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

How evolutionary changes in genes and neurons encode species variation in complex motor behaviors is largely unknown. Here, we develop genetic tools that permit a neural circuit comparison between the model species Drosophila melanogaster and the closely related species D. yakuba, which has undergon...

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Bibliographic Details
Published in:Current biology Vol. 34; no. 11; p. 2319
Main Authors: Ye, Dajia, Walsh, Justin T, Junker, Ian P, Ding, Yun
Format: Journal Article
Language:English
Published: England 03.06.2024
Subjects:
Animal Communication
Animals
Drosophila - classification
Drosophila - cytology
Drosophila - physiology
Drosophila Proteins - genetics
Drosophila Proteins - metabolism
Efferent Pathways - cytology
Neurons - cytology
Sexual Behavior, Animal - physiology
Single-Cell Gene Expression Analysis
Drosophila
TN1
doublesex
neural circuits
apoptosis
single-cell transcriptome
courtship song
behavioral evolution
ISSN:1879-0445, 1879-0445
Online Access:Get more information
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Summary:How evolutionary changes in genes and neurons encode species variation in complex motor behaviors is largely unknown. Here, we develop genetic tools that permit a neural circuit comparison between the model species Drosophila melanogaster and the closely related species D. yakuba, which has undergone a lineage-specific loss of sine song, one of the two major types of male courtship song in Drosophila. 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 supporting the sine circuit connectivity. Optogenetic activation confirms that TN1 neurons in D. yakuba have lost the ability to drive sine song, although they have maintained the ability to drive the singing wing posture. Single-cell transcriptomic comparison shows that D. yakuba specifically 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 gene doublesex in D. yakuba to 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.
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ISSN:1879-0445
1879-0445
DOI:10.1016/j.cub.2024.04.020