COMMENTARY

What brains say about arthropod phylogeny

Susan E. Fahrbach* Department of Entomology, University of Illinois at Urbana–Champaign, 320 Morrill Hall, 505 South Goodwin Avenue, Urbana, IL 61801

hat can we learn from the joining and but plac- innermost neuropil, are linked by chias- brain of a single member ing a non- hexapod group, the mata. Similar optic neuropils can be of a species? If the brain is Collembola, outside of (9). readily discerned in crustaceans, which, that of a remipede, the These molecular phylogenies are at like insects, also have compound eyes. focusW of a report by Fanenbruck et al. odds with striking morphological syna- The lamina in both of these groups is (1) in this issue of PNAS, the answer is pomorphies that unite the organized into columnar visual sampling something new about arthropod phylog- and , such as tracheae, Mal- units called optic cartridges of similar eny. The Remipedia, discovered in 1979, pighian tubules, and the absence of sec- cellular composition. The are crustaceans found deep in the wa- ond antennae. A reexamination of these (decapods such as crabs and lobsters, ters of coastal caves (2, 3). To date, morphological characters from a de- and the isopods) also have three distinct twelve species of remipedes are known: tailed cellular, molecular, and develop- optic neuropils joined by two chiasmata. one from a single cave in Western Aus- mental perspective therefore is By contrast, other crustaceans such as tralia and the others from the Carib- warranted. the shrimps () and copep- bean. The remipede body is divided into ods () have no lobula com- a head and an elongated trunk with up Phylogenetic Reconstruction and plex and lack a chiasma between the to 32 segments. The trunk segments fea- Neuroanatomy lamina and the medulla. Analysis of a ture paddle-like appendages that give As Strausfeld (10) has indicated, infer- large library of arthropod brains led the taxon its name (‘‘oar feet’’). Remi- ence of phylogeny from shared neural Strausfeld to suggest that all optic lobe pedes show adaptations to life in dark- characters is by no means a new ap- features proximal to the medulla are ness, including the absence of pigmenta- proach, but it was not until the 1990s products of convergence (homoplasies), tion and eyes, but like other crustaceans that modern researchers sought inspira- with similarities reflecting constraints they have two pairs of antennae. tion from the early 20th century investi- imposed initially by the organization of The evolutionary history of these rare gations of Holmgren and Hanstro¨m on the photoreceptors and secondarily by is uncertain. In their study the brains of arthropods. Recent en- the organization of the lamina and me- of the brain of Godzilliognomus fron- deavors in this field have naturally been dulla (10, 11). Strausfeld’s groundbreak- dosus, Fanenbruck et al. (1) provide a stimulated by the opportunity to apply ing analysis, based not just on the optic fresh look at remipede phylogeny. Their advanced cell-labeling techniques to ar- lobes but on 100 neural features scored neuroanatomical studies suggest that thropod brains, but techniques alone do as present or absent in 28 taxa, yielded the Remipedia are most likely part of not drive the renascence of comparative a tree identifying hexapods and crusta- a larger clade that includes the Mala- neuroanatomy. Some of the most excit- ceans as sister groups. costraca and the Hexapoda, two arthro- ing new studies rely on venerable meth- This topic was readdressed by Harzsch pod groups well known for their ods such as Bodian’s reduced silver stain (12) in a study of insect, malacostracan, complex brains. and the Golgi technique. Instead, it is and branchiopod optic neuropils by This result is surprising because, at controversy produced by discrepancies antihistamine immunocytochemistry. first inspection, the simplicity of the between morphological and molecular Harzsch interpreted his data as evidence remipede body plan suggests that this phylogenies of the arthropods that has against convergence, arguing that the group provides a glimpse of untagma- shown neuroanatomists ‘‘where to look.’’ third optic neuropil and the two optic tized ancestors with numerous unspe- Three arthropod brain regions have chiasmata are synapomorphies for Mala- cialized appendages and should be received much attention in recent stud- costraca and Insecta (13). Strausfeld and placed in a basal position in the crusta- ies: the optic lobes, mushroom bodies, colleagues (14) revisited the issue of cean lineage (4). This view, based on and central complex. Other major brain optic lobe architecture in a study with gross morphology, is contradicted by regions have been less extensively ana- antisera to the inhibitory neurotransmit- molecular analyses suggesting that the lyzed. Comparisons of the aforemen- ter ␥-aminobutyric acid (GABA). One remipedes are a sister group to the tioned brain regions generally provide striking finding was the absence of evi- hexapods (six-legged arthropods, includ- support for the pancrustacean hypothe- dence that the medulla is ing insects) (5, 6). These studies were sis. Brain-based conclusions regarding divided into inner and outer regions, based on comparisons of sequences for arthropod phylogeny, however, typically leading (along with other details of op- RNA polymerase II and elongation fac- remain tentative because certain groups, tic neuropil structure and development) tors 1 and 2. The results not only ele- such as the Chilopoda and Diplopoda, to the conclusion that the lamina and vated the Remipedia from a basal sta- are understudied, and others, such as outer medulla of insects are homologous tus, but also provided support for the the Remipedia, have until now not been to the lamina and the entire medulla of much-discussed idea that hexapods are studied at all. the malacostracans. These consider- more closely related to crustaceans than ations highlight a characteristic tension to the other tracheated arthropods, the Optic Lobes in this field. It can be argued that differ- and (Chilopoda The optic lobes of insects comprise a set ences in the morphology of GABAergic and Diplopoda; collectively, Myriapoda). of three nested, retinotopic neuropils. strata in insect and crustacean medullas This hypothesis unites the hexapods and The outermost of these neuropils, the crustaceans in a larger clade designated lamina, receives direct inputs from pho- Pancrustacea (7, 8). Recent phylogenetic toreceptors in the compound eye. The See companion article on page 3868. reconstructions based on complete mito- lamina and the medulla, and in turn the *E-mail: [email protected]. chondrial genomes go a step further by medulla and the lobula complex, the © 2004 by The National Academy of Sciences of the USA

www.pnas.org͞cgi͞doi͞10.1073͞pnas.0400472101 PNAS ͉ March 16, 2004 ͉ vol. 101 ͉ no. 11 ͉ 3723–3724 Downloaded by guest on September 26, 2021 are simply details; it can be equally ar- a set of protocerebral midline neuropils. located on the basal segments of the first gued that they change everything. Note, In insects, these complex neuropils in- pair of antennae. The tritocerebrum, however, that both data sets are consis- clude a distinctive ellipsoid body, a fan- which receives inputs from the nonchemo- tent with a malcostracan͞insect clade, shaped body, a pair of lateral neuropils sensory second pair of antennae and in- although the proposed neuroanatomical connected by a protocerebral bridge, nervates the cephalic shield, is similar in synapomorphies are different. and a pair of noduli immediately ventral organization to the tritocerebrum of mala- to the ellipsoid body. Unpaired midline costracans. These observations, particu- Deutocerebrum and Mushroom Bodies neuropils are present in crustaceans, but larly the organization of the deutocere- The mushroom bodies are the insect they are simpler in structure and con- brum, leave us with a brain like that of an brain structure best known to non-ento- tain fewer subunits than the insect cen- eyeless malacostracan: distinct olfactory mologists because of their functional tral complex (19). In a study with anti- glomeruli, bipartite 1 neuropils, association with learning and memory sera directed against tachykinin-related and a prominent olfactory globular tract (15) and their structural plasticity in peptide (TRP) and allatostatins, Loesel that links the olfactory glomeruli with adult insects (16). A set of lobed neuro- et al. (20) reported that all groups exam- the hemiellipsoid bodies. The results of pils originating from dorsal clusters of ined but the Diplopoda have the same Fanenbruck et al. (1) therefore provide numerous small neurons (globuli or Ke- protocerebral midline structures. Al- support for the hypothesis of a Remipedia– nyon cells), they are typically the most though the key finding in this report is Malacostraca–Hexapoda clade. prominent features of the insect proto- refutation of the monophyly of the Adult Brains Are Useful, Too cerebrum. One of their functions is to Myriapoda, new information is pre- serve as a second order olfactory neuro- sented on the midline structures of Comparative studies of gene expression pil, and they receive massive ipsilateral malocostracans, who match the insects during early development have contrib- projections from the deutocerebral ol- in many details of central complex struc- uted significantly to our understanding factory interneurons, but mushroom ture, including the presence of distinct of arthropod relationships and the evo- bodies are present even in primarily and allatostatin- and TRP-positive layers. lution of the arthropod body plan (21). The present study joins a growing num- secondarily anosmic insects (17). The ber of articles demonstrating the contri- presence of recognizable mushroom The Remipede Brain butions comparative neuroanatomy of body-like structures in other inverte- It is against this background that the adult brains can make to phylogenetic brates such as annelids and onych- rich implications of the Fanenbruck et reconstruction (10, 12, 14, 17), even ophorans diminishes the usefulness of al. study (1) of Godzilliognomus frondo- when, as in the case of the Remipedia, the mushroom bodies for phylogenetic sus can be appreciated. Because this developmental studies are impossible. reconstruction. Either mushroom bodies remipede is eyeless, there are no optic This study further draws attention to the were present deep in the ancestry of neuropils to consider. In the protocere- relative lack of detailed comparative groups that we recognize today as being brum, this leaves us with the hemiellip- studies of regions of the arthropod brain significantly diverged, or they have soid bodies and the midline neuropils. beyond the protocerebrum and its asso- evolved independently many times. The hemiellipsoid bodies strongly resem- ciated optic lobes. The comparative neu- Surprisingly, there are no mushroom ble those of malacostracans. The major roanatomy of the deutocerebrum and bodies in crustaceans. Instead, the proto- components of the malacostracan mid- tritocerebrum need a level of scrutiny cerebral projections of olfactory interneu- line neuropils are also recognizable. equal to that afforded by recent studies rons project bilaterally to dense neuropils Fanenbruck et al. also estimate that the to the optic lobes, the mushroom bodies, called hemiellipsoid bodies (18), which are number of neurons in the remipede pro- and the central complex. Elucidating associated with numerous globuli cells but tocerebrum is larger than in branchio- details of cell cytoarchitectonics and do not have either the lobed structure or pods, comparable to the greater num- patterns of immunoreactivity are the parallel fibers of the insect mushroom bers found in malacostracans and first steps, but, following the lead of the body. Although early 20th century neuro- insects. developmental biologists, comparative anatomists assumed that the hemiellipsoid The absence of optic neuropils in studies of gene expression must follow bodies were highly modified mushroom Remipedia has led to a focus on the less- when possible so that we do not over- bodies, this assertion of homology remains studied deutocerebrum and tritocerebrum. look homologies concealed by the com- unproved. In the deutocerebrum, the presence of plexity of the adult arthropod brain. A glomeruli comparable to the olfactory synthesis of evo–devo approaches to Central Complex glomeruli of malacostracans (and insects) nervous system development with com- The third set of characters that has at- is convincingly argued. These glomeruli parative studies of adult brains could be tracted the attention of comparative appear to receive inputs from the aes- the key that unlocks the phylogeny of neuroanatomists is the central complex, thetascs, rows of chemosensory neurons the arthropods.

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