Comparative single-cell transcriptomic atlases reveal conserved and divergent features of drosophilid central brains

Abstract

AbstractTo explore how brains change upon species evolution, we generated single-cell transcriptomic atlases of the central brains of three closely-related but ecologically-distinct drosophilids: the generalistsDrosophila melanogasterandDrosophila simulans, and the noni fruit specialistDrosophila sechellia. The global cellular composition of these species’ central brains is well-conserved, but we predicted a few cell types (perineurial glia, sNPF and Dh44 peptidergic neurons) with divergent frequencies. Gene expression analysis revealed that distinct cell types within the central brain evolve at different rates and patterns; notably, glial cell types exhibit the greatest divergence between species. Compared toD. melanogaster, the cellular composition and gene expression patterns of the central brain inD. sechelliadisplay greater deviation than those ofD. simulans- despite their similar phylogenetic distance fromD. melanogaster- that the distinctive ecological specialization ofD. sechelliais reflected in the structure and function of its brain. Expression changes inD. sechelliaencompass metabolic and ecdysone signaling genes, suggestive of adaptations to its novel ecological demands. Additional single-cell transcriptomic analysis onD. sechelliarevealed genes and cell types responsive to dietary supplement with noni, pointing to glia as sites for both physiological and genetic adaptation to novel conditions. Our atlases represent the first comparative analyses of “whole” central brains, and provide a comprehensive foundation for studying the evolvability of nervous systems in a well-defined phylogenetic and ecological framework.