One template, two outcomes: How does the sex-shared nervous system generate sex-specific behaviors?

Salzberg, Yehuda; Gat, Asaf; Oren‐Suissa, Meital

doi:10.1016/bs.ctdb.2020.08.003

Cited by 5 publications

(7 citation statements)

References 80 publications

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“…To ensure maximal survival success, the neural circuitry of an organism, which encodes and decodes sensory information, has to be adaptive, but it also has to retain its sex-dependent characteristics [15]. Owing to its experimental simplicity, C. elegans has been used to decode circuit dynamics.…”

Section: Caenorhabditis Elegansmentioning

confidence: 99%

“…In C. elegans , when given a choice of two attractants, such as diacetyl or pyrazine, a dimorphic bias is observed: Hermaphrodites choose diacetyl over pyrazine and vice versa in males. Overexpression of specific transcription factors from the sex‐determination pathway can change the sex of a particular tissue in an otherwise hermaphrodite/male animal [15]. When hermaphrodite sensory neurons were transformed to male‐like by over‐expressing FEM‐3, a preference towards pyrazine over diacetyl emerged [18].…”

Section: Sexually Dimorphic Responses To Environmental Stimuli In Cae...mentioning

confidence: 99%

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Environmental experiences shape sexually dimorphic neuronal circuits and behaviour

2023

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Dimorphic traits, shaped by both natural and sexual selection, ensure optimal fitness and survival of the organism. This includes neuronal circuits that are largely affected by different experiences and environmental conditions. Recent evidence suggests that sexual dimorphism of neuronal circuits extends to different levels such as neuronal activity, connectivity and molecular topography that manifest in response to various experiences, including chemical exposures, starvation and stress. In this review, we propose some common principles that govern experience‐dependent sexually dimorphic circuits in both vertebrate and invertebrate organisms. While sexually dimorphic neuronal circuits are predetermined, they have to maintain a certain level of fluidity to be adaptive to different experiences. The first layer of dimorphism is at the level of the neuronal circuit, which appears to be dictated by sex‐biased transcription factors. This could subsequently lead to differences in the second layer of regulation namely connectivity and synaptic properties. The third regulator of experience‐dependent responses is the receptor level, where dimorphic expression patterns determine the primary sensory encoding. We also highlight missing pieces in this field and propose future directions that can shed light onto novel aspects of sexual dimorphism with potential benefits to sex‐specific therapeutic approaches. Thus, sexual identity and experience simultaneously determine behaviours that ultimately result in the maximal survival success.

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Section: Caenorhabditis Elegansmentioning

confidence: 99%

Section: Sexually Dimorphic Responses To Environmental Stimuli In Cae...mentioning

confidence: 99%

Environmental experiences shape sexually dimorphic neuronal circuits and behaviour

2023

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“…To gain insight into the molecular and genetic mechanisms underlying the sexual component of nervous system development, we asked how sexual identity, neuronal identity, and developmental stage intersect to drive gene expression in a model organism. We addressed this question using the nematode Caenorhabditis elegans ( C. elegans ), due to the detailed anatomical and molecular understanding of the nervous system of both sexes and the extensive sexual dimorphism they exhibit 17 , 18 at the resolution of single identifiable neurons, connections, and behaviors 2 , 19 – 21 . As most sexual differences arise late in development, C. elegans offers a unique opportunity to track how sex-specific characteristics emerge during neuronal development.…”

Section: Introductionmentioning

confidence: 99%

Sex-specific developmental gene expression atlas unveils dimorphic gene networks in C. elegans

Haque,

Kurien,

Setty

et al. 2024

Nat Commun

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Sex-specific traits and behaviors emerge during development by the acquisition of unique properties in the nervous system of each sex. However, the genetic events responsible for introducing these sex-specific features remain poorly understood. In this study, we create a comprehensive gene expression atlas of pure populations of hermaphrodites and males of the nematode Caenorhabditis elegans across development. We discover numerous differentially expressed genes, including neuronal gene families like transcription factors, neuropeptides, and G protein-coupled receptors. We identify INS-39, an insulin-like peptide, as a prominent male-biased gene expressed specifically in ciliated sensory neurons. We show that INS-39 serves as an early-stage male marker, facilitating the effective isolation of males in high-throughput experiments. Through complex and sex-specific regulation, ins-39 plays pleiotropic sexually dimorphic roles in various behaviors, while also playing a shared, dimorphic role in early life stress. This study offers a comparative sexual and developmental gene expression database for C. elegans. Furthermore, it highlights conserved genes that may underlie the sexually dimorphic manifestation of different human diseases.

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“…Sexually dimorphic behavior in C. elegans can arise from altered expression of sensory channels 39,68 , variation in synaptic connectivity and strength 38,69 and different gene expression networks 29,70 , some of which may already be active prior to sexual maturation 71 . However, to our knowledge, specific and robust differences in complex dendritic arborization between hermaphrodite and male C. elegans have not been characterized.…”

Section: Introductionmentioning

confidence: 99%

The PVD neuron has male-specific structure and mating function inC. elegans

Iosilevskii,

Hall,

Katz

et al. 2024

Preprint

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Neurons display unique shapes and establish intricate networks, which may differ between sexes. In complex organisms, studying sex differences in structure and function of individual neurons is difficult. The nematode Caenorhabditis elegans hermaphrodites and males present an exceptional model for studying neuronal morphogenesis in a simple, sexually-dimorphic system. We focus on the polymodal sensory bilateral neuron pair PVD, which forms a complex but stereotypic dendritic tree composed of multiple subunits that resemble candelabra. PVD was previously studied in hermaphrodites, but not in males. We find here that during larval development, male PVDs extend a similar architecture to the hermaphrodite utilizing a sexually-shared patterning mechanism. In early adulthood, however, male PVD develops a unique extension into the copulatory tail structure. This sexually-dimorphic arborization is absent in mutant backgrounds which perturb the sex-shared PVD guidance complex. SAX-7/L1CAM, a hypodermal component of this complex, shows a male-specific expression pattern which precedes PVD extension. Further, our results reveal that genetically altered arborization or ablation of the PVD result in male mating behavioral defects, particularly as males turn around the hermaphrodite. These results uncover an adult-stage sexual dimorphism of dendritic branching and uncover a new function for PVD in male sexual behavior.

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One template, two outcomes: How does the sex-shared nervous system generate sex-specific behaviors?

Cited by 5 publications

References 80 publications

Environmental experiences shape sexually dimorphic neuronal circuits and behaviour

Environmental experiences shape sexually dimorphic neuronal circuits and behaviour

Sex-specific developmental gene expression atlas unveils dimorphic gene networks in C. elegans

The PVD neuron has male-specific structure and mating function inC. elegans

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