same criteria, mushroom bodies, which are learning and memory centers that support place memory, have been argued to correspond to the vertebrate hippocampus (Wolff & Strausfeld, 2016). Across Panarthropoda, neuronal organization reaches its greatest elaboration and neuronal diversity in the central complex (Strausfeld, 2012), although as shown by developmental studies those many variations can all be referred to the same neuronal ground pattern of axonal growth, called fascicle switching, expressed in embryogenesis—an observation offering strong support for homology (Loesel et al., 2002; Boyan et al., 2015, 2017).
Our current understanding of panarthropod evolution refers to phylogenomics, molecular clock analyses, and fossil evidence, all approaches that provide what is now a plausible timeline for when the euarthropod and onychophoran lineages originated and diverged (Giribet & Edgecombe, 2012; Rota-Stabelli et al., 2013; Edgecombe & Legg, 2014). This means that it is possible to relate certain brain regions recognized today to each of the four corresponding cerebral ground patterns identified in Cambrian fossils: the radiodontan brain corresponding to the onychophoran brain; the megacheiran brain corresponding to chelicerate brains; the fuxianhuiid brain corresponding to the pancrustacean cerebral ground pattern; and the brain of Jianfengia multisegmentalis, and species possessing similar morphology (Strausfeld et al., 2016b), corresponding to the cerebral ground pattern of Myriapoda (Strausfeld et al., 2016a). The times of divergence of these groups suggest when major neuroanatomical transformations occurred to provide the evolution of higher brain centers, exemplified here by the central complexes and mushroom bodies.
Trace fossils from the Ediacaran-Cambrian border suggest the first appearance of Panarthropoda, a timing that agrees with the divergence of onychophoran–euarthropod lineages that molecular dating methods suggest occurred toward the end of the Ediacaran (see dos Reis et al., 2015; Wolfe et al., 2016). Direct fossil evidence for chelicerate-like species, such as Alalcomenaeus described earlier, and stem mandibulates, such as Fuxianhuia protensa, comes from around 518-million-year-old lower Cambrian Lagerstätten. However, the timeline suggested by molecular clock data for the divergence of the onychophoran stem places central complex and mushroom body origins much earlier, before the end of the Ediacaran, and their subsequent divergence to morphologies typical of chelicerates and mandibulates corresponding to the time of appearance of novel marine ecologies occurring from the end of the Ediacaran through to the lower Cambrian, 545 million years ago (Erwin, 2015).
In extant mandibulates, the central complex is denoted by a prominent midline neuropil that in Myriapoda consists of a layered region of densely packed columnar neurons that stands out against other layered neuropils extending across the whole brain. The morphology of the myriapod central body suggests a greater affinity with the central bodies (“arcuate bodies”) of Onychophora and Chelicerata than with those of Pancrustacea (Fig. 7). In crustaceans, the central body can be long, spindle-shaped and composed of up to 18 modules, or it may appear more condensed, comprising eight to nine modules intersected by discrete strata, but fewer than those in insects. Examples are shown in Figure 7. Only one order of insects possesses a simple two-layered central body, similar to that found in some eumalacostracan crustaceans. This is the monocondylic Archaeognatha, the central complex of which is almost identical to that of a caridid shrimp (Strausfeld, 2012). In dicondylic insects, the central body can assume a variety of arrangements, all referring to a fan-like organization of eight to nine synaptic modules that achieves great complexity (Wolff et al., 2015). In species that have pronounced appendicular dexterity these modules are accentuated, whereas in species that are less dexterous they are inconspicuous and may not even be distinguishable, even though homologous neurons compose them (Strausfeld & Hirth, 2013). The insect fan-shaped body is also highly stratified due to layers of terminals provided by neurons from regions of the protocerebrum that, thus far, have escaped detailed analysis (Phillips-Portillo & Strausfeld, 2012; Wolff & Strausfeld, 2015b).
Contrasting with mandibulates, the central complex of chelicerates is arch-shaped, hence its appellation “arcuate body,” composed of palisades of thousands of small interneurons intersected by strata of local interneurons (Strausfeld et al., 1993). As shown in Figure 7, this organization corresponds to the onychophoran arcuate body, particularly when viewed using comparable neuronal markers (see Strausfeld et al., 2006b). It is significant that in both chelicerates and onychophorans one visual pathway extends directly to the arcuate body (Lehmann et al., 2012; Lehmann & Melzer, 2013), whereas in pancrustaceans the central body receives indirect visual input via intermediate relays in the protocerebrum (Strausfeld, 1976; Pfeiffer and Homberg, 2014; Omoto et al., 2017).
Neuroarchitectural equivalence of the onychophoran and chelicerate central bodies identified by conventional histology and immunocytology supports geological and molecular inferences that Chelicerata was the first euarthropod trajectory to branch from the ancestral stem group. The myriapod central complex displays intermediate ancestral-like neuroachitectures; comparable to the columnar arrangement in chelicerates but approaching the condensed midline organization typical of pancrustaceans (Fig. 7). Reflecting its later time of origin (Collette & Hagadorn, 2010), the subphylum Pancrustacea possesses the most derived central body neuroarchitecture denoted by its spindle- or fan-shaped neuronal arrangements (Fig. 8). Divergence within Pancrustacea is also reflected by evolved additions and elaborations of satellite neuropils contributing to the total central complex, such as the protocerebral bridge, which like the central body is also modular and whose axons provide both direct or chiasmatal (or both) projections into the central body (Hanesh et al., 1989). The permutations of these projections are most elaborated in pterygote (winged) insects and, within Crustacea, in Stomatopoda (Wolff et al., 2015; Thoen et al., 2017).
This last-mentioned correspondence is relevant to determining whether neuronal architectures shared by distantly related pancrustacean groups should be viewed as homoplastic (convergent) or genealogically corresponding (homologous). Recent molecular phylogenomics of Pancrustacea resolves Hexapoda as the sister group of Remipedia, thereby placing them phyletically distant from Eumalacostraca, to which Stomatopoda belongs (Dunn et al., 2008; Oakley et al., 2013; Schwentner et al., 2017). Thus, while Pancrustacea (except Cephalocarida; Stegner & Richter, 2011), including Diplura (Bohm et al., 2012), possess a central body, only the stomatopod central body and its associated centers approach the elaboration of the hexapod counterpart. The presence of central complexes across Pancrustacea suggests homology, whereas the comparable elaboration of stomatopod and hexapod central complexes suggests convergent evolution of elaborations of the central body ground pattern. One interpretation for similarities of these centers and associated neuropils in stomatopods and insects may refer to their known roles in insect behavior involving path integration and navigation (Turner-Evans & Jayaraman, 2016) as well as the control of appendicular dexterity relating to the selection of motor actions (Varga et al., 2017). Among crustaceans, the absence of these centers in Cephalocarida has been suggested to reflect the very simple range of movements shown by its species Hutchinsoniella macracantha (Stegner & Richter, 2011) in striking contrast to stomatopods, which are renowned for their versatile behaviors and appendicular control (Vetter & Caldwell, 2015).
As schematized for the central body (Fig. 7), the evolution of mushroom bodies is summarized in Figure 9, upper inset. At first sight the overall shape of the mushroom body ascribed to each lineage offers fewer interpretational challenges. But this is extremely deceptive when taking Crustacea into consideration.
Mushroom bodies are probably the most studied part of the insect nervous system. These paired centers were originally identified in the brains of hymenopteran insects in 1850 by the French polymath Félix Dujardin, who proposed that their functional attributes included cognition (Dujardin, 1850). Application of the Golgi method half a century later showed the defining features of insect mushroom bodies (Kenyon, 1896): precise arrangements of parallel fibers arising from densely packed cell bodies (now called globuli cells or Kenyon cells), converging as a distinctive neck or pedunculus extending in the brain ventrally before dividing into column-like tributaries traditionally referred to as “lobes” (Schürmann, 1973). Branched terminals and dendritic trees belonging, respectively, to input and output neurons intersect parallel fibers, partitioning the columns into discrete territories (Ito et al., 1998; Li & Strausfeld, 1999). In neopteran insects, globuli cell processes that extend as parallel fibers first provide dendritic branches that contribute to a distinct cup or cap-like synaptic neuropil called the calyx, from which the pedunculus emerges. The calyx receives inputs from olfactory neuropil in the second brain segment, the deutocerebrum. These olfactory centers historically referred to as the “antennal lobes” receive inputs from olfactory receptor neurons on the antennules (historically referred to as the antennae of insects and myriapods, as discussed earlier). In many species, the calyx is also supplied by inputs from the optic lobes and from gustatory centers (Gronenberg, 2001). Calyces are absent in paleopteran insects such as Odonata and Ephemeroptera (dragonflies, darters, mayflies), a group much older than Neoptera; yet calyces occur in Thysanura, flightless insects that are the sister group to Paleoptera and Neoptera. As mentioned earlier, mushroom bodies are absent in Archaeognatha, sister group to all other Insecta. Within Neoptera, species that have evolved as aquatic predators have lost olfactory neuropils (mammals that have returned to the marine environment are also anosmic), and their mushroom bodies lack calyces, although there is one exception: in Gyrinidae, mushroom bodies retain the calyces, which are exclusively supplied by inputs from the optic lobe (Strausfeld et al., 2009; Lin & Strausfeld, 2012). Mushroom bodies are further defined in insects by enriched expression of three proteins essential for learning and memory functions in Drosophila (Skoulakis et al., 1993; Skoulakis & Davis, 1996; Wang et al., 1998).
Mushroom bodies have been identified in Myriapoda (centipedes and millipedes) and Chelicerata (arachnids, horseshoe crabs) using the morphological criteria described earlier, including their enriched expression of learning and memory proteins (Wolff & Strausfeld, 2015a). Based on neuroanatomical characters, mushroom bodies have also been identified in Onychophora (Fig. 9; also Strausfeld et al., 2006a, b). Within Chelicerata, Aranaea (spiders) possesses neuroanatomically identified mushroom bodies that lack the aforementioned proteins. Aranean mushroom bodies have been evolutionarily co-opted for visual processing (Strausfeld & Barth, 1993): in spiders, each mushroom body provides parallel fibers that extend across the brain’s midline to interdigitate with those from its contralateral counterpart. Distally, at a level corresponding to the calyces in an insect mushroom body, the aranean mushroom bodies receive retinotopic inputs from the lateral eye laminas via the lateral eye medullas relaying information from the lateral eyes’ achromatic photoreceptors. The aranean mushroom bodies are thus the deepest level of a system that mediates responses to visual motion (Strausfeld & Barth, 1993). Later, this chapter will further compare the organization of visual pathways in araneans and insects, which provide a textbook example of neurological convergence.
Given the almost ubiquitous occurrence of mushroom bodies in the taxa so far discussed, it might be concluded that mushroom bodies are a characteristic feature of Panarthropoda. However, this has been contested because paired higher olfactory centers in the lateral protocerebra of crustaceans were thought to have few if any of the identifying characters of insect mushroom bodies described earlier (Fig. 10). These higher centers in crustaceans are known as the “hemiellipsoid bodies,” a literal translation of Giuseppi Bellonci’s descriptor “corpo emielissoidale” given to reflect their bulbous appearance in the lateral protocerebra of the stomatopod crustacean Squilla mantis (Bellonci, 1882). In all crustaceans that possess eyestalks, the lateral neuropils of the protocerebrum lie immediately proximal to the optic lobes or nearer the base of the eyestalks, as in the land hermit crab Coenobita clypeatus and its cousin, the gigantic coconut crab, Birgus latro. However, in many species the eyestalks are reduced such that the eyes are flush with the cuticle of the protocerebral segment, as they are in insects. Consequently, the optic lobes and the lateral protocerebral neuropils are contained entirely within the head. In 1925, Hanström was the first to point out that the location of the hemiellipsoid body in species with reduced eyestalks corresponds to the location of the calyx of the insect mushroom body (Hanström, 1925); and, like the calyx, the hemiellipsoid body receives its main inputs from bundles of axons belonging to relay neurons that originate in the antennular lobes (historically referred to as the crustacean’s olfactory lobes). Hanström concluded from this that the hemiellipsoid body is the crustacean mushroom body.
Hanström, however, was deceptive with respect to the organization of neurons connecting the olfactory lobes to the hemiellipsoid body. His depictions show relay neurons typifying those of insect “antennal” lobes (homologues of the crustacean olfactory lobes); each with its dendrites localized within a discrete subunit, called a glomerulus. In reality, insect and crustacean olfactory lobes are very differently organized (Schachtner et al., 2005). In insects, the “antennal” lobe is indeed partitioned into discrete islets of synaptic neuropil called olfactory glomeruli. Each glomerulus gives rise to one or more relay neurons, the dendrites of which are constrained to that glomerulus. These “uniglomerular” neurons extend axons to the mushroom body on the same side of the brain. In crustaceans, the olfactory lobes are usually composed of many (sometimes hundreds) small spindle- or wedge-shaped units, also referred to as glomeruli (Harzsch & Hansson, 2008). But their internal organization differs from the insect counterpart in being strictly stratified into an outer and inner zone. Whereas insect olfactory glomeruli are uniquely identifiable, and have species-specific arrangements, crustacean glomeruli are generally uniform. Exceptions are in Phyllocarida and Stomatopoda, where the olfactory lobe’s subunits are not spindle-shaped but approach the insect morphology; and in Remipedia, where glomeruli are ovoid and clustered into groups, much like the arrangements in the insect Periplaneta americana (see Fig. 6F in Stemme et al., 2012 and Fig. 5.39 in Strausfeld, 2012). Despite these occasional similarities, crustacean olfactory lobes are not known to contain neurons with highly restricted dendritic trees. Instead, relay neurons, some of great complexity, branch profusely to extend dendritic processes into all or most of the olfactory lobe’s glomeruli (Schmidt & Ache, 1996; Schmidt, 2016). Relay neuron axons from the lobes ascend to the medial protocerebrum, where they bifurcate to send an axonal branch to both lateral protocerebra. These branches then terminate in various parts of the hemiellipsoid bodies, as well as in other defined neuropils of the lateral protocerebra. The organization of terminals, and the degree to which they innervate these neuropils, differs across species, with the eumalacostracans showing the greatest diversity (Sullivan & Beltz, 2004, 2005).
Uncertainty as to whether the hemiellipsoid bodies are the crustacean homologues of the insect mushroom bodies derives from two sources. One is the absence of mushroom bodies (and indeed a hemiellipsoid body) in the brain of Archaeognatha, the monocondylic sister taxon of all other insects. The absence of mushroom bodies in this most “basal” insect clade has been taken to suggest that mushroom bodies evolved independently in Hexapoda and are thus an apomorphy convergent with similar centers observed in Myriapoda and Chelicerata (Farris, 2013). Another uncertainty arises from studies of the remipede brain. Its hemiellipsoid body shows no evidence of a mushroom body-like organization. But because molecular phylogenetics insist that Remipedia is the sister clade of Hexapoda, the absence of a lobed center has also been used to argue that Hexapoda independently evolved the characteristic lobed morphology of the mushroom body (Stemme et al., 2016). The argument for apomorphy is weakened, however, by observations of the brain of Diplura, a hexapod group basal to Insecta yet possessing prominent insect-like mushroom bodies (Giribet et al., 2004; Böhm et al., 2012; Beutel et al., 2017). Similarities of these and other cerebral arrangements in malacostracan crustaceans and insects have frequently been ascribed to convergence (e.g. Lozano-Fernandez et al., 2016), although there has been yet no rationale to explain why convergence pertaining to so many brain regions might have been driven by such different ecologies, one marine and the other terrestrial; and the convergentist view has to accommodate observations that the disposition of centers, connections, and neuronal arrangements are the same in Remipedia and Eumalacostraca (Fanenbruck et al., 2004; Stemme et al., 2012; Kenning et al., 2013).
There are, though, many distinctions between the hexapod and crustacean olfactory systems. Foremost is the nature of olfactory receptor neurons. On the crustacean antennules, these express ionotropic receptors (Stensmyr et al., 2005; Corey et al., 2013; Harzsch & Krieger, 2017; Eyun et al., 2017), whereas in insects most olfactory receptor neurons on the antennules are ligand-gated (Sato et al., 2008); each type of odorant receptor neuron is a “specialist,” responding to the identity of one or a few related odorant molecules. The basal monocondylic Archaeognatha is the exception, possessing a crustacean-like ionotropic receptor system (Missbach et al., 2014). In dicondylic insects, during development the axon from each type of genetically determined odorant receptor neuron grows into the brain to occupy a specific olfactory glomerulus in the “antennal” (antennular) lobe. The distribution of olfactory receptor neuron endings in the lobe results in an odortypic map, where each glomerulus receives inputs about a limited range of related odorant molecules (Fishilevich & Vosshall, 2005; Grabe et al., 2016). As remarked earlier, each glomerulus sends its own relays to the mushroom body. Within the insect’s “antennal” lobe each glomerulus is connected to others by systems of local interneurons that integrate information about different odorants to reconstruct specific features of odor space (Marin et al., 2002; Shang et al., 2007).
Nothing like these arrangements has been resolved in crustaceans, and it is still not known why their olfactory (antennular) lobes have so many glomeruli and why their relay and local interneurons appear to provide a massively all-to-all system of connections. Might the crustacean olfactory lobe have to learn by experience to distinguish features of its odor space, whereas the insect “antennal” lobe is hard-wired to reconstruct odors from a limited range of detectable odorant molecules? In the adult insect, the number of “antennal” lobe neurons is finite, in decapod crustaceans the adult olfactory lobe is continuously supplied with newly generated neurons (Sandeman et al., 2011). In insects, each glomerulus corresponds to a population of genetically determined olfactory receptor neurons receptive to a specific range of odorant ligands. Insects such as social Hymenoptera that detect a vast range of odorants can possess hundreds of glomeruli, whereas others whose behaviors are driven by fewer odorants possess fewer glomeruli. No such relationships exist in crustaceans, where ionotropic olfactory receptor neurons innervate several glomeruli (Tuchina et al., 2015).
These distinctions between the crustacean and insect olfactory systems have reinforced the view that although the dome-like hemiellipsoid bodies of crustaceans serve the same function as the insect mushroom body in integrating chemical, haptic, and visual information (Mellon et al., 1992; Schmidt & Mellon, 2011), they are so structurally distinct from each other as to have entirely different origins. Yet, like the mushroom body, the hemiellipsoid body neuropil is situated at a corresponding location in the lateral protocerebrum and is supplied by many thousands of minute globuli cells. Unlike a mushroom body, the hemiellipsoid body neuropil is folded into different domains, hillocks, and sulci and divided into discrete territories. Lobes and parallel fibers appear to be absent.
But appearances belie: mushroom bodies do indeed exist in crustaceans. They were already identified in Bellonci’s 1882 study of Squilla mantis, where he illustrates lobes extending from the “corpo emielissoidale,” naming these the “corpo allungato.” These observations were almost completely forgotten other than a brief mention by Hanström in 1925. Also forgotten was Bellonci’s conclusion that “the hemiellipsoid body continues as an elongated body located transversely in the posterior-lower part of the optic ganglion. This unique body completely assumes the shape of the pedunculus of the insect mushroom body” (Bellonci, 1882, page 42, lines 8–11). More than a dozen independent neuroanatomical characters support this phenotypic correspondence of the insect mushroom body and Bellonci’s stomatopod mushroom body (Wolff et al., 2017). It is now recognized that the stomatopod lateral protocerebrum contains a massive calyx-like structure surmounting one of four distinct columns (lobes), each consisting of many thousands of parallel processes intersected by terminal arborizations and dendritic trees (Wolff et al., 2017). These impart orthogonal arrangements of synaptic networks that are arranged serially along the lengths of the columns, as they are in the insect mushroom body lobes (Ito et al., 1998; Li & Strausfeld, 1999). Close eumalacostracan relatives of stomatopods have also been identified that have enormous hemiellipsoid bodies, from which extend columnar arrangements of orthogonal networks, although these are not so pronounced as in Stomatopoda. Among Eumalacostraca, certain caridid shrimps, such as pistol shrimps (Alpheoidea), cleaner shrimps (Stenopodidea, Thoridae), and a single group of anomurans, the land hermit crabs, all possess mushroom body characters, including proteins that in Drosophila are required for learning and memory (Wolff et al., 2012, 2017).
Within Eumalacostraca, mushroom bodies thus appear to have undergone lavish divergence, whereby the ground pattern organization of columnar neuropils consisting of parallel fibers and serially arranged orthogonal networks has undergone transformation to a more modest columnar neuropil surmounted by a dendritic cap or calyx of increasing complexity (Fig. 11). Further transformations suggest a complete foreshortening of columnar neuropil, resulting in a center elaborated into many stratified palisades of neurons and discrete lateralized domains (Sullivan & Beltz, 2004). The land hermit crabs suggest a transitional arrangement in which orthogonal networks of the columns are subsumed into the volume of the hemiellipsoid body as shown in Figure 9 (Wolff et al., 2012). In more derived eumalacostracans, as in other crustacean lineages (Copepoda, Remipedia), there are neither parallel fibers nor discernable orthogonal networks. The absence of those features provides a calyx-like neuropil, long known by its other name: the hemiellipsoid body. In certain eumalacostracans such as Astacidae, hemiellipsoid bodies are prominent, whereas in others they are much reduced even though the olfactory lobes are not. An example is in varunid crabs, where hemiellipsoid body neuropil is difficult to distinguish from adjacent regions. In isopods, the hemiellipsoid body is greatly reduced, in some species barely distinguishable, and in certain amphipods hemiellipsoid bodies are absent (Stemme et al., 2014; Ramm & Scholtz, 2017).
These observations suggest that the mushroom body ground pattern is ubiquitous to Euarthropoda but that in crustaceans it has diverged to such a degree that it is unrecognizable as such in most species (Figs. 10, 11). This raises many questions, the first being why within one clade, Eumalacostraca, the mushroom body ground pattern has evolved such radical modifications (Fig. 11). By comparison, insect mushroom bodies appear to have undergone only modest divergence. Their enlargement in certain insect species may reflect certain behavioral traits, such as the requirement for place memory by foragers or by obligate parasitoids. The calyces may be variously divided into concentric domains, reflecting attributes such as dietary specialists or generalists, or the representation of different modalities (Ehmer & Gronenberg, 2002; Farris & Roberts, 2005; Farris, 2013). And, as already mentioned, calyces are not present in Hemiptera and Coleoptera that are secondarily aquatic or in paleopterans that start their life as aquatic larvae, as do Odonata and Ephemeroptera (Strausfeld et al., 2009). Yet the range of the mushroom body’s divergent forms in Insecta pales in contrast with that observed across Eumalacostraca. Might it be that ecologies are so much more diverse in the ocean than on land that crustacean mushroom body attributes have been subject to more varied selective pressure?
Homology or Convergence?
Molecular phylogenies of Pancrustacea make the case for insects originating from crustaceans, with the morphologically simple, blind, cave-dwelling Remipedia as the closest relative of Hexapoda (von Reumont et al., 2012; Oakley et al., 2013; Schwentner et al., 2017). Comparing the organization of central complexes (Fig. 8) and mushroom bodies across a molecular-based pancrustacean phylogeny (Fig. 10) demonstrates why a prima facie acceptance of mushroom body homology faces obvious difficulties, whereas acceptance of central body homology may not. With one exception (Stegner & Richter, 2011), the central body occurs throughout Pancrustacea, and its participation in the broader arrangement of the central complex and its satellite neuropils occurs both in hexapods and remipedes as well as in eumalacostracans and phyllocarids (Utting et al., 2000; Strausfeld, 2009; Kollman et al., 2011; Böhm et al., 2012; Stemme et al., 2012; Kenning et al., 2013). Mushroom bodies, however, as defined earlier in this chapter, were first identified in insects but in no other pancrustacean group until their very recent rediscovery in Stomatopoda (Wolff et al., 2017). The original neuroanatomical criteria for identification across Hexapoda have been expanded from a meager three to thirteen, and it is these that support the identification of corresponding centers in Stomatopoda (Wolff et al., 2017). However, Malacostraca, to which Stomatopoda belongs, is phyletically very distant from Hexapoda. Complicating the issue is that the older Phyllocarida, sister to all Eumalacostraca, shows evidence neither of mushroom bodies nor of a clearly defined hemiellipsoid body. These observations suggest two evolutionary scenarios. One is that mushroom bodies evolved convergently in insects and Eumalacostraca, such that analogous centers are present in Hexapoda, Stomatopoda, and Cephalocarida. The other is that the mushroom body is an ancient plesiomorphy of Pancrustacea that has been retained only in Hexapoda, Stomatopoda, and Cephalocarida, but lost in all other groups, including Phyllocarida. This second possibility is indicated by the green trajectory traced within the phylogenetic tree in Figure 10. While the assumption of character loss is unverifiable, character reduction that might presage loss is suggestive; and there are many examples of this as, for example, in Malacostraca whose pelagic species reveal significant reduction of centers such as visual neuropils and hemiellipsoid bodies (Strausfeld, 2012), or in related species with markedly different habitats (Ramm & Scholtz, 2017). And simplification from a more elaborate morphology is commonplace in nature when selection maintaining a structure or behavior is weakened (Faulkes, 2008: Strauß & Stritih, 2017).
If mushroom bodies in insects and stomatopods evolved independently in response to comparable constraints, then what were these constraints to have driven convergent evolution despite such different biotopes, one terrestrial the other marine? And why might a mushroom body-like morphology have been lost in most Eumalacostraca but not in Hexapoda? One recent paper suggests that elaborations of marine and terrestrial visual ecologies through geological time introduced novel physical parameters, such as chromatic and polarized light reflection, as well as unprecedented geometries and dynamics that would have driven the evolution of superior vision and, consequently, visually evoked behaviors that also require multisensory integration and memory (Wolff et al., 2017). Among crustaceans, it is the stomatopods that possess the most refined retinal organization, including a unique horizontal band of color- and polarized-light-sensitive photoreceptors that divides the upper eye hemisphere from the lower one. This organization is reflected in the underlying optic lobe circuitry, also unique to this group (Thoen et al., 2017, 2018), the eyes of which can independently scan the visual scene (see Land et al., 1990). Many other eumalacostracans possess prominent eyes supplying information to visual centers. Shore crabs, for example, respond readily to visual motion (de Astrada et al., 2001; Sztarker et al., 2005), as do crayfish and many kinds of shrimps. Yet these lack insect- or stomatopod-like mushroom bodies.
What aspects of visual behavior common to stomatopods and insects might be relevant to the possession in both of mushroom bodies? One proposed driver of mushroom body evolution is the requirement to recall exact locations and their value from which to obtain nourishment. Helicoid butterflies, for example, enlarge their mushroom body lobes during repeated visits to distributed foraging sites, the location and sequence of which are learned: a strategy known as “trap-line” foraging (Montgomery et al., 2016). It has been suggested that the large mushroom bodies of social hymenopterans first evolved in parasitoid wasps in conjunction with the requirement to learn the many locations of potential hosts (Farris & Schulmeister, 2011). The only eumalacostracan groups besides stomatopods that are known to evidence memory of exact locations that are repetitively visited are cleaner shrimps, pistol shrimps, and land hermit crabs, all of which have mushroom body-like characters, including orthogonal association networks. Cleaner shrimps have accurate memory for specific locations visited by the fish they clean (Limbaugh et al., 1961). Pistol shrimps are the only crustaceans known to have evolved eusociality (Duffy, 1996), for which memory of place must play a major role. Land hermit crabs are renowned for memory of sites at which they socially interact (Rotjan et al., 2010). These are all examples of behaviors that argue for mushroom bodies having evolved by convergence.
Nevertheless, stomatopod and insect mushroom bodies pass three crucial tests for phenotypic homology (Patterson, 1988). These are as follows: the correspondence of many parts; the exclusion of other centers that might similarly be interpreted as mushroom bodies (Wolff et al., 2017); and the coexistence of additional homologies. With respect to the last, an argument for homology is the correspondence of neuropils in the insect and eumalacostracan lateral protocerebra. As shown in Figure 12, there is little to distinguish the many centers comprising the lateral protocerebrum of a neopteran insect from the neuropils interposed between the stomatopod or caridid mushroom body-like centers and the optic lobes. Neuropils receiving outputs from the insect and eumalacostracan optic lobes have comparable glomerular-like arrangements. Also, neuropils lateral to the mushroom bodies and their calyces receive additional tributaries from the olfactory lobes. In insects, these tributaries project directly from the lobes or via the calyces to an area called the lateral horn (Galizia & Rössler, 2010). In eumalacostracans, comparable dye tracing experiments show that relays from the antennular (olfactory) lobes supply the hemiellipsoid bodies and neuropils ventral and lateral to it (Sullivan & Beltz, 2005). Coexistence of additional homologies is implied by corresponding morphologies in the midbrain (Fig. 12), with reference to the central complex neuropils. Such comparisons also reveal that certain centers in the eumalacostracan brain, such as the reniform body (also originally identified by Bellonci in 1882), may have no known equivalent in the hexapod brain (Wolff et al., 2017).
Neuroanatomical evidence thus seems to support the hypothesis that mushroom bodies evolved very early in pancrustacean or even in panarthropod evolution (Wolff & Strausfeld, 2016) and that the other similarities observed across Pancrustacea, including the malacostracan-like organization of the remipede brain (Fanenbruck et al., 2004), are plesiomorphic, implying that there was considerable complexity in the ancestral pancrustacean brain.
That identical centers of such stunning complexity may have evolved convergently has also to be considered and, ideally, genetic studies might decide one way or the other. For example, recent investigations of craniate brain centers have demonstrated examples of genotypic homologies of centers whose anatomical correspondences were not immediately obvious in distantly related species (Sugahara et al., 2016). The use of transcriptomics for testing homology versus convergence of comparable brain areas and functions has demonstrated that in songbirds and humans parallel evolution of corresponding neural centers required for vocal learning is associated with convergent molecular changes in a suite of ancient ancestral genes (Jarvis et al., 2006). Transcriptomics demonstrate instances where morphologically corresponding structures in widely separated species are genotypically convergent, a recent example being the light-producing organs in disparate cephalopod species (Pankey et al., 2014). Phenotypic similarity can be deceptive, therefore; and, as many have cautioned, the presence of homologous structures in related species does not mean that their development is directed by the identical sets of genes (Wagner, 2014).
An overarching objective of future research will have to confront such challenges and in doing so also consider other brain regions that look so much alike in different pancrustacean lineages but where similarities may be misleading. One example is optic lobe organization. Although three nested optic neuropils appear to be the ancestral condition for Mandibulata, as suggested by fossil data (Ma et al., 2012), and although the presence of four cone cells in compound eye ommatidia defines Mandibulata (also as Tetraconata; Dohle, 2001; Richter 2002), intriguing distinctions are emerging that suggest important differences between Hexapoda and Malacostraca. For example, in the latter only one photoreceptor axon from each ommatidium reaches the second synaptic neuropil, called the medulla (Kleinlogel & Marshall, 2005), whereas in insects a pair of photoreceptors in each ommatidium sends two axons (“long visual fibers”) that terminate in it. In Drosophila, these axons carry chromatic information (Morante & Desplan, 2004). The only crustacean possessing multichromatic vision is Stomatopoda, where as many as 10 separate chromatic channels originate from ommatidia that extend as a narrow band across the eye, equatorially dividing the upper and lower eye halves (Cronin & Marshall, 1989). There is, however, just one long visual fiber from each ommatidium to the medulla; yet each ommatidium also provides at least two chromatic channels to the lamina carried by short visual fibers (Thoen et al., 2016). Chromatic information relayed to the medulla may thus require more than relays to it by lamina monopolar cells and involve synaptic interactions between long visual fiber axons passing through the lamina and short visual fibers from spectrally tuned photoreceptors ending in it. Such an arrangement would be convergent with certain lepidopterous insects, in which interactions occur in the lamina between paired long visual fibers and terminals of spectrally tuned photoreceptor terminals (Hamanaka et al., 2013).
Another difference between insects and crustaceans that suggests convergence refers to the third visual neuropil (the lobula). In Malacostraca, the retinotopic arrangements of output neurons from the lobula, and the interactions of those neurons with successive levels of local interneurons within the lobula, suggest computational layers that area at least as complex as those typifying the medulla. Thus, these extremely dense arrangements in the malacostracan lobula radically differ from the sparser arrangements in the insect lobula (Thoen et al., 2018). These and other distinctions, such as the organization of the crustacean and insect antennular lobes and olfactory pathways discussed earlier in this chapter, suggest again that genealogical correspondence cannot be taken for granted despite close morphological similarity.
Convergent Evolution of Parallel Visual Pathways
There are, however, many examples of convergent evolution that seem self-evident. Here I will review just one, the parallel organization of chromatic and achromatic pathways in pancrustacean and arachnid visual systems (Fig. 13).
Expression of transcription factors encoded by genes that determine segmental identity along the rostro-caudal body axis reveals similarities and differences across taxa regarding segmental homology and the appendages arising from segments (Lewis, 1992; Akam, 1998; Pavlopoulos & Averof, 2002). As already remarked, euarthropods have evolved a spectacular variety of segmental and thus functional specializations (tagmosis) that are as diverse as are appendicular morphologies. Such variations are reflected in the size, clustering, and sometimes fusion of ventral ganglia as well as segment-specific enlargement or apoptotic reduction of their neuropils and the fate of cell lineages that support different levels of functional complexity (Truman et al., 2010; Fusco & Minelli 2013; Harris et al., 2015). In contrast, the organization of cerebral ganglia appears to be highly stable. Manipulation of gene expression, such as RNA interference, knockdown, or overexpression (Jager et al., 2006; Sharma et al., 2015) has ascertained that the euarthropod head, irrespective of whether it is chelicerate or mandibulate, comprises three segments, thereby confirming the original conclusions by the Canadian entomologist Jacob Rempel in 1975 (Rempel, 1975). Gene expression demonstrates the segmental location of the eyes as protocerebral and the appendage pair belonging to the second head segment as deutocerebral: antennules in mandibulates, chelicerae in arachnids. Developmental gene expression also indicates that certain centers of the protocerebrum, such as the arcuate body and mushroom body of arachnids, appear to be homologues of hexapod central bodies and mushroom bodies despite disparities in their neuronal organization (Doeffinger et al., 2010).
In the fully grown animal, such differences can be profound yet still support comparable integrative functions, as demonstrated by the organization of color-, form- and motion-encoding visual pathways in arachnids and insects (Fig. 13). Paleontological evidence suggests that the single-lens eyes of arachnids evolved from two pairs of ancestral compound eyes, such as those typifying megacheirans and which are optically comparable to the lateral eye pair in extant Limulus (Strausfeld et al., 2016b). In the arachnid lineage, the ancestral lateral eye pair has broken up to provide four pairs of single-lens eyes laterally whereas the ancestral medial eye pair has evolved as a pair of single lens eyes. In most araneans, those eyes are the forward-viewing principal eyes. An exception is in the nocturnal Dinopidae, where one pair of enormously enlarged lateral eyes assumes the role of the principal eyes (Blest & Land, 1977). Photoreceptors serving each eye terminate in their own separate synaptic neuropils, collectively called laminas. In jumping spiders (salticids), the pair of frontally directed principal eyes is specialized in that the refractive properties of its lenses allow light of different wavelengths to be focused at different depths in a retina composed of a tiered arrangement of photoreceptors providing three to four channels, each of which responds to a different wavelength (Blest et al., 1981; Land, 2005). The salticid frontal eyes thus serve color vision, whereas the lateral eyes equipped with achromatic photoreceptors mediate motion detection, including motion of small targets that trigger prey capture (Duelli, 1978; Zurek et al., 2010). Neuroanatomy demonstrates that relays from the color-sensitive frontal eyes of salticids project to successive retinotopic neuropils and that subsequent relays target the arcuate body. This chromatic pathway is separate from the visual centers serving the lateral eyes. The third visual center serving the lateral eyes is a pair of highly modified mushroom bodies, the parallel axons of which originate from dense clusters of globuli cells and interdigitate across the brain’s midline. This functional segregation of principal and lateral channels does not pertain to chromatic versus achromatic vision but pertains to object versus motion detection; the same anatomical organization is seen in hunting spiders where the greatly enlarged frontal eyes, which are achromatic, send relays that reach the arcuate body, whereas the lateral eyes supply the modified mushroom body (Strausfeld et al., 1993; Strausfeld & Barth, 1993).
Insects detect color as well as structured features of their visual ecology and use information about panoramic visual motion for flight control. But rather than having different eyes for different tasks, as do spiders, color-sensitive and achromatic photoreceptors occur together in each optic unit of the compound eye, the ommatidium, and are thus distributed across the whole eye (Rister & Desplan, 2011). Relays from ommatidia terminate at two levels of the optic lobes: achromatic relays in the first synaptic neuropil, called the lamina, and color-sensitive relays in the second neuropil, called the medulla. Channels associated with these relays next segregate out to provide information about color and form to a cortex-like neuropil, called the lobula. Information about visual motion across the retina is channeled to a separate tectum-like neuropil, called the lobula plate, or an equivalent region of the lobula in certain orders of insects, such as Hymenoptera (DeVoe et al., 1982). The outputs from these deep neuropils further segregate such that information used to generate optokinetic movements and provide visual balance is relayed from the lobula plate or its equivalent to relevant motor pathways (Strausfeld & Lee, 1991). Channels from the lobula and associated glomerulus-like centers carry reconstructed details of the visual scene to areas of the midbrain and, eventually, to their relevant motor pathways after integration with other sensory information (Strausfeld et al., 2007). The parallel processing of form, color, and visual motion has evolved in arachnids, insects, and also in chordates where it is best documented (Sanes & Zipursky, 2010).
Whether in Crustacea there is comparable parallel processing, such as channels reconstructing aspects of the visual scene and channels devoted to signaling wide-field motion, is not yet known. With the exception of Isopoda (Sinakevitch et al., 2003), crustaceans possess no prominent lobula plate to suggest the segregation of wide-field motion-sensitive channels from other types of channels. In other malacostracan crustaceans, a diminutive neuropil that does not even subtend the whole visual field is all that implies a possible lobula plate equivalent; but this neuropil lacks small field inputs that are characteristic of the dipteran and hymenopteran motion-detecting systems (Buschbeck & Strausfeld, 1996). As far as has been ascertained, most crustaceans make do with dichromatic vision (Marshall et al., 2015), which raises the question whether if there are parallel channels do they segregate to distinct parts of the lobula. As mentioned earlier, only one crustacean group is known to possess multichannel color vision. This is Stomatopoda, where equatorial systems of photoreceptors detect up to 10 different spectral maxima, as well as linear and circular polarized light (Cronin & Marshall, 1989; Thoen et al., 2014; Gagnon et al., 2015). These channels are separately represented in a special zone of the lamina and medulla, and relays from it to the lobula extend laterally across all the achromatic relays representing the upper and lower eye halves (Thoen et al., 2017, 2018). What this means in terms of integrating color information with achromatic information is not yet known, but it is certain that color plays an important role in stomatopod behavior (Marshall et al., 1996; Marshall & Oberwinkler, 1999).
Tardigrades and the Enigma of the Protocerebrum
The one group of Arthropoda that until this point has not been discussed is Tardigrada. Phyletically enigmatic, minute, and resistant to extremes of temperature and pressure, these lobopodian animals appear to be divided into just four segments.
As proposed by the palaeontologist Graham Budd (Budd, 2001), when there is a paucity of developmental or molecular data, as is the case for Tardigrada, an expeditious determinant of a segment is an organ system that is repeated metamerically along the rostro-caudal axis. Tardigrade segmentation is defined developmentally by serial indentation of the ectoderm and the appearance of four pairs of mesodermal somites at positions that later give rise to paired lobed appendages. The expression of the gene engrailed posterior to each somite further resolves segments despite the absence of coelomic cavities (Smith & Goldstein, 2017). Four ventral ganglia associated with four pairs of legs and the repeat organization of trunk and leg musculature are sufficient in demonstrating that tardigrades possess a ladder-like segmental nervous system connected by paired nerve cords to a rostral brain (Smith & Goldstein, 2017). Up until that level, the ventral nervous system conforms to the organization typical of an euarthropod, but the brain is problematic. Originally assumed to lie either above the gut or around it, there has been no agreement whether the brain comprises discrete lobes, whether it is truly dorsal, whether it has identifiable centers, or whether it consists of three fused neuromeres or just one (Dewel & Dewel, 1996; Zantke et al., 2008; Persson et al., 2012; Mayer et al., 2013; Smith et al., 2017). Arguing against such a tripartite brain is the absence of appendages associated with the “head,” although it could be countered that in tardigrades appendages may have undergone evolved loss as, most likely, have all segments caudal to segment 4 (Smith & Goldstein, 2017).
The true organization of the tardigrade brain has recently been resolved by high-resolution confocal microscopy to resolve labeling by specific antisera of neuronal processes, distinguishing these from neuron cell bodies. Observations of four species of tardigrades, representative of this group of animals, demonstrate that their brains are neither tripartite nor supraesophageal. Rather, the brain’s neuropil encircles the pharynx (Smith & Goldstein, 2017).
Possibly this arrangement is an apomorphy, another evolved modification, reflecting miniaturization and the simple habits of these animals. However, the superphylum Ecdysozoa, to which Arthropoda belongs (Giribet & Edgecombe, 2017), embraces a second clade of organisms that molt and are characterized by apical brains that encircle the gut, as does the tardigrade brain. This clade is the asegmental Cycloneuralia, which includes nematodes and priapulids, from which Panarthropoda originated (Rota-Stabelli et al., 2013). A 535-million-year-old priapulid-like fossil from the early Cambrian strata suggests these ecdysozoans were already present at the advent of the Cambrian; and the first fossil that showed any evidence of a preserved ventral nerve cord is a middle Cambrian priapulid (Conway Morris, 1977; Liu et al., 2014). Extant priapulids possess a circumpharyngeal brain, from which extend many parallel nerve tracts as well as a nerve cord composed of twin nerve bundles that extend along the ventral midline of the body (Schmidt-Rhaesa & Henne, 2016). Few neuroanatomical studies have been performed on the adult priapulid brain or, for that matter, on other cycloneuralian brains, with the obvious exception of Coenorhabditis elegans (White et al., 1986). Nevertheless, cycloneuralian brains are not trivial, the largest comprising substantial numbers of neurons that provide discrete but contiguous heterolateral neuropils (Schmidt-Rhaesa & Henne, 2016).
Returning to tardigrades, the prevailing view is that their brains are cycloneuralian-like and that because the brain is distinct from the ventral ganglia and is apical it should correspond to the euarthropod protocerebrum (Mayer et al., 2013; Smith & Goldstein, 2017; Martin et al., 2017). However, there are problems with such an interpretation because unlike the four ventral ganglia, each of which is associated with a definable segment (Smith et al., 2017), the volume containing the brain has no obvious segmental affinity, nor is it demarcated by the expression of the segment polarity gene engrailed (Gabriel & Goldstein, 2007). This absence and the brain’s cycloneuralian character imply that the tardigrade brain might occupy a special status when considering the evolution of the arthropod head, particularly if the tardigrade brain is used as a proxy for interpreting the segmental affinity of fossilized brains (Park et al., 2018).
If the tardigrade’s circumesophageal brain is a discrete apical neuropil with no ganglionic affinity then the first three segmental ganglia, albeit part of the tardigrade’s ventral nervous system, would correspond to the euarthropod proto-, deuto-, and tritocerebra. It has already been suggested by various authors that the euarthropod protocerebrum may ancestrally derive from two quite distinct parts (Schmidt-Ott et al., 1994; Urbach & Technau, 2003, 2004; Strausfeld, 2012), a proposition already made in 1899 by Charles Turner who was the first African American neuroanatomist (Turner, 1899). Turner identified mushroom bodies in the apical nonsegmental brain of annelids and within the anterior part of the segmented insect brain, thereby concluding that insects possess a specialized frontal neuropil in common with annelids. At that time, this was a perfectly reasonable suggestion that accorded with the Articulata theory: that annelids and arthropods, both segmented, originated from a common segmented ancestor. An extension of this was that the first segment of the arthropod brain possessed two domains: the prosocerebrum, equivalent to the asegmental annelid brain, and the segmental archicerebrum.
Despite there being no molecular phylogenies supporting Articulata, might there be evidence that an ancestral apical brain originating in deep time persists and is present in Euarthropoda? A meticulous study of neuroblast lineages by Urbach and Techau (2004) suggest there is such evidence. They identified two domains of the embryonic insect protocerebrum, which they termed the prosocerebrum and archicerebrum. These give rise to two distinct neuronal lineages. Neuroblasts from the anterior domain give rise to the mushroom bodies, central body and medial neurosecretory neurons whereas neuroblasts in the second domain give rise to neurons serving the visual system and circuits typifying ganglia (Urbach & Technau, 2004). It has also been demonstrated that the most rostral domain in the insect protocerebrum is associated with the expression of the gene Six3, which also denotes the nonsegmental apical brain of polychaete annelids (Steinmetz et al., 2010).
In pancrustaceans, neuronal arrangements of the adult protocerebrum indeed suggest two distinct parts. The first is defined by the central complex, mushroom bodies, neurosecretory pathways from the pars intercerebralis and neuropils associated with the labrum (Strausfeld, 2012). The second part is associated with the visual system and its central neuropils. The segmental nature of the second part is suggested by those crustaceans that possess appendicular eyestalks, an arrangement already a feature of the stem arthropod Fuxianhuia protensa (Ma et al., 2012; Strausfeld et al., 2016). Protocerebral appendages are also inducible: in Drosophila, eye development can be genetically switched to that of a leg-like appendage (Kumar & Moses, 2001). Neural pathways carrying information from the compound eyes segregate to glomerular-like domains in the protocerebrum that provide outputs to intersegmental relay neurons (Gronenberg & Strausfeld, 1991; Strausfeld, 2012). This ground pattern of sensory inputs to defined ganglionic territories connected by intersegmental relays is a motif repeated at every segmental ganglion irrespective of evolved modifications that reflect the sensory-motor specializations of its parent segment (Burrows, 1997; Jacobs & Theunissen, 1996).
As mentioned above, the two neuropils found nowhere else except rostrally in the protocerebrum – the mushroom bodies and the central body – have anatomically corresponding counterparts in the nonsegmental apical brains of errant marine annelids, such as Nereis bicolor and the scale worm Harmothöe areolata, as well as in asegmental polyclad flatworms (Heuer et al., 2010; Wolff & Strausfeld, 2015a), both members of that other superphylum of invertebrate animals, Lophotrochozoa.
Half a century of progress in developmental biology and molecular phylogenetics has extinguished any lingering thoughts that segmentation is a unifying trait relating Arthropoda and Annelida. These crown phyla did not exist in the late Proterozoic when asegmental bilaterians left tracks that can today be interpreted as recording behaviors that required action selection and allocentric memory (Seilacher et al., 2005), both demonstrable today in simple bilaterians such as triclad flatworms Dugesia japonica (Inoue et al., 2015; Shomrat and Levin, 2013). If neuronal circuits mediating such behaviors have persisted through geological time, then ground pattern organization – the principal circuitries – of the central complex and mushroom bodies may be present in the apical brains of all motile bilaterians irrespective of the organization of their nerve cords (see Martín-Durán et al., 2017). In this context, it is encouraging that recent transcriptomics has demonstrated highly conserved genes and signaling underlying the common patterning of the bilaterian head (Luo et al., 2017).
The hypothesis is explicit: that in crown Euarthropoda the protocerebrum is a hybrid arrangement comprising an ancient apical brain subsumed into the most rostral neuromere, the first segment of a “tripartite” brain that obtains its present morphology from the forward migration to positions above and around the gut of what were ancestrally three ventral ganglia. This evolutionary innovation is played out during early pancrustacean embryogenesis; as demonstrated in Drosophila and the locust Schistocerca, the presumptive deuto- and tritocerebra, each initially flanking the side of the esophagus, grow forward to achieve contiguity with the supraesophageal protocerebrum. The final adult ensemble is a brain penetrated by the gut at the level of the deutocerebrum (Boyan et al., 2003; Hirth et al., 2003).
Is the circumesophageal brain of Tardigrada key to resolving the segmental organization of the euarthropod head, as suggested by the hypothetical evolutionary events sketched in the final illustration of this chapter (Fig. 14)? It should be possible to show exactly how far rostrally Otd is expressed in the tardigrade and whether that expression domain includes the brain, or whether it is the expression of Six3 expression that is apical. Might the central complex and mushroom body ground patterns be demonstrable in the brain of a tardigrade or a species of cycloneuralian? With such questions still unanswered at the time of writing, the origin and subsequent pedigree of the central complex and mushroom body – centers that command so much attention today – are almost as hidden to us now as they were when Dujardin made his discovery over 160 years ago.
Studies of fossil brains would not have been possible without the support of Xianguang Hou, Director of Yunnan Key Laboratory of Paleobiology, Kunming, China. I am indebted to Xiaoya Ma and Greg Edgecombe at London’s Museum of Natural History with whom collaboration on studies of Chengjiang fossil brains have been pivotal to issues discussed in this chapter. The chapter has also benefitted from Greg’s expertise, advice, and encyclopedic knowledge, particularly with respect to the timing of lineage divergences shown in Figures 7 and 9. Several years of collaboration with Gabriella Wolff, University of Washington, Seattle, have resulted in a breadth of knowledge about the occurrence of higher brain centers across invertebrate phyla. Frank Hirth, University of London King’s College, has contributed to ideas expressed here about possible correspondences of arthropod and vertebrate brains. I am grateful to Justin Marshall and Hanne Thoen, at the Queensland Brain Institute, for their support and collaboration on stomatopod brains and to Marcel H. Sayer, University of Arizona, for contributing vital confocal data on eumalacostracan brains. This chapter would not be what it is without the support and advice of Camilla Strausfeld, who also read, edited, and advised on its various versions. I am responsible for errors and omissions.
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