Evolution of connectivity architecture in theDrosophilamushroom body

Abstract

Brain evolution has primarily been studied at the macroscopic level by comparing the relative size of homologous brain centers between species. How neuronal circuits change at the cellular level over evolutionary time remains largely unanswered. Here, using a phylogenetically informed framework, we compare the olfactory circuits of three closely related Drosophila species that differ radically in their chemical ecology: the generalists Drosophila melanogaster and Drosophila simulans that feed on fermenting fruit, and Drosophila sechellia that specializes on ripe noni fruit. We examine a central part of the olfactory circuit that has not yet been investigated in these species, the connections between the projection neurons of the antennal lobe and the Kenyon cells of the mushroom body, an associative brain center, to identify species-specific connectivity patterns. We found that neurons encoding food odors, the DC3 neurons in D. melanogaster and D. simulans and the DL2d neurons in D. sechellia, connect more frequently with Kenyon cells, giving rise to species-specific biases in connectivity. These species-specific differences in connectivity reflect two distinct neuronal phenotypes: in the number of projection neurons or in the number of presynaptic boutons formed by individual projection neurons. Our study shows how fine-grained aspects of connectivity architecture in a higher brain center can change during evolution to reflect the chemical ecology of a species.

Sensory neuron population expansion enhances odor tracking without sensitizing projection neurons

“…2d) and measured glomerular volumes and the number of postsynaptic puncta in DM2, VM5d and a control glomerulus (DM6). We first confirmed the larger glomerular volume of DM2 and VM5d in D. sechellia [22][23][24][25]35 (Fig. 2e).…”

“…4c). Together with data that the Ir75b glomerulus, DL2d, has the same number of PNs in D. melanogaster, D. simulans and D. sechellia 22,41 Next, we expressed a post-synaptic marker, the GFP-tagged D7 acetylcholine receptor subunit, in PNs 38,42,43 in D. melanogaster and D. sechellia (Fig. 4d).…”

Diversity of visual inputs to Kenyon cells of theDrosophilamushroom body

“…Nearly all uniglomerular olfactory projection neurons target the olfactory calyx with a probability of forming connections onto Kenyon cells that depends on glomerular and Kenyon cell types consistently across individuals within a species 7, 8, 30, 31, 53, 54 . VPNs and LVINs are far more developmentally diverse than are olfactory projection neurons, and the neurons we identify projecting to the left vACA in FlyWire are only a tiny fraction of all VPNs (49 out of 3933 total left VPNs, ∼1.2%).…”

The neurodevelopmental genesalan shepardandNeurogliancontribute to female mate preference in AfricanDrosophila melanogaster

“…It is possible that differences in Nrg across populations could result in differences in the mushroom body, either at the gross anatomical level, or at the circuit level and how it receives input from olfactory receptors (Akalal et al 2006). In closely related species of Drosophila differences in olfactory preference can be explained by the connections made between olfactory receptors and the mushroom body (Ellis et al 2023). shep is an RNA/DNA binding gene that regulates alternative splicing (Chen et al 2018; Olesnicky et al 2018).…”