As demonstrated in Drosophila melanogaster, paired mushroom bodies in the insect brain play manifold roles in learning and memory (Aso et al., 2014a; Aso et al., 2014b; Cognigni et al., 2018). One diagnostic tool for identifying putative mushroom body homologues in other mandibulates is an antibody raised against the catalytic subunit of protein kinase A, encoded by the Drosophila gene DC0 (Kalderon and Rubin, 1988), and required for effective learning and memory (Skoulakis et al., 1993). The antibody, known as ‘anti-DC0’, selectively identifies the columnar neuropils of mushroom bodies of insects (Farris and Strausfeld, 2003) and of other arthropods with, until very recently, the notable exception of crustaceans (Wolff and Strausfeld, 2015). Indeed, numerous studies have disputed or expressed ambivalence about centers in comparable locations in the crustacean brain being mushroom body homologues (e.g., Strausfeld et al., 1998; Fanenbruck et al., 2004; Fanenbruck and Harzsch, 2005; Farris, 2013; Sandeman et al., 2014; Krieger et al., 2015; Krieger et al., 2019; Harzsch and Krieger, 2018; Machon et al., 2019; Wittfoth et al., 2019).

The discovery of mushroom bodies in mantis shrimps by Wolff et al. (2017) caused us to revise our view of mushroom bodies in crustaceans and to look for these centers in other lineages of this taxon. Here, we provide evidence that mushroom bodies generally occur in Crustacea, thereby further supporting Hexapoda + Crustacea as the established subphylum Pancrustacea (Zrzavý and Štys, 1997; Regier and Shultz, 2001).

Historically, identification of the insect mushroom body relied on just four neuroanatomical traits: an overall fungiform shape; a location exclusively in the brain’s rostrolateral protocerebrum; an internal composition comprising hundreds to tens of thousands of intrinsic neurons originating from minute cell bodies clustered at the brain’s rostral surface; and the possession of columnar lobes formed by the extended axon-like processes of intrinsic neurons. An often-included fifth character typical of almost all insects is a cap of neuropil called the calyx comprising the dendrites of intrinsic neurons, which receive inputs from the antennal lobes and other sensory neuropils. Even flightless Zygentoma (silverfish and firebrats) possess calyces (Farris, 2005a), as do Diplura and Collembola, two sister groups of Insecta (Böhm et al., 2012; Kollmann et al., 2011). However, Ephemeroptera (mayflies) and Odonata (dragonflies, darters) are calyxless; inputs to their mushroom bodies supply their columnar lobes directly (Strausfeld et al., 2009). Such distinctions demonstrate a general property of all well-defined protocerebral brain centers: retention of ancestral ground patterns despite evolved modifications such as losses of some components and elaborations of others. For the insect mushroom body these modifications include: variations of columnar lobe organization; expanded representations of sensory modalities; and loss, or hypertrophy, of the calyces (Strausfeld et al., 2009).

Despite such variations, the insect mushroom body has additional features that are always present. Foremost is that the columnar lobes are serially partitioned down their length such that inputs to the lobes are constrained to discrete synaptic domains (Li and Strausfeld, 1997; Ito et al., 1998; Strausfeld, 2002). These domains receive functionally defined inputs and supply functionally defined mushroom body output neurons (MBONs; Aso et al., 2014a) that extend to circumscribed regions of the medial and rostral protocerebrum. There, they contribute to further higher processing and have arrangements comparable to those relating the mammalian hippocampus to cortical areas (Bienkowski et al., 2018). Certain outputs from the columns also project recurrently to more distal levels of the mushroom body itself (Gronenberg, 1987; Zwaka et al., 2018). These arrangements are defined by neurons usually expressing GABA (Liu and Davis, 2009). The same organization typifies the columnar lobes of the stomatopod mushroom bodies where input and output neurons are arranged along the length of the lobes (Wolff et al., 2017).

Also apparent across insect species is that subsets of intrinsic neurons parse the mushroom body lobes into longitudinal subunits that are differentiated from each other with regard to their clonal lineages (Yang et al., 1995; Crittenden et al., 1998; Tanaka et al., 2008), as well as by their aminergic and peptidergic identities (Sjöholm et al., 2006; Strausfeld et al., 2000; Strausfeld et al., 2003). Comparable longitudinal divisions of the stomatopod mushroom body are represented by four columnar lobes that extend together approximately in parallel (Wolff et al., 2017). In Drosophila and other insects these characteristic attributes have been shown to be critical in supporting functions relating to the modality, valence, stored memories and behavioral relevance of information computed by the mushroom body (Li and Strausfeld, 1999; Aso et al., 2014a; Aso et al., 2014b; Owald et al., 2015; Takemura et al., 2017; Hattori et al., 2017; Cognigni et al., 2018).

In total, thirteen characters have been identified that define both the insect (Drosophila) and mantis shrimp (Stomatopod) mushroom bodies (see Wolff et al., 2017). We show here that crown eumalacostracan species belonging to lineages originating early in evolutionary history share the same expanded set of diagnostic characters that define insect mushroom bodies, including the partitioning of columns into discrete circuit-defined domains. These can occur not only as segment-like partitions of the columnar lobes but also as tuberous outswellings, as they do in basal insects belonging to Zygentoma and Pterygota (Farris, 2005a; Farris, 2005b; Strausfeld et al., 2009).

Because stomatopods are unique amongst crustaceans in possessing elaborated optic lobes that serve a multispectral color and polarization photoreceptor system (Thoen et al., 2017; Thoen et al., 2018), it could be argued that mushroom bodies in the mantis shrimp are unique apomorphies that have evolved specifically to serve those modalities. However, Stomatopoda are an outgroup of Eucarida (Euphausiacea + Decapoda) and the status of mushroom bodies as the ancestral ground pattern is supported by corresponding centers in the lateral protocerebrum of later evolving eumalacostracan lineages. For example, Lebbeus groenlandicus, a member of the caridid family Thoridae, has been shown to possess paired mushroom bodies each comprising a layered calyx supplying intrinsic neuron processes to columnar lobes (Sayre and Strausfeld, 2019). Here we describe neuroanatomical characters defining mushroom bodies also in cleaner shrimps (Stenopodidae) and several groups of carideans.

The recognition that mushroom bodies occur in crustaceans is not new. In his 1882 description of stomatopod brains, the Italian neuroanatomist Giuseppe Bellonci identified domed neuropils (corpo emielissoidale), from which extend columnar neuropils (corpo allungato). Bellonci explicitly homologized these with, respectively, the insect mushroom body calyx and its columnar lobes (Bellonci, 1882). Hanström adopted this terminology for his studies of Reptantia (Hanström, 1925; Hanström, 1931), a relatively recent malacostracan lineage that includes crayfish and lobsters. Hanström used the terms ‘hemiellipsoid body’ or corpora pedunculata to denote centers lacking columnar lobes he considered to be homologues of the mushroom body (Hanström, 1932). However, over the last four decades numerous studies on Reptantia have insisted that hemiellipsoid bodies are apomorphic – genealogically distinct from mushroom bodies – and that they represent the ancestral ground pattern of crustacean learning and memory centers (Kenning et al., 2013; Sandeman et al., 2014; Machon et al., 2019; Krieger et al., 2019). Apart from a fundamental misunderstanding of the original meaning of the term ‘hemiellipsoid body,’ that viewpoint is incorrect and is in conflict with the demonstration here, and in two recent studies, that mushroom bodies hallmark eumalacostracan lineages that diverged earlier than Reptantia (Wolff et al., 2017; Sayre and Strausfeld, 2019). Studies of Reptantia also show that at least one anomuran group has mushroom bodies equipped with columnar lobes (Strausfeld and Sayre, 2020). Comparisons across Eumalacostraca described here indicate that mushroom bodies are indeed ubiquitous across Crustacea. However, in contrast to mushroom bodies in insects, evolved modifications of the mushroom body ground pattern in crustaceans have resulted in highly divergent morphologies including, both within Caridea and in certain lineages of Reptantia, centers lacking defined lobes.

In the following, descriptions of mushroom bodies and their evolved derivatives are organized by lineage from the oldest to most recent as shown in Figure 1A. The exception is Leptostraca, the sister group of Eumalacostraca, which is considered in the Discussion. Each of the following descriptions is preceded by a brief Background of the species considered followed by Observations. To provide context we first provide an overview of mushroom body organization as exemplified by the stomatopod brain (Figure 2).

Figure 1

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Reduced protocerebral centers in Dendrobranchiata (Figure 3A)

Background

Dendrobranchiata is the second oldest eumalacostracan lineage, today represented by peripatetic/pelagic penaeid shrimps. Using antibodies raised against α-tubulin, FMRFamide, and allatostatin on Penaeus vannamei, Meth et al. (2017) were unable to delineate a target neuropil supplied by the olfactory globular tract (OGT). Sullivan and Beltz (2004), using dye tracing into the OGT of Penaeus duorarum, identified a small twinned neuropil situated extremely rostral in the lateral protocerebrum. The neuropil receives collaterals from the OGT, the axons of which terminate mainly in lateral protocerebral neuropil beneath.

Observations

Immunostaining the lateral protocerebra of Penaeus vannamei with anti-DC0 (Figure 3A) resolves a small intensely immunoreactive four-component center, at the location identified by Sullivan and Beltz (2004). A similarly reduced center typifies some isopods (Figure 3B). There is a notable absence of a columnar lobe in the Penaeus center and in the corresponding neuropil of isopods.

Figure 3

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Elaborated mushroom bodies in Stenopodidea (Figures 4 and 5)

Background

Mitochondrial genomics resolves the infraorder Stenopodidea as the sister taxon of Caridea (Shen et al., 2013). Its molecular clock age is Jurassic with a Cretaceous fossil calibration (Wolfe et al., 2019). The following description is restricted to the coral banded cleaner shrimp Stenopus hispidus, one of the few well-documented cleaner shrimps that inhabit tropical coral reefs and groom fish of external parasites or detritus (Vaughan et al., 2017). These shrimps are well known for their knowledge of place, occupying a specific territory – their cleaning station – to which they return daily and which is visited by favored fish (Limbaugh et al., 1961). Long-term memory in S. hispidus is suggested by observation of individuals pair bonding and recognizing a partner even after an absence of several days (Johnson, 1977). Allocentric recognition of place and partner recognition are mediated by chemoreception (Esaka et al., 2016).

Observations

We confirm here the original description by Sullivan and Beltz (2004) of the S. hispidus lateral protocerebral center that they referred to as a hemiellipsoid body divided into three contiguous domains that receive layered OGT terminals. A neuropil named by Sullivan and Beltz as the ‘lateral protocerebral complex’ and described as an entirely separate neuropil, as it is by Krieger et al. (2019), is clearly a columnar lobe originating from these domains and terminating as a set of tubercular swellings, (Figure 4A–C). The swellings are strongly immunoreactive to anti-DC0 (Figure 4D–F). Reduced silver staining (Figure 4C) and immunohistology (Figure 4E) demonstrate that the three domains (Ca1-Ca3) assume the configuration of a layered mushroom body calyx. Intrinsic neurons in each domain (Figure 5A,B,D) contribute many hundreds of axon-like fibers that converge into a common root, from which arises the compound columnar lobe terminating as three adjacent tubercular domains, corresponding to the three calyces (Figures 4D–F and 5A,B). Parallel fibers branch in these tubercles where they provide pre- and postsynaptic specializations (Figure 4A,B). As remarked above, anti-DC0 is expressed at high levels in the tubercles and at lower levels just distally in the columnar lobe (Figure 4D–F). And, as shown by immunolabelling with antibodies against GAD, 5HT and TH, the tubercles are further divided into smaller territories such that the entire structure assumes the serial domain arrangement characterizing the mushroom body ground pattern (Figure 4G–J).

Figure 4

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The calyces correspond to Sullivan and Beltz’s ‘hemiellipsoid body.’ They are composed of many thousands of intrinsic neuron dendrites. Their axon-like extensions, resolved by Golgi impregnations (Figure 5A), converge predominantly beneath Ca2 in the columnar root but also recruit from both Ca1 and Ca3 through an elaborate system of interweaving processes (upper and lower insets, Figure 5A). Groups of parallel fibers segregate before invading different tubercles, each denoting a discrete integrative domain.

Figure 5

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As in Lebbeus and Stomatopoda, the calyces are profusely invaded by branches of TH-containing neurons (Figure 5B). These are arranged through three successive calycal layers (Figure 5C–E), each of which is defined by its elaborate cytoarchitecture reflecting specific neuronal components, as described from Stomatopoda and the alpheoid shrimp Lebbeus (Wolff et al., 2017; Sayre and Strausfeld, 2019). Layer 1 of each of the three calyces (Ca1-Ca3) contains ascending processes of slender varicose afferents and the apical dendrites of intrinsic neurons (Figure 5F,G). Climbing fibers enter the calyces from other lateral protocerebral centers. Layer 2 (Figure 5D,E) is denoted by the numerous parallel projecting terminals originating from the olfactory globular tract. Layer 3 (Figure 5D) contains the massively arborizing inner dendrites of intrinsic neurons, some of which are shown at the corresponding level in Figure 5A, upper right. Processes of intrinsic neurons sweep laterally beneath layer 3 to enter the root of the mushroom body’s columnar lobe (Clm R; Figure 5A,D).

Caridean mushroom bodies (and reniform body) (Figures 6–11)

Background

Caridea splits from its sister group Procaridea in the Carboniferous (Bracken et al., 2010), with most caridean crown group diversification occurring in the Jurassic (Wolfe et al., 2019). Caridea comprises the second largest decapod taxon, with two-thirds of its species occupying marine habitats. Here, we consider marine species belonging to the families Alpheidae and Thoridae (members of the superfamily Alpheoidea), and intertidal species of the family Crangonidae. These families originated approximately 220, 160 and 70 mya, respectively (Davis et al., 2018). Alpheidae is a diverse family that contains snapping shrimps, commonly referred to as pistol shrimps, which include the only known crustaceans to have evolved eusociality (Duffy et al., 2000), and visored shrimps closely related to the genus Alpheus (Anker et al., 2006). Pistol shrimps are represented here by the non-social species Alpheus bellulus, which, like other snapping shrimps, possesses asymmetric claws (chelae). The visored shrimp is Betaeus harrimani. Like pistol shrimps, B. harrimani is an active predator, although not employing concussion, and is also facultatively commensal, sharing burrows of the ghost shrimp Neotrypaea californiensis (Anker and Baeza, 2012). Unlike the genus Alpheus, Betaeus has symmetric claws, reflecting the more basal position of this genus within Alpheidae (Anker et al., 2006).

Observations

Comparisons of the brains of A. bellulus and B. harrimani revealed almost no discernible differences other than that the eyes and visual neuropils of B. harrimani are smaller than those of A. bellulus. Figures 6 and 7 therefore illustrate relevant features of the mushroom body using both species. Immunolabelling with anti-DC0 reveals an elaborate system of neuropils expressing high levels of the antigen, demonstrating the relationship of those areas predominantly to the globuli cell cluster medially and to the protocerebrum rostrally (Figure 6A,B). Notably, alpheid species lack eyestalks and possess very small compound eyes. The nested optic centers (lamina, medulla and lobula) are correspondingly reduced, and the enormous mushroom bodies occupy much of the rostral and lateral protocerebrum’s volume (Figure 6A,B). The calyx is elaborate, showing through its depth high affinity to DC0 (Figure 6C). As in Stomatopoda and Stenopodidea, the calyx has three layers, each of which is defined by the dendritic disposition of its intrinsic cells (Figure 6D–F). Intrinsic cells extend their axon-like processes in parallel bundles for a short distance before forming elaborate networks in the columnar lobes (Figure 6D,E), which extend dorso-ventrally as convoluted volumes comprising tubercular domains (Figure 6G). These volumes are heavily invested by anti-TH-, anti-5HT- and anti-GAD-positive arborizations (Figure 6H,I).

Figure 6

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Figure 7

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As in Stomatopoda and varunid Brachyura (shore crabs), the alpheid protocerebrum has a prominent DC0-positive reniform body, the components of which correspond to those described for Neogonodactylus oerstedii and Hemigrapsus nudus (Thoen et al., 2019). This center consists of four discrete neuropils linked by a branching axonal tract (pedestal) that extends axons from a glomerular initial zone to three separate zones (lateral, distal and proximal) each with its own characteristic immunomorphology (Figure 7A–E). Abutting the mushroom body ventrally, these territories are similar to, but spatially distinct from, a columnar extension from the mushroom body calyx that, like the main columnar ensemble shown in Figure 6B,G, consists of discrete tubercles, each denoted by its affinity to antisera against GAD, DC0, TH and 5HT (Figure 7F–I).

We next consider Thoridae, a separate lineage of the superfamily Alpheoidea that includes the genera Lebbeus and Spirontocaris.

Backgound

Lebbeus groenlandicus and Spirontocaris lamellicornis are exotically patterned shrimps and protected from predation by sharp spiny protuberances from their exoskeleton. They are solitary, highly active, and territorial, living on reefs or rocks. The two species look similar; both are patterned into irregular white and orange-pink bands, a feature suggesting self-advertisement or aposomatic warning. There is one report of a lebbeid cleaning the mouths of fish, reminiscent of behavior by the banded coral shrimp described above (Jensen, 2006).

Observations

Figures 8, 9 and 10A expand a recent study of Lebbeus (Sayre and Strausfeld, 2019), resolving two completely distinct calyces that share a common organization into three concentric layers. These correspond to the dense arrangements of intrinsic neurons (inset to Figure 8A). Defined by their immunoreactivity to DC0 and affinity to a palette of antibodies (Figure 8A,B,D), the layers in the larger calyx (Ca1, Figure 8A) demonstrate elaborate synaptic strata enriched with synaptic proteins (Figure 8C). Dense arrangements of processes belonging to anti-5HT-positive afferent neurons (Figure 8C) correspond to intrinsic neuron layers (Figure 8B) and arrangements of anti-TH-positive terminals (Figure 8D). Thin processes of intrinsic neurons belonging to the two calyces extend centrally as two separate columnar lobes Clm1 and Clm2.

Figure 8

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The column provided by Ca1 (Clm1) demonstrates an orthogonal network – characteristic of insect and stomatopod mushroom bodies – of intrinsic cell processes intersected by afferent and efferent neurons and by modulatory elements (Figure 9B–E,H,I). The columns contain dense arrangements of synaptic specializations (Figure 9F,G) and although these do not clearly distinguish successive synaptic domains, the arrangement of anti-TH-positive processes reveals this organization, one of the diagnostic characteristics of the mushroom body ground pattern (Figure 9I). The smaller of the two calyces provides intrinsic fibers to its columnar extension (Clm2), which terminates as a system of tubercles corresponding to the organization of the mushroom bodies in basal insects (Zygentoma, Ephemeroptera). These also show dense arrangements of synaptic sites (Figure 9J, inset).

Figure 9

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Background

The family Crangonidae is here represented by the sand shrimp Crangon franciscorum and the horned shrimp Paracrangon echinata, belonging to the superfamily Crangonoidea, which originated at the end of the Cretaceous (Davis et al., 2018). Both species provide interesting comparisons with the alpheids with respect to their habitat and mode of life. Paracrangon looks superficially like an almost colorless version of Lebbeus. However, unlike Lebbeus, which is highly active and hunts on rocky substrates and reefs, P. echinata is an almost immobile nocturnal ambush predator confined to crevasses. Its relative inactivity may be attributable to having only four walking legs compared to Lebbeus‘s six (Jensen, 2011).

Observations

The lateral protocerebrum of Lebbeus (Figure 10A) or Spirontocaris lamellicornis (Figure 10B) is radically different from that of Paracrangon echinata (Figure 10C), which possesses a single but substantial calyx that has an intense affinity to anti-DC0. Its cytoarchitecture appears to be generally homogeneous apart from a subtle indication of a peripheral layer immediately beneath its rostral covering of globuli cells (Figure 10C). The calyx gives rise to a diminutive system of anti-DC0-positive parallel fibers that provide a narrow column terminating in a small tubercular cluster (Figure 10D).

Figure 10

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The last caridean considered here is Crangon franciscorum, which inhabits subtidal sandy habitats where it actively preys on smaller shrimp species, amphipods and other microfauna (Siegfried, 1982). The calyx of C. franciscorum shows low affinity to anti-DC0 but gives rise to a prominent system of anti-DC0-positive columns that terminate in swollen tubercles (Figure 11A). The entire system of the calyx, lobes and adjacent neuropils, including the visual system’s lobula, is densely packed with anti-GAD-positive processes (Figure 11B). The calyx possesses stratified arborizations, resolved by anti-5HT and anti-TH immunostaining, some of which suggest subdivisions laterally across the calyx (Figure 11C,D). In this species, several of the lateral protocerebral neuropils caudal to (beneath) the calyx appear to comprise many neuropil islets, each with as strong an affinity to anti-DC0 as has the calyx. The disposition of these islets suggests a system possibly corresponding to the reniform body (Figure 11A).

Figure 11

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Transformed mushroom body in recent astacids

Background

Fossil and geologically calibrated molecular phylogenies place the origin of the infraorder Astacidea, the lineage providing what are generally known as ‘lobsters’ and ‘crayfish’ at 250–400 mya (Wolfe et al., 2019). Here we identify derivations of the ancestral mushroom body in the lateral protocerebra of the North American freshwater species Orconectes immunis (calico crayfish) and Procambarus clarkii (Louisiana crawfish).

Observations

The description by Sullivan and Beltz (2001) of the hemiellipsoid body of Procambarus clarkii identified its overall organization as two layered volumes, which we have named the cupola and torus (Strausfeld and Sayre, 2020). Neither volume appears outwardly distinct, the matrix of each comprising many microglomeruli (Figure 12A). However, closer inspection shows that these are larger and more densely packed in the torus than the cupola (Figure 12A, inset). Golgi impregnations, described in Strausfeld and Sayre (2020), resolve further differences between these two neuropils: each possesses a constrained organization of intrinsic neurons, which have their dendrites and short axon-like processes limited to either the cupola or torus. Both neuropils contain elaborate systems of local interneurons and glomerular ensembles, suggestive of local circuits, orthogonal arrangements appearing more pronounced in the torus (see also Figure 12—figure supplement 1). Anti-DC0 immunoreactivity shows both cupola and torus to be usually, but not invariably, highly immunoreactive (compare Figure 12C with Figure 12D,E), as are discrete regions beneath them, here referred to as the subcalycal neuropil area VII Figure 12C (nomenclature from Blaustein et al., 1988) and, laterally, the reniform body (RB, Figure 12C). Depending on the angle of sectioning, the outer level is dome-like – hence the nomenclature cupola – whereas the inner level appears to have a toroidal architecture. These volumes are matched by the distribution of anti-GAD immunoreactivity (Figure 12E). Organization of the cupola and torus as two independent units is also matched by the distribution of profuse anti-TH-immunoreactive efferent neurons and more sparsely distributed anti-5HT-immunoreactive processes (Figure 12F–H). Recordings from these neurons show them to be multimodal output neurons, comparable to MBONs of mushroom body columns (Mellon, 2000; Mellon and Alones, 1997; McKinzie et al., 2003).

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The chimeric mushroom body of Paguroidea and its evolved derivative

Background

Originating in the Devonian, Reptantia gave rise to two branches, one providing the infraorders Achelata, Polychelida and Astacidea, the other providing the infraorders Axiidea and Gebiidea, and infraorders Anomura and Brachyura (together Meiura). Fossil-calibrated molecular phylogenies (Wolfe et al., 2019) demonstrate the superfamily Paguroidea within the infraorder Anomura diverging in the late Triassic to provide six families of which two, Paguroidae and Coenobitidae, are marine and land hermit crabs, respectively. Coenobitidae is the younger, diverging approximately 35 mya. Here we compare anti-DC0-immunoreactive centers in the lateral protocerebrum of the marine hairy hermit crab Pagurus hirsutiusculus with those of the land hermit crab Coenobita clypeatus (McLaughlin et al., 2010).

Observations

In Pagurus, affinity to anti-DC0 (Figure 13A) reveals two immediately adjacent calycal domains in the lateral protocerebrum that together are continuous with an anti-DC0-positive columnar lobe. The neural architecture of the calyces (Figure 13B–D,F–H) is remarkably similar to the organization of afferents and intrinsic neurons in successive layers of the multistratified anti-DC0-immunoreactive hemiellipsoid body of the land hermit crab Coenobita clypeatus (Figure 13I–O). As demonstrated by Golgi impregnations (Wolff et al., 2012; Strausfeld and Sayre, 2020), both Pagurus and Coenobita have corresponding networks provided by a variety of morphological types of intrinsic neurons. These form precisely defined orthogonal networks (Figure 13B,C) of dendritic processes and terminals. In Pagurus, one population of intrinsic neurons provides axon-like extensions into the lobes (Strausfeld and Sayre, 2020). In Coenobita, all of the axon-like processes of intrinsic neurons are constrained to within the layered arrangements of its hemiellipsoid body (Wolff et al., 2012). In Pagurus, the dendrites of anti-5HT- and anti-TH-immunoreactive MBONs intersect intrinsic neuron terminals in the tubercular swellings at the end of the columnar lobes. The layered arrangements of the dendrites of these immunoreactive neurons reflect the repeat organization of precisely aligned intrinsic neuron dendrites across each calyx’s width (Figure 13C,E).

Figure 13

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The hemiellipsoidal mushroom body of Coenobita clypeatus

Background

The anomuran family Coenobitidae, to which the Caribbean land hermit crab belongs, is a recent group appearing approximately 35–40 mya (Bracken-Grissom et al., 2013; Wolfe et al., 2019). Coenobita clypeatus and its cousin the coconut crab Birgus latro have attracted considerable attention regarding olfactory adaptations associated with terrestrialization (Stensmyr et al., 2005). However, the juveniles develop in a marine habitat and, as expected, their antennular olfactory receptor neurons are typical of marine species in possessing ionotropic receptors, the axons of which terminate in large deutocerebral olfactory lobes (Harzsch and Hansson, 2008; Groh et al., 2013).

Observations

As shown in both B. latro and C. clypeatus, massive relays from the olfactory lobes project to the lateral protocerebra to terminate in greatly inflated centers referred to as hemiellipsoid bodies (Harzsch and Hansson, 2008). These neuropils are defined by numerous anti-DC0-positive stratifications (Figure 14A,B). Golgi impregnations and electron microscopy demonstrated that these tiered arrangements consist of orthogonal networks of intrinsic neurons, postsynaptic to afferent terminals and presynaptic to dendrites, resulting in an organization that corresponds to circuitry recognized in the insect mushroom body’s columnar lobe (Brown and Wolff, 2012; Wolff et al., 2012). Volumes of neuropil situated laterally beneath the dome are also anti-DC0-positive, as is a globular center corresponding to the reniform body (Figure 14A,B). The correspondence of this center’s internal organization with that of a mushroom body’s column is further demonstrated by the arrangements of dendritic trees belonging to output neurons, which are equivalent to MBONs. Figure 14C shows that anti-TH- and anti-5HT-immunoreactive dendrites extend across strata, each of which is also defined by synaptic configurations revealed by F-actin and anti-synapsin (Figure 14D) and, in Figure 14F, by anti-α-tubulin and an antibody against PKA-RII that regulates DC0 (see Methods). Antibodies against GAD reveal broadly distributed processes that are not aligned within rows but extend across them (Figure 14C,E).

Figure 14

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Extreme divergence of the mushroom body in Brachyura

Background

Brachyura (true crabs) is a species-rich infraorder, now comprising about 6800 species (Ng et al., 2008), which diverged 240 mya (Wolfe et al., 2019). Here we consider two species, both of which spend intertidal periods out of water, the shore crab Hemigrapsus nudus (Varunidae) and fiddler crab Uca (Minuca) minax (Ocypodidae). Fossil-calibrated molecular phylogenies indicate a mid-to-late Cretaceous origin for the Varunidae and Ocypodidae (Tsang et al., 2014; Wolfe et al., 2019).

The opportunistic detritivore H. nudus lives in a flat visual ecology interrupted by occasional pebbles and rocks. These shore crabs often come into immediate contact with each other, where they may initiate contact-induced actions, such as defensive aggression involving jousting and pushing, but there is no obvious ritualized courtship as there is in fiddler crabs. Individuals employ crevices as transitory residences, responding to predatory threats by opportunistically retreating and hiding in them (Jacoby, 1981). It is likely that they can deploy allocentric memory, judging from the habit of near- or fully-grown individuals to retreat to a specific location when threatened. These actions contrast with those of fiddler crabs, such as Uca minax – deposit feeders living on mudflats – that are renowned for their ritualized courtship displays and rapid path integration to established home sites to escape predation (Crane, 1975), and visual behaviors that relate to compound eyes adapted for vision in a flat world (Zeil and Hemmi, 2006).

Observations

Treatment of eyestalks of six H. nudus with anti-DC0 resulted in four of twelve eyestalks showing barely detectable immunoreactivity with one specimen exhibiting some immunoreactivity in a tributary of the OGT. Eight consistently showed various levels of immunoreactivity in regions of the rostral lateral protocerebrum. Figure 15A–F shows three of five specimens that all resolved strong immunoreactivity of large parts of the rostral neuropil associated with clusters of globuli cells lying over the lateral protocerebrum’s rostral surface. One cluster of globuli cells also supplies a well-defined anti-DC0-immunoreactive neuropil positioned immediately proximal to the lobula. This matches the elaborations of the reniform body (Figure 15E), as resolved in Golgi impregnations and Bodian reduced-silver-stained specimens (Thoen et al., 2019). This center is known to participate in visual habituation and was understandably (but mistakenly) interpreted by Maza et al. (2016) as a mushroom body. As shown by Thoen et al. (2019), this center is not a homologue of the mushroom body or the hemiellipsoid body but is present with either of those centers. Depending on the tilt of sectioning and the section’s depth the intensely anti-DC0-immunoreactive pedestal of the reniform body can be resolved extending obliquely from the rostro-dorsal to the caudal margin of the lateral protocerebrum (Figure 15A–F). Sections of fortuitously oriented blocks can reveal the entire reniform body complex, here shown digitally enhanced against other anti-DC0 territories in Figure 15E.

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Figure 15 depicts territories of the lateral protocerebrum of H. nudus indicating that almost the entire rostral half of the neuropil is occupied by very large anti-DC0-immunoreactive domains characterized by cortex-like boundaries of fissures and lobes (Figure 15B). In H. nudus, the volume associated with the anti-DC0-labelled domain is relatively free of anti-GAD immunoreactivity, whereas antibodies raised against 5HT and TH suggest that anti-TH may be more abundant in the lateral protocerebrum’s upper half than in the lower (Figure 15G,H). The fiddler crab, Uca minax (Figure 15—figure supplement 1), reveals similar anti-RII-immunoreactive territories that also appear to be highly folded. Less extensive than those in H. nudus, the two most immunoreactive territories are separated by a volume showing lower affinity to anti-DC0. Notably, vibratome sections treated with SYNORF1 (anti-synapsin) and phalloidin (F-actin) to resolve synaptic microglomeruli, selectively reveal only specific subterritories of the volume occupied by the anti-DC0-positive center (inset: Figure 15—figure supplement 1 inset).

Scrutiny of anti-DC0 territories identifies anti-synapsin as well as anti-TH- and anti-5HT-immunoreactive arrangements suggestive of mushroom body-like configurations (Figure 15I,J), the locations of which correspond to the boxed area of Figure 15D.

To screen for putative mushroom bodies or centers in corresponding locations we employed anti-DC0 immunostaining of lateral protocerebra. Identified centers were then subjected to various histological techniques to detect character arrangements that define the hexapod-stomatopod mushroom body ground pattern. The nuclear stain Syto13 was used to identify neuronal cell bodies and to distinguish minute basophilic cell bodies associated with anti-DC0-immunoreactive centers. Antisera were used to reveal neuroarchitectures as well as putative serotoninergic and dopaminergic neurons belonging to mushroom body input or output neurons (MBINs, MBONs; Aso et al., 2014a; Aso et al., 2014b) and feedforward or recurrent GABAergic elements within mushroom body circuitry (Perisse et al., 2016; Bicker et al., 1985; Leitch and Laurent, 1996). Reduced silver staining and α-tubulin immunohistology was employed to reveal the fibroarchitecture of the lateral protocerebrum. Golgi impregnation methods revealing quantities of single neurons were used to compare neuronal organization in mushroom bodies and their suspected ‘hemiellipsoid body’ homologues in Reptantia.

Data generated and analyzed for this study derive from histological material kept and curated in the first author's laboratory at the Department Neuroscience, University of Arizona.

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Author details

1. Nicholas James Strausfeld

   Department of Neuroscience, School of Mind, Brain and Behavior, University of Arizona, Tucson, United States

   Contribution

   Conceptualization, Resources, Data curation, Formal analysis, Funding acquisition, Investigation, Visualization, Methodology, Writing - original draft, Writing - review and editing

   For correspondence

   flybrain@email.arizona.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-1115-1774

2. Gabriella Hanna Wolff

   Department of Biology, University of Washington, Seattle, United States

   Contribution

   Conceptualization, Resources, Formal analysis, Funding acquisition, Validation, Investigation, Visualization, Methodology, Writing - review and editing

   For correspondence

   gabwolff@uw.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-0075-4975

3. Marcel Ethan Sayre

   Lund Vision Group, Department of Biology, Lund University, Lund, Sweden

   Contribution

   Conceptualization, Resources, Data curation, Formal analysis, Investigation, Visualization, Methodology, Writing - original draft, Writing - review and editing

   For correspondence

   marcel.sayre@biol.lu.se

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-2667-4228

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