Divergent populations across different environments are exposed to critical sensory information related to locating a host or mate, as well as avoiding predators and pathogens. These sensory signals generate evolutionary changes in neuroanatomy and behavior; however, few studies have investigated patterns of neural architecture that occur between sensory systems, or that occur within large groups of closely-related organisms. Here we examine 62 species within the genus Drosophila and describe an inverse resource allocation between vision and olfaction, which we consistently observe at the periphery, within the brain, as well as during larval development. This sensory variation was noted across the entire genus and appears to represent repeated, independent evolutionary events, where one sensory modality is consistently selected for at the expense of the other. Moreover, we provide evidence of a developmental genetic constraint through the sharing of a single larval structure, the eye-antennal imaginal disc. In addition, we examine the ecological implications of visual or olfactory bias, including the potential impact on host-navigation and courtship.

Here we report on ultrastructural features of brain synapses in the fly Drosophila melanogaster and outline a perspective for the study of their functional significance. Images taken with the aid of focused ion beam-scanning electron microscopy (EM) at 20 nm intervals across olfactory glomerulus DA2 revealed that some synaptic boutons are penetrated by protrusions emanating from other neurons. Similar structures in the brain of mammals are known as synaptic spinules. A survey with transmission EM (TEM) disclosed that these structures are frequent throughout the antennal lobe. Detailed neuronal tracings revealed that spinules are formed by all three major types of neurons innervating glomerulus DA2 but the olfactory sensory neurons (OSNs) receive significantly more spinules than other olfactory neurons. Double-membrane vesicles (DMVs) that appear to represent material that has pinched-off from spinules are also most abundant in presynaptic boutons of OSNs. Inside the host neuron, a close association was observed between spinules, the endoplasmic reticulum (ER) and mitochondria. We propose that by releasing material into the host neuron, through a process triggered by synaptic activity and analogous to axonal pruning, synaptic spinules could function as a mechanism for synapse tagging, synaptic remodeling and neural plasticity. Future directions of experimental work to investigate this theory are proposed.

To manage the great complexity of detecting and identifying olfactory cues, the insect olfactory system has evolved two main strategies: combinatorial coding and specialized, narrowly tuned olfactory pathways. In combinatorial coding, odorants are encoded by activation of multiple, broadly tuned olfactory sensory neurons that innervate distinct sets of glomeruli. In specialized olfactory pathways, information regarding a single or a few odorants is processed in a discrete, narrowly tuned circuit within a dedicated glomerulus. Here, we compared the narrowly tuned glomerulus DA2 with the broadly tuned glomerulus DL5 at the ultrastructural level, by using volume based focused ion beam scanning electron microscopy. We provide a detailed analysis of neuronal innervation, synaptic composition as well as a circuit diagram of the major glomerular cell types: olfactory sensory neurons (OSNs), uniglomerular projection neurons (uPNs) and multiglomerular neurons (MGNs). By comparing our data with a previously mapped narrowly tuned glomerulus (VA1v), we disclose putative generic features of narrowly tuned glomerular circuits: a high density of neuronal fibers and synapses, a low degree of sensory lateralization, strong axo-axonic connections between OSNs as well as dendro-dendritic connections between uPNs, and a low degree of presynaptic inhibition at the OSN axons. We also show a unique property of the large uPN dendrite in DL5, which forms substantial amount of autapses.

In the Drosophila olfactory system most odorants are encoded in the antennal lobe in a combinatory way, activating several glomerular circuits. However, odorants of particular ecological role for the fly are encoded through activation of a single specialized olfactory pathway. Comparative analyses of densely reconstructed connectomes of one broadly tuned glomerulus (DL5) and one narrowly tuned glomerulus (DA2) gained detailed insight into the variations of synaptic circuitries of glomeruli with different computational tasks. Our approach combined laser-branding of glomeruli of interest with volume based focused ion beam-scanning electron microscopy (FIB-SEM) to enable precise targeting and analysis of the two glomeruli. We discovered differences in their neuronal innervation, synaptic composition and specific circuit diagrams of their major cell types: olfactory sensory neurons (OSNs), uniglomerular projection neurons (uPNs) and multiglomerular neurons (MGNs). By comparing our data with a previously mapped narrowly tuned glomerulus (VA1v), we identified putative generic features of narrowly tuned glomerular circuits, including higher density of neuronal fibers and synapses, lower degree of OSN lateralization, stronger axo-axonic connections between OSNs, dendro-dendritic connections between many uPNs, and lower degree of presynaptic inhibition on OSN axons. In addition, this work revealed that the dendrites of the single uPN in DL5 contain a substantial amount of autapses interconnecting distant regions of the dendritic tree. The comparative analysis of glomeruli allows to formulate synaptic motifs implemented in olfactory circuits with different computational demands.

In the Drosophila olfactory system most odorants are encoded in the antennal lobe in a combinatory way, activating several glomerular circuits. However, odorants of particular ecological role for the fly are encoded through activation of a single specialized olfactory pathway. Comparative analyses of densely reconstructed connectomes of one broadly tuned glomerulus (DL5) and one narrowly tuned glomerulus (DA2) gained detailed insight into the variations of synaptic circuitries of glomeruli with different computational tasks. Our approach combined laser-branding of glomeruli of interest with volume based focused ion beam-scanning electron microscopy (FIB-SEM) to enable precise targeting and analysis of the two glomeruli. We discovered differences in their neuronal innervation, synaptic composition and specific circuit diagrams of their major cell types: olfactory sensory neurons (OSNs), uniglomerular projection neurons (uPNs) and multiglomerular neurons (MGNs). By comparing our data with a previously mapped narrowly tuned glomerulus (VA1v), we identified putative generic features of narrowly tuned glomerular circuits, including higher density of neuronal fibers and synapses, lower degree of OSN lateralization, stronger axo-axonic connections between OSNs, dendro-dendritic connections between many uPNs, and lower degree of presynaptic inhibition on OSN axons. In addition, this work revealed that the dendrites of the single uPN in DL5 contain a substantial amount of autapses interconnecting distant regions of the dendritic tree. The comparative analysis of glomeruli allows to formulate synaptic motifs implemented in olfactory circuits with different computational demands.