Female-biased dimorphism underlies a female-specific role for post-embryonic Ilp7 neurons inDrosophilafertility

Abstract

SUMMARYIn Drosophila melanogaster, much of our understanding of sexually dimorphic neuronal development and function comes from the study of male behavior, leaving female behavior less well understood. Here, we identify a post-embryonic population of Insulin-like peptide 7 (Ilp7)-expressing neurons in the posterior ventral nerve cord that innervate the reproductive tracts and exhibit a female bias in their function. They form two distinct dorsal and ventral subsets in females, but only a single dorsal subset in males, signifying a rare example of a female-specific neuronal subset. Female post-embryonic Ilp7 neurons are glutamatergic motoneurons innervating the oviduct and are required for female fertility. In males, they are serotonergic/glutamatergic neuromodulatory neurons innervating the seminal vesicle but are not required for male fertility. In both sexes, these neurons express the sex-differentially spliced fruitless-P1 transcript but not doublesex. The male fruitless-P1 isoform (fruM) was necessary and sufficient for serotonin expression in the shared dorsal Ilp7 subset, but although it was necessary for eliminating female-specific Ilp7 neurons in males, it was not sufficient for their elimination in females. By contrast, sex-specific RNA-splicing by female-specific transformer is necessary for female-type Ilp7 neurons in females and is sufficient for their induction in males. Thus, the emergence of female-biased post-embryonic Ilp7 neurons is mediated in a subset-specific manner by a tra-and fru-dependent mechanism in the shared dorsal subset, and a tra-dependent, fru-independent mechanism in the female-specific subset. These studies provide an important counterpoint to studies of the development and function of male-biased neuronal dimorphism in Drosophila.

Mechanosensitive Neurons on the Internal Reproductive Tract Contribute to Egg-Laying-Induced Acetic Acid Attraction in Drosophila

“…It has been shown recently, and we confirmed, that some of the ILP7-Gal4 -expressing neurons in the ventral nerve cord (VNC) are motor neurons that innervate the tract (Fig. 2B) (Castellanos et al, 2013). Importantly, inhibiting ILP7 neurons with Kir2.1 (Baines et al, 2001) consistently causes one or more eggs to be “jammed” in the tract (Castellanos et al, 2013; Yang et al, 2008) (Fig.…”

“…2A). The reproductive tract has a small diameter and is encased by muscles that are innervated by sensory and motor neurons (Castellanos et al, 2013; Häsemeyer et al, 2009; Yang et al, 2009). Because egg-delivery in the tract precedes physical egg deposition, we hypothesize that perhaps females start to increase AA attraction once they sense eggs are being pushed through the tract.…”

“…2B) (Castellanos et al, 2013). Importantly, inhibiting ILP7 neurons with Kir2.1 (Baines et al, 2001) consistently causes one or more eggs to be “jammed” in the tract (Castellanos et al, 2013; Yang et al, 2008) (Fig. 2C), providing us with the desired phenotype to test our hypothesis.…”

Discovery of a novel insulin-like peptide and insulin binding proteins in the Eastern rock lobster Sagmariasus verreauxi

“…The timing of this activation might explain the absence of Sv-ILP1 expression in the pre-metamorphic (puerulus) stage, with its emergence in the juvenile. By adulthood, DILP7 in larval D. melanogaster shows spatial expression similar to that seen in S. verreauxi and is found in the brain and nerve swellings along the abdomen, with extensions innervating the intestine, rectum (Miguel-Aliaga et al, 2008) and the reproductive tract (Yang et al, 2008) where additional neurons have been identified in females (Castellanos et al, 2013). In Anopheles sp., ILP5 was found in both sexes, weakly expressed in the head and thorax but abundant in abdomen (Krieger et al, 2004).…”

“…It has been suggested that DILP7 may act as an invertebrate relaxin, stimulating the relaxation/contraction of the ovipositor during egg-laying (Yang et al, 2008). However, more recently, the co-expressing neurotransmitter glutamate was attributed with this function (Castellanos et al, 2013). When one considers the lack of phenotypic disruption seen in DILP7 mutants (Grönke et al, 2010) and the apparent evolutionary age of the ILP7 family, it could be suggested that the ILP7s are an evolutionary relic.…”