The sex of specific neurons controls female body growth in Drosophila.

Sexual dimorphisms in body size are widespread throughout the animal kingdom but their underlying mechanisms are not well characterized. Most models for how sex chromosome genes specify size dimorphism have emphasized the importance of gonadal hormones and cell-autonomous influences in mammals versu...

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Main Authors: Annick Sawala, Alex P Gould
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-10-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.2002252
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spelling doaj-abc08630b5fc476bbd95ed5f5124c0942021-07-02T16:27:06ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852017-10-011510e200225210.1371/journal.pbio.2002252The sex of specific neurons controls female body growth in Drosophila.Annick SawalaAlex P GouldSexual dimorphisms in body size are widespread throughout the animal kingdom but their underlying mechanisms are not well characterized. Most models for how sex chromosome genes specify size dimorphism have emphasized the importance of gonadal hormones and cell-autonomous influences in mammals versus strictly cell-autonomous mechanisms in Drosophila melanogaster. Here, we use tissue-specific genetics to investigate how sexual size dimorphism (SSD) is established in Drosophila. We find that the larger body size characteristic of Drosophila females is established very early in larval development via an increase in the growth rate per unit of body mass. We demonstrate that the female sex determination gene, Sex-lethal (Sxl), functions in central nervous system (CNS) neurons as part of a relay that specifies the early sex-specific growth trajectories of larval but not imaginal tissues. Neuronal Sxl acts additively in 2 neuronal subpopulations, one of which corresponds to 7 median neurosecretory cells: the insulin-producing cells (IPCs). Surprisingly, however, male-female differences in the production of insulin-like peptides (Ilps) from the IPCs do not appear to be involved in establishing SSD in early larvae, although they may play a later role. These findings support a relay model in which Sxl in neurons and Sxl in local tissues act together to specify the female-specific growth of the larval body. They also reveal that, even though the sex determination pathways in Drosophila and mammals are different, they both modulate body growth via a combination of tissue-autonomous and nonautonomous inputs.https://doi.org/10.1371/journal.pbio.2002252
collection DOAJ
language English
format Article
sources DOAJ
author Annick Sawala
Alex P Gould
spellingShingle Annick Sawala
Alex P Gould
The sex of specific neurons controls female body growth in Drosophila.
PLoS Biology
author_facet Annick Sawala
Alex P Gould
author_sort Annick Sawala
title The sex of specific neurons controls female body growth in Drosophila.
title_short The sex of specific neurons controls female body growth in Drosophila.
title_full The sex of specific neurons controls female body growth in Drosophila.
title_fullStr The sex of specific neurons controls female body growth in Drosophila.
title_full_unstemmed The sex of specific neurons controls female body growth in Drosophila.
title_sort sex of specific neurons controls female body growth in drosophila.
publisher Public Library of Science (PLoS)
series PLoS Biology
issn 1544-9173
1545-7885
publishDate 2017-10-01
description Sexual dimorphisms in body size are widespread throughout the animal kingdom but their underlying mechanisms are not well characterized. Most models for how sex chromosome genes specify size dimorphism have emphasized the importance of gonadal hormones and cell-autonomous influences in mammals versus strictly cell-autonomous mechanisms in Drosophila melanogaster. Here, we use tissue-specific genetics to investigate how sexual size dimorphism (SSD) is established in Drosophila. We find that the larger body size characteristic of Drosophila females is established very early in larval development via an increase in the growth rate per unit of body mass. We demonstrate that the female sex determination gene, Sex-lethal (Sxl), functions in central nervous system (CNS) neurons as part of a relay that specifies the early sex-specific growth trajectories of larval but not imaginal tissues. Neuronal Sxl acts additively in 2 neuronal subpopulations, one of which corresponds to 7 median neurosecretory cells: the insulin-producing cells (IPCs). Surprisingly, however, male-female differences in the production of insulin-like peptides (Ilps) from the IPCs do not appear to be involved in establishing SSD in early larvae, although they may play a later role. These findings support a relay model in which Sxl in neurons and Sxl in local tissues act together to specify the female-specific growth of the larval body. They also reveal that, even though the sex determination pathways in Drosophila and mammals are different, they both modulate body growth via a combination of tissue-autonomous and nonautonomous inputs.
url https://doi.org/10.1371/journal.pbio.2002252
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