Abstract
Changes to the structure and function of neural networks are thought to underlie the evolutionary adaptation of animal behaviours. Among the many developmental phenomena that generate change programmed cell death (PCD) appears to play a key role. We show that cell death occurs continuously throughout insect neurogenesis and happens soon after neurons are born. Mimicking an evolutionary role for increasing cell numbers, we artificially block in the medial neuroblast lineage in Drosophila melanogaster, which results in the production of 'undead' neurons with complex arborisations and distinct neurotransmitter identities. Activation of these 'undead' neurons and recordings of neural activity in behaving animals demonstrate that they are functional. Focusing on two dipterans, which have lost flight during evolution, we reveal that reductions in populations of flight interneurons are likely caused by increased cell death during development. Our findings suggest that the evolutionary modulation of death-based patterning could generate novel network configurations.
Highlights
In insects the number and arrangement of neural progenitor cells that generate central neurons is highly conserved despite a remarkable diversity of insect body plans and behaviors
Our findings suggest that the evolutionary modulation of death-based patterning could generate novel network configurations. 16 KEYWORDS Programmed cell death, postembryonic neurogenesis, hemilineage, medial neuroblast, octopamine, evo-devo, ventral nerve cord, Drosophila melanogaster, Braula coeca, Crataerina pallida, Thermobia domestica 21 INTRODUCTION Nervous systems are exquisitely adapted to the biomechanical and ecological environments in which they operate
Because programmed cell death (PCD) selectively eliminates hemilineages in the fruit fly, and has been reported to kill off immature octopaminergic neurons produced by the median neuroblast (MNB) in the grasshopper (Jia and Siegler, 2002), we wondered if PCD occurs in the development of the central nervous system (CNS) in a ‘primitive’
Summary
In insects the number and arrangement of neural progenitor cells that generate central neurons (termed neuroblasts, NBs) is highly conserved despite a remarkable diversity of insect body plans and behaviors Flying insects have greater numbers of octopaminergic neurons within segments that control wings (Figure 1D; Stevenson and Spörhase-Eichmann, 1995), while grasshoppers have more GABAergic neurons in the fused metathoracic/abdominal ganglia, where they receive auditory input from the abdomen (Figure 1D; Witten and Truman, 1998; Thompson and Siegler 1991). The greater number of GABAergic cells in each segment results from PCD targeting octopaminergic neurons in both grasshoppers (Jia and Siegler, 2002) and fruit flies (Truman et al, 2010). Except for the moth, a higher number of octopaminergic neurons can be found in winged segments in flying insects (yellow boxes) Cell numbers in this homologous lineage vary both between segments and species. Lineage 0 is the postembryonic name given to the MNB lineage
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