Diversity and Evolution of the Insect Ventral Nerve Cord Jeremy E. Niven,1'2 Christopher M. Graham,2 and Malcolm Burrows2 Smithsonian Tropical Research Institute, Panama City, Republic of Panama -Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom; email: [email protected]; [email protected] Annu. Rev. Entomol. 2008. 53:253-71 Key Words First published online as a Review in Advance on ganglion, central nervous system, phylogeny, energetic costs, September 5, 2007 modularity, convergence The Annual Review of Entomology is online at ento.annualreviews.org Abstract This article's doi: Is the remarkable diversity in the behavior of insects reflected in 10.1146/annurev.ento.52.110405.091322 the organization of their nervous systems? The ventral nerve cords Copyright © 2008 by Annual Reviews. (VNCs) have been described from over 3 00 insect species covering All rights reserved all the major orders. Interpreting these data in the context of phy- 0066-4170/08/0107-0253$20.00 logenetic relationships reveals remarkable diversity. The presumed ancestral VNC structure is rarely observed; instead the VNCs of most insects show extensive modification and substantial conver- gence. Modifications include shifts in neuromere positions, their fusion to form composite ganglia, and, potentially, their separation to revert to individual ganglia. These changes appear to be facili- tated by the developmental and functional modularity of the VNC, a neuromere for each body segment. The differences in VNC struc- ture emphasize trade-offs between behavioral requirements and the costs incurred while maintaining the nervous system and signaling between its various parts. The diversity in structure also shows that nervous systems may undergo dramatic morphological changes dur- ing evolution. -r. INTRODUCTION developmental constraint (49, 117), although some individual brain regions can change dra- The insects are the most speciose group of matically in volume relative to body mass (8, Ventral nerve cord animals on the planet, making up 63% of 117). Although no such relationships have (VNC): the chain of all named species (53). They have a vast be- been described for insects, it seems likely that ganglia linked by havioral repertoire that encompasses numer- paired connectives the structure of the nervous system in modern ous locomotory, feeding, and reproductive and lying beneath insect species has been influenced by the de- the alimentary canal strategies, as well as learning, navigation, and sign of the ancestral nervous system (43, 55, communication. Their behavior may differ Central nervous 67,115). system (CNS): radically in the wide range of habitats that dif- Strong selective pressures to generate region of the nervous ferent insects inhabit. Closely related species, adaptive behavior with a limited energy bud- system composed of as well as castes, sexes, and morphs within get suggest that the nervous system should the brain, species, may also show dramatic differences subesophageal be diverse and specialized, within the bounds in behavior. Furthermore, larval and adult in- ganglion, and ventral set by both physical and developmental nerve cord along sects frequently differ radically in lifestyle, constraints on these evolutionary processes. with several smaller body form, and behavior. The evolution of Many comparative studies of the neurons or ganglia this behavioral diversity must have required neural circuits of insects and other inverte- Neuromere: part of morphological or physiological changes in the brates have concluded that neuronal mor- the central nervous nervous system or sometimes both. The ner- phology is highly conserved during evolution system belonging to vous systems of both invertebrates and ver- one body segment (43, 67, 106), although at more recent phy- tebrates, however, are constrained by limited that contains the logenetic scales, anatomical variation may be neural circuitry energy budgets for neural processing (74, 87, sufficient to infer phylogenetic relationships responsible for the 88), physical limitations of their design (45) (4,25,26, 112, 115). Thus, the extent of mor- processing of sensory and the space they can occupy (118), and the phological and physiological diversity within signals of a segment processes by which they are formed during and for controlling insect nervous systems remains unclear. The development (49). the movements of insect ventral nerve cord (VNC) provides an that segment Large amounts of energy are needed to ideal starting point from which to assess the maintain a nervous system and to process in- extent of diversity of central nervous systems formation within neural circuits (6, 76, 88, (CNSs), particularly given its modular struc- 90). Constraints on the energy budget of an- ture, with a neuromere associated with each imals therefore suggest that there is strong body segment. Indeed, the small size and low selective pressure to reduce neural structures resting metabolic rates relative to body mass and neural processing to the minimum nec- of many insects and the high energetic de- essary to behave appropriately (87, 88, 121). mands of behaviors such as flight (1, 89, 104) In contrast, improved performance in specific mean that several factors such as space and en- behavioral tasks is correlated with the expan- ergy constraints may be more acute in the ner- sion of particular regions of both insect and vous systems of insects compared with those vertebrate brains (e.g. 46, 47, 56, 79), which of vertebrates. The overall structure of the is likely to incur additional energetic costs, insect VNC has been documented for many thus implying strong selective pressure to im- species from all of the major insect orders prove behavioral performance. Physical con- (Figure 1) (13-18, 29, 42, 81, 86, 123, 138). straints within the nervous system have also Here, we combine data on the overall struc- been identified. For example, noise generated ture of the insect VNC with phylogenetic ap- by the random fluctuations of voltage-gated proaches and recent advances in understand- ion channels places lower limits on axon di- ing the costs associated with nervous systems ameter (45). Similarly, in mammals, concomi- to assess the diversity and evolution of the tant changes in the volumes of specific brain insect VNC. regions relative to body mass may represent a 2H Niven • Graham • BWTOVJS NEUROMERES, GANGLIA, distortion of the two original outlines with, AND FUSION at most, a small indentation between neu- romeres. Insects are segmental animals and their CNSs Ganglion: part of reflect, although sometimes only obliquely, the central nervous their segmentally based developmental pro- system consisting of one or more gram. The number of pregnathal segments DIVERSITY IN VENTRAL NERVE neuromeres (anterior to the mouthparts) is still debated, CORD STRUCTURE Neuropile: a region but there are likely to be four (53, 129). There Establishing the structure of the ancestral in- of the insect central are three additional gnathal segments (bearing sect VNC is essential for understanding the nervous system the mouthparts) in the head and three thoracic structural changes that have taken place dur- bounded by the segments (pro-, meso-, and metathorax) asso- ing the evolution of the insects. The VNCs cortex of cell bodies ciated with each pair of legs. Ancestrally there documented from the apterygote insect or- and mainly consisting of are 11 abdominal segments, but in almost all ders, Archaeognatha (51, 59) and Zygentoma dendrites, axons, and extant species this number is reduced by one (7, 59, 140), all possess three thoracic (TI- synaptic connections or more segments, depending on the order TS) and eight abdominal ganglia (A1-A8), (53,83,114). ranged across the whole length of the ab- The basic organizational unit of the central domen and ending in a fused terminal gan- nervous system is the neuromere, an accretion glion (Figure la.l). The anterior seven ab- of neurons that are responsible for processing dominal ganglia (A1-A7) are unfused and the sensory signals of a segment and for control- terminal ganglion (A8) consists of at least ling the movements of that segment. These three fused neuromeres. Thus, the ancestral segmental neuromeres are combined in var- condition is likely to have been that all tho- ious ways to form the pre-oral, dorsal brain, racic and abdominal neuromeres were un- the subesophageal ganglion, and the thoracic fused except for the three to four neuromeres and abdominal ganglia of the VNC, which to- contributing to the terminal abdominal gan- gether form most of the CNS (22, 109, 114). glion. What is the arrangement of thoracic Each of these structures is linked in a chain and abdominal ganglia in extant groups of by pairs of connectives that consist of the ax- winged insects? ons of many different types of neurons. Each The Pterygota or winged insects are ex- segmental ganglion of the ventral chain may traordinarily diverse in their size, body form, consist of a single neuromere or it may be a and behavior. Within and between the differ- fusion of two or more neuromeres. In ganglia ent orders there is a corresponding diversity composed of two or more fused neuromeres, in the size, structure, and position of ganglia the connectives between neuromeres are re- along the VNC relative to the segments they duced in length but still exist as tracts of axon innervate, and in the fusion patterns of neigh- bundles within the fused neuropile areas (22, boring ganglia (Figure 1). The