Summary The evolution of animal behaviour is poorly understood 1 , 2 . Despite numerous correlations of behavioural and nervous system divergence, demonstration of the genetic basis of interspecific behavioural differences remains rare 3 – 5 . Here, we develop a novel neurogenetic model, Drosophila sechellia , a close cousin of D. melanogaster 6 , 7 that displays profound behavioural changes linked to its extreme specialisation on noni fruit 8 – 16 . Using calcium imaging, we identify D. sechellia olfactory pathways detecting host volatiles. Mutational analysis indicates roles for different olfactory receptors in long- and short-range attraction to noni. Cross-species allele transfer demonstrates that tuning of one of these receptors is important for species-specific host-seeking. We identify the molecular determinants of this functional change, and characterise their evolutionary origin and behavioural significance. Through circuit tracing in the D. sechellia brain, we find that receptor adaptations are accompanied by increased sensory pooling onto interneurons and novel central projection patterns. This work reveals the accumulation of molecular, physiological and anatomical traits linked to behavioural divergence, and defines a powerful model for investigating nervous system evolution and speciation.
The Drosophila domino gene encodes protein of the SWI2/SNF2 family that has widespread roles in transcription, replication, recombination and DNA repair. Here, the potential relationship of Domino protein to other chromatin-associated proteins has been investigated through a genetic interaction analysis. We scored for genetic modification of a domino wing margin phenotype through coexpression of RNAi directed against a set of previously characterized and more newly characterized chromatin-encoding loci. A set of other SWI2/SNF2 loci were also assayed for interaction with domino. Our results show that the majority of tested loci exhibit synergistic enhancement or suppression of the domino wing phenotype. Therefore, depression in domino function sensitizes the wing margin to alterations in the activity of numerous chromatin components. In several cases the genetic interactions are associated with changes in the level of cell death measured across the dorsal-ventral margin of the wing imaginal disc. These results highlight the broad realms of action of many chromatin proteins and suggest significant overlap with Domino function in fundamental cell processes, including cell proliferation, cell death and cell signaling.
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.
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