Developmental organization of the mushroom bodies of Thermobia domestica (Zygentoma, Lepismatidae): insights into mushroom body evolution from a basal insect

Abstract

The mushroom bodies of the insect brain are sensory integration centers best studied for their role in learning and memory. Studies of mushroom body structure and development in neopteran insects have revealed conserved morphogenetic mechanisms. The sequential production of morphologically distinct intrinsic neuron (Kenyon cell) subpopulations by mushroom body neuroblasts and the integration of newborn neurons via a discrete ingrowth tract results in an age-based organization of modular subunits in the primary output neuropil of the mushroom bodies, the lobes. To determine whether these may represent ancestral characteristics, the present account assesses mushroom body organization and development in the basal wingless insect Thermobia domestica. In this insect, a single calyx supplied by the progeny of two neuroblast clusters, and three perpendicularly oriented lobes are readily identifiable. The lobes are subdivided into 15 globular subdivisions (Trauben). Lifelong neurogenesis is observed, with axons of newborn Kenyon cells entering the lobes via an ingrowth core. The Trauben do not appear progressively during development, indicating that they do not represent the ramifications of sequentially produced subpopulations of Kenyon cells. Instead, a single Kenyon cell population produces highly branched axons that supply all lobe subdivisions. This suggests that although the ground plan for neopteran mushroom bodies existed in early insects, the organization of modular subunits composed of separate Kenyon cell subpopulations is a later innovation. Similarities between the calyx of Thermobia and the highly derived fruit fly Drosophila melanogaster also suggest a correlation between calyx morphology and Kenyon cell number.