Postembryonic lineages of the Drosophila ventral nervous system: Neuroglian expression reveals the adult hemilineage associated fiber tracts in the adult thoracic neuromeres

Abstract

During larval life most of the thoracic neuroblasts (NBs) in Drosophila undergo a second phase of neurogenesis to generate adult‐specific neurons that remain in an immature, developmentally stalled state until pupation. Using a combination of MARCM and immunostaining with a neurotactin antibody, Truman et al. (2004; Development 131:5167–5184) identified 24 adult‐specific NB lineages within each thoracic hemineuromere of the larval ventral nervous system (VNS), but because of the neurotactin labeling of lineage tracts disappearing early in metamorphosis, they were unable extend the identification of these lineages into the adult. Here we show that immunostaining with an antibody against the cell adhesion molecule neuroglian reveals the same larval secondary lineage projections through metamorphosis and bfy identifying each neuroglian‐positive tract at selected stages we have traced the larval hemilineage tracts for all three thoracic neuromeres through metamorphosis into the adult. To validate tract identifications we used the genetic toolkit developed by Harris et al. (2015; Elife 4) to preserve hemilineage‐specific GAL4 expression patterns from larval into the adult stage. The immortalized expression proved a powerful confirmation of the analysis of the neuroglian scaffold. This work has enabled us to directly link the secondary, larval NB lineages to their adult counterparts. The data provide an anatomical framework that 1) makes it possible to assign most neurons to their parent lineage and 2) allows more precise definitions of the neuronal organization of the adult VNS based in developmental units/rules. J. Comp. Neurol. 524:2677–2695, 2016. © 2016 The Authors The Journal of Comparative Neurology Published by Wiley Periodicals, Inc.

Doublesex Regulates the Connectivity of a Neural Circuit Controlling Drosophila Male Courtship Song

“…The neurons within each hemilineage tend to develop similar arborization patterns (Truman et al, 2004) and contribute to specific, different subsets of adult fly behaviors (Harris et al, 2015;Truman et al, 2004). For example, neurons of hemilineage 12A innervate the dorsal neuropil of the ventral nervous system, including the tectulum and the wing neuropil, and thus arborize in appropriate locations to regulate wing movements (Shepherd et al, 2016). Many hemilineage 12A neurons develop in similar ways in males and females and contribute to various wing movements (Harris et al, 2015), whereas others, such as the TN1 neurons, are present in males but not females and contribute specifically to male courtship song.…”

Developmental organization of central neurons in the adult Drosophila ventral nervous system

“…In this study, we have presented and analyzed the adult morphology of postembryonically induced MARCM clones to reveal the anatomy of the vast majority of adult neuronal lineages in the thoracic neuromeres of the VNS. This work builds on previous studies of the developmental origins of the adult neurons of the VNS (Harris, Pfeiffer, Rubin, & Truman, ; Shepherd et al, ; Truman et al, ) to produce a definitive description of the clonal organization of neurons in the adult VNS. We present data for 58 of the 66 postembryonic thoracic lineages (85 of the 98 possible thoracic hemilineages), excluding the motor neuron producing lineages (15 and 24 found in all thoracic hemineuromeres).…”

“…While Truman et al () provided insight into the larval organization of the postembryonic neurons, they were unable to study the hemilineages in adult stages because the neurotactin labeling, used to identify each hemilineage, disappeared early in metamorphosis. In this study, we have overcome this limitation by building on the work of Shepherd, Harris, Williams, and Truman (), who used an antibody to neuroglian to reveal the hemilineage scaffold from larva through metamorphosis and into the adult VNS, to follow every larval lineage through metamorphosis to identify its adult fate.…”

Unc-4 acts to promote neuronal identity and development of the take-off circuit in the Drosophila CNS

“…The adult fly VNC is composed of 34 segmentally repeated hemilineages, which are groups of lineally related neurons with similar features e.g., axonal projection and neurotransmitter expression (TRUMAN et al 2004;TRUMAN et al 2010;LACIN et al 2014;HARRIS et al 2015;LACIN AND TRUMAN 2016;SHEPHERD et al 2016;LACIN et al 2019;SHEPHERD et al 2019). These hemilineages also appear to function as modular units, each unit appears responsible for regulating particular behaviors, indicating the VNC is assembled via a lineage-based functional organization (HARRIS et al 2015).…”

“…We previously mapped the embryonic origin, axonal projection pattern, transcription factor expression, and neurotransmitter usage of essentially all hemilineages in the adult Drosophila VNC (TRUMAN et al 2004;TRUMAN et al 2010;LACIN et al 2014;HARRIS et al 2015;LACIN AND TRUMAN 2016;SHEPHERD et al 2016;LACIN et al 2019;SHEPHERD et al 2019). Here, we leverage this information to elucidate how a specific transcription factor, Unc-4, acts within individual hemilineages during adult nervous system development to regulate neuronal connectivity and function, and animal behavior.…”