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Changes in the cellular makeup of motor patterning circuits drive courtship song evolution in Drosophila

ABSTRACT: How evolutionary changes in genes and neurons encode species variation in complex motor behaviors are largely unknown. Here, we develop genetic tools that permit a neural circuit comparison between the model speciesDrosophila melanogasterand the closely-related speciesD. yakuba, who has undergone a lineage-specific loss of sine song, one of the two major types of male courtship song inDrosophila. Neuroanatomical comparison of song patterning neurons called TN1 across the phylogeny demonstrates a link between the loss of sine song and a reduction both in the number of TN1 neurons and the neurites serving the sine circuit connectivity. Optogenetic activation confirms that TN1 neurons inD. yakubahave lost the ability to drive sine song, while maintaining the ability to drive the singing wing posture. Single-cell transcriptomic comparison shows thatD. yakubaspecifically lacks a cell type corresponding to TN1A neurons, the TN1 subtype that is essential for sine song. Genetic and developmental manipulation reveals a functional divergence of the sex determination genedoublesexinD. yakubato reduce TN1 number by promoting apoptosis. Our work illustrates the contribution of motor patterning circuits and cell type changes in behavioral evolution, and uncovers the evolutionary lability of sex determination genes to reconfigure the cellular makeup of neural circuits.

ORGANISM(S): Drosophila yakuba Drosophila melanogaster

PROVIDER: GSE262732 | GEO | 2024/04/03

REPOSITORIES: GEO

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Project description:Like human speech, birdsong is a complex vocal behavior that is acquired by sensorimotor learning based on coordination of auditory input and vocal output to mimic memorized tutor song. Here we investigate neural circuits for vocal learning and production in deafened songbirds to elucidate how sensory-input regulate genetic and epigenetic property of vocal development and its associated gene expression dynamics. Compared with audition-intact birds, in deafened zebra finches, the vocal development is delayed but song crystallization is observed at more than three times later, producing individually different but structured vocal patterns. In contrast to the distinct difference of vocal ontogeny between audition (+) and (-), unexpectedly, developmental regulation of gene expression dynamics is strictly conserved with age-locked trend in vocal motor circuit in both intact and deafened birds, indicating sensory-input independent robustness of developmental gene expression dynamics in the motor circuit for sensorimotor learning. This discrepancy between outward vocal phenotype and inward gene expression dynamics provides new insight into neural regulation at closing of the critical period for vocal learning by two different forms: auditory inputs-dependent M-bM-^@M-^XactiveM-bM-^@M-^Y crystallization and gene expression dynamics-mediated M-bM-^@M-^XpassiveM-bM-^@M-^Y crystallization. We collected brain samples from intact and early-deafened birds (deafened at day-post hatch 17-23) under silent and dark condition. Song nuclei in vocal motor circuit, HVC and RA tissue samples (juvenile; n = 3, young; n = 3, old; n = 3 of intact and early-deafened birds for HVC and RA) were laser-microdissected from total 24 birds (intact; n = 12, early-deafened; n = 12). Each sample was hybridized to a single array, totaling 36 arrays. Birds were selected per slide such that early-deafened birds were paired with intact birds. To minimize possible interslide bias or batch effects, intact and early-deafened bird samples matching with brain area and age conditions were hybridized side by side on same array glass.

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Changes in the cellular makeup of motor patterning circuits drive courtship song evolution in Drosophila

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