Insect-Like Organization of the Stomatopod Central Complex: Functional and Phylogenetic Implications

Abstract

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

Keywords: central complex; crustaceans; evolution; eye movements; insects; stomatopod.

Figure 1

Stomatopod crustacean, brain and central complex. (A) Gonodactylus smithii, with raised eyes and frontal “head” region (bracketed). Image: Roy Caldwell. (B) Schematic of brain (based on sections of Neogonodactylus oerstedii) showing the fused neuromeres of tritocerebrum (indicated by the antennal lobes, AL (TR)), deutocerebrum (indicated by the antennular olfactory lobes, OL (DE)) and the medial protocerebrum (MP), the latter containing the central complex (enlarged showing protocerebral bridge, PB; fan-shaped and ellipsoid bodies, FB, EB; noduli, NO). Neuropils within the eyestalks comprise the lateral protocerebrum (LP) and optic lobes (La, Me, Lo). Ascending axon bundles (dark gray) from the OL extend to the lateral protocerebra; descending axon bundles (dark blue) extend from the optic lobes, and optic glomeruli to reach the midbrain and central complex. Scale bar for a small example of this species is 2 mm.

Figure 2

Noduli and lateral accessory lobe (LAL) neuropils. (A) Overview of the two lateral bulbs (Bu), paired noduli (No) and LAL. (B) The noduli (one boxed) are prominent and have been resolved in all species so far examined. Unlike in insects, each nodulus appears to have two side-by-side domains, as revealed by FMRF and 5HT immunocytology of N. oerstedii (C) and H. trispinosa (D). (E) Bodian staining resolves the LAL as a multi-lobed neuropil, one of which (boxed) is shown here. (F) Bodian staining of the lateral bulbs distinguishes their large dendritic trees and different staining densities. Scale bars: (B–F) 50 μm.

Figure 3

Modular organization of the PB and projections to the FB. (A) Reconstruction from Bodian serial sections (Pseudosquilla ciliata) and synapsin immunocytology (Gonodactylus smithii) resolve eight modules of the PB. Each module is numbered 1–8. Pairs of modules relate to the w, x, y, z ground pattern of axon projections originally described for the insect CX. Each PB module provides bundled axons (each schematized as a single fiber) that map all eight modules from each side of the bridge across the entire FB, itself divided into eight modules. (B) Bodian stained decussation (box) and PB in P. ciliata. Region of decussation arrowed. (C) Bodian-stained decussation (arrowed) in G. smithii where the y and z bundles are clearly resolved. (D) Anti-synapsin labeled PBs of G. smithii. The box indicates the volume used for the reconstruction lower left. The top- and bottom-right panels show feature extractions revealing tangential processes extending across the bridge (green profiles) and some of the modular dendritic arrays of modular neurons supplying the FB (yellow profiles). (E,F) Enlargements showing tangential processes extending across the bridge. As in other pancrustaceans, these characteristically invert their top-down order at the midline (arrowed). Scale bars: (B–D) 50 μm: (E,F) 25 μm.

Figure 4

Organization of modules and fan-shaped neurons. (A) Reconstruction of the FB and EB of P. ciliata, and some of its largest fan-shaped neurons. These originate from the lateral bulbs (Bu) and anterolateral protocerebral neuropils. (B,C) Serotonin immunolabeling resolved the modular organization of the FB (1–4) as well as major axons, some of which correspond to those identified in P. ciliata. Of interest are minor differences of serotonergic labeling in these two species (H. trispinosa in B, G. smithii in C), particularly the density of labeling and the stratification of the FB, which in G. smithii clearly resolves three layers. The boxed areas indicate the neuropil of the bulbs. Scale bars: (B,C) 100 μm.

Figure 5

Immunocytological partitions of the fan-shaped and ellipsoid bodies in Neogonodactylus oerstedii. Antibodies raised against FMRFamide resolve the EB (upper left) and the upper layer of the modular FB (middle left). In contrast, anti-5HT labels modules through the depth of the FB. Anti-NPF also selectively resolves modules in the FB. In contrast anti-GABA thus far resolves an arch-like territory in the most ventral area of the EB that appears to be supplied by axons entering it from the anterior protocerebrum. Anti-DC0 labels the EB, as it does in Coenobita clypeatus and dicondylic insects (Wolff et al., 2012). Bodian-stained CXs (right hand column) show corresponding cytoarchitectures in P. ciliata. Abbreviations as for other figures. Corresponding areas shown boxed, corresponding axon trajectories indicated by arrows. Scale bars, 50 μm.

Figure 6

Eyestalk convergence at the central complex. (A) Silver stained brain of P. ciliata reveals numerous heterolateral fiber projections to the central complex amongst which are tracts originating from the eyestalks (arrowed). (B) Dye tracing in Haptosquilla trispinosa resolves tracts as providing processes mainly to the FB, showing that most but not all fibers appear to terminate there. (C) Summary figure showing FB in relation to the antennal glomerular tract (AGT), carrying olfactory neuron relays, and the two main tributaries of the heterolateral optic tracts (HOT). (D) Golgi impregnation showing eyestalk axons (above asterisks) extending across the CX, providing discrete terminal processes clustered in the FB modules. Scale bars: (A) 50 μm; (B) 100 μm.

Figure 7

Eyestalk convergence at the central complex. (A) Dextran-fluorescein fills into the LP retrogradely label axons in the AGT and anterogradely filled axons extending to lateral midbrain regions as well as the midline PB. (B) Large heterolateral axons from the LP supplying the FB, their upper margins delineating FB modules. (C) Dextran-Texas Red fills reveal heterolateral inputs to the EB. (D) Detail of the EB showing heterolateral terminals of eyestalk axons. Scale bars: (A,B) 50 μm; (C,D) 25 μm.

Figure 8

PB and central body (CB) connections in two other eumalacostracans. (A) The littoral isopod Ligia exotica. (B) Reconstruction of the PB and bistratified CB showing the incomplete decussation of axons from each side of the PB to the opposite site of the CB. Like other pancrustaceans, transverse fibers spanning the PB undergo a chiasma-like cross over at the mid-line (PBCh). (C) In many eumalacostracans, the CX lacks noduli and an obvious EB homolog. Instead, the composite CB is clearly divided into two levels each with different immunocytological properties: here affinities to allatostatin (green) and tachykinin (magenta) (image: Rudi Loesel). Bodian stained brain reveals the PBCh (D), the contralateral projections of w, x, y, z, bundles (E) and the bistratified architecture of the CB (F). (G) Homolateral projections (HP) of the w, x, y, z projections between the PB and CB in the fossorial crayfish Cherax destructor (H) (after Utting et al., 2000). Scale bars: (C–F) 100 μm.

Figure 9

Central complexes and pancrustacean phylogeny (Oakley et al., 2012). CX organization in the phyletically distant Stomatopoda and Dicondylia (here represented by an odonate naiad) show close correspondence of their PB, FB, EB, and noduli (NO), and the representation of the PB in the FB by decussating axons (inset). Other CXs in eumalacostracans show simpler arrangements. Decapoda have either homolateral PB-CB projections (as in C. destructor) or partially decussating projections, as in Caridea and Dendrobranchiata (examples of species not shown here) that are almost identical to those of monocondylic insects (Strausfeld, 2012). Central complex neuropils, though not their detailed morphologies, have been identified in Branchiopoda (Strausfeld, 2012), Copepoda (Andrew et al., 2012), Remipedia (Fanenbruck et al., 2004), and possibly in Ostracoda. Their presence in cirripede larvae has not been established. There is no evidence for a central complex in Cephalocarida (Stegner and Richter, 2011) where it is assumed to have undergone reduction and loss.

Figure 10

Behavioral actions in stomatopods. Stomatopods frequently compete over burrows in coral reef substrate. Haptosquilla trispinosa (shown here) also meet for potential mating and both activities may be hazardous, hence the approach of the intruder/suitor using the telson as armor. During these encounters, sensory structures such as the antennae, antennules, antennal scales and eyes (for clearer view, see Figure 2) are pointed in a forward position and actively gather information through both independent and conjoint movements. Image: Roy Caldwell.