Evolution of the larval peripheral nervous system in Drosophila species has involved a change in sensory cell lineage

Abstract

A key challenge in evolutionary biology is to identify developmental events responsible for morphological changes. To determine the cellular basis that underlies changes in the larval peripheral nervous system (PNS) of flies, we first described the PNS pattern of the abdominal segments A1-A7 in late embryos of several fly species using antibody staining. In contrast to the many variations reported previously for the adult PNS pattern, we found that the larval PNS pattern has remained very stable during evolution. Indeed, our observation that most of the analysed Drosophilinae species exhibit exactly the same pattern as Drosophila melanogaster reveals that the pattern observed in D. melanogaster embryos has remained constant for at least 40 million years. Furthermore, we observed that the PNS pattern in more distantly related flies (Calliphoridae and Phoridae) is only slightly different from the one in D. melanogaster. A single difference relative to D. melanogaster was identified in the PNS pattern of the Drosophilinae fly D. busckii, the absence of a specific external sensory organ. Our analysis of sensory organ development in D. busckii suggests that this specific loss resulted from a transformation in cell lineage, from a multidendritic-neuron-external-sensory-organ lineage to a multidendritic-neuron-solo lineage.

FlyPNS, a database of the Drosophila embryonic and larval peripheral nervous system

“…1), with the notable presence of 13 neurons in the dorsal cluster (as also mentioned recently in [10,11]). In previous representations that indicated a smaller number of cells in the cluster, either the anterior-located Cut-negative neuron that we have named dmd1 (Fig.…”

“…Since we found that the precise position of sensory cells may vary with segment, embryo and developmental stage (unpublished data), the most reliable criteria for identification of Drosophila embryonic and larval sensory organs are marker expression and cell morphology, and these should be used whenever possible. Our study of the cell markers Cut, Collier, E7-2-36, E7-3-49, Elav, Engrailed and Nubbin/Pdm1 [11-13] and unpublished data), as well as neuron morphology [8,13], revealed that distinctive features can be attributed to each neuron, thereby allowing the unambiguous identification of every PNS neuron. The sections entitled Sensory organ description, Antibodies and enhancer-traps, and Gal4 lines relate these observations.…”

colliertranscription in a singleDrosophilamuscle lineage: the combinatorial control of muscle identity

“…During embryogenesis, col is expressed in the MD2/PS0 head region, the somatic DA3 muscle, precursor cells of the lymph gland, a small set of multidendritic (md) neurons of the peripheral nervous system and specific neurons of the central nervous system (CNS) (Baumgardt et al, 2007;Crozatier et al, 2004;Orgogozo and Schweisguth, 2004). We previously generated a lacZ reporter transgene (P{5col::lacZ}, abbreviated P5cl, Fig.…”

Development of the embryonic and larval peripheral nervous system of Drosophila

“…For example ch lineages generate attachment cells and cap cells from the pIIa division, whereas in es organ lineages the analogous division generates the external shaft of the bristle and the socket that anchors this shaft. Specific lineages also generate specialized sensilla by adjustments in lineage‐specific cell death or proliferation . For example, some lineages produce only md neurons, known as the ‘solo‐md’ lineages, due to programmed cell death of pIIa and pIIIb cells .…”