Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea+Hexapoda)

Abstract

The olfactory lobes of crustaceans and the antennal lobes of insects are the primary olfactory brain centers in Tetraconata. Recent publications considered the apparent lack of olfactory centers in several crustacean and insect taxa and structural differences in the organization of olfactory and antennal lobes as evidence for an independent origin of both brain areas. In depth comparison of species within and across tetraconate taxa, however, rather demonstrates that many characters of the organization of tetraconate olfactory centers are shared even among distantly related clades, but have been modified in various taxon-specific ways. From the available data and from comparison with the situation in chilopods, a closely related mandibulate outgroup, we conclude that an olfactory lobe organized into spheroidal glomeruli is a plesiomorphic character of the tetraconate brain. Shared features between decapod crustaceans and neopteran insects are cholinergic uniglomerular afferent neurons, a single large serotonin-immunoreactive neuron, multiglomerular GABAergic local interneurons, and projection neurons of similar morphology. Taxon-specific apomorphies include loss of olfactory sensilla and olfactory lobes in palaeopteran insects, certain branchiopod, maxillopod, and isopod crustaceans, profound changes in glomerular architecture in decapod crustaceans, and decomposition of glomerular boundaries in orthopteroid insects. In holometabolous insects, olfactory afferent projections from mouthpart sensilla are integrated into the antennal lobe and an increased tendency of contralateral connections is observed in lepidopterans and dipterans. Sexual dimorphism of antennal lobes, prominent in several neopteran insects, has most likely occurred convergently, and is not observed in malacostracan crustaceans.