Sexual dimorphism in olfactory signaling

doi:10.1016/j.conb.2010.08.015

Current Opinion in Neurobiology

Volume 20, Issue 6, December 2010, Pages 770-775

https://doi.org/10.1016/j.conb.2010.08.015 Get rights and content

What makes males and females behave differently? Although genetic master-regulators commonly underlie physical differences, sexually dimorphic behavior is additionally influenced by sensory input such as olfactory cues. Olfaction requires both ligands for signaling and sensory neural circuits for detection. Specialized subsets of each interact to generate gender-dimorphic behavior. It has long been accepted that males and females emit sex-specific odor compounds that function as pheromones to promote stereotypic behavior. Significant advances have now been made in purifying and isolating several of these sex-specific olfactory ligands. In contrast, the neural mechanisms that enable a gender-dimorphic response to these odors remain largely unknown. However, first progress has been made in identifying components of sexually dimorphic olfactory circuits in both Drosophila and the mouse.

Introduction

Males and females display well-characterized behaviors specific to each gender such as territorial aggression, parental care, and mating. While genetic factors have been shown to underlie sex-specific anatomy and physiology less is known about neural mechanisms that control behavioral dimorphisms. Sex-specific behavior is primarily released in response to specific sensory information. Such stimuli include coloration, courtship songs, and chemosensory cues, such as pheromones [1]. While the neural mechanisms that underlie gender-dimorphic behavior in humans are largely unknown, Box 1, in many species, including the fly and the mouse, olfactory sensation is necessary to display appropriate sex-specific behavior. Loss of olfactory sensory transduction impairs, ablates, or transforms the appropriate display of gender-specific behavior [2, 3••, 4, 5, 6, 7•, 8•]. How olfaction regulates specific behaviors is mostly unknown. In the mouse, each olfactory neuron expresses one of approximately 1300 G-protein-coupled receptors (GPCRs) which can be located in one of several anatomically distinct subsystems [9, 10, 11]. Furthermore, much of the olfactory system appears to function similarly in both males and females, such as the sensory response initiated by food odors. Amid such complexity, to molecularly identify and study the specific olfactory sensory neurons and circuits that underlie gender-dimorphic behavior has been a daunting task. However, recent advances in the purification of signaling ligands, primarily emitted from either males or females, have now led to the identification of their cognate subsets of sensory neurons and enabled the study of the neural mechanisms initiate sex-specific behavior.

Section snippets

Sexually dimorphic olfactory ligands

A number of species produce a range of gender-specific chemicals which are transmitted to others by secretion in exocrine fluids such as urine, saliva, tears, or sweat. In the mouse, three distinct families of sex-specific ligands have primarily been identified by comparing the bioactivity and odor constituents of male and female secretions. The vomeronasal organ (VNO) is a specialized olfactory subsystem that has been well characterized to detect these ligands [12, 13, 14•]. A variety of

Sexually dimorphic olfactory circuits

What are the neural mechanisms that enable males and females to behave differently in the presence of the same olfactory ligand? One model predicts that the sensory neurons of males and females differentially respond to the same cue. In the mouse, intense investigation has revealed VNO sensory neurons that are tuned to either male or female cues [12, 13, 14•, 27]. VNO neurons of mice are thought to detect individual odor ligands by specifically expressing one variant of >350 GPCRs [9, 10, 11].

Drosophila: from odor ligands to sex-specific behavior

Significant advances have been made towards the anatomic and genetic characterization of a sexually dimorphic olfactory circuit in Drosophila. Like mammals, fruit-flies transmit social information via pheromones. One such chemical specifically expressed on the cuticle of male fruit-flies, 11-cis-vaccenyl acetate (cVA), is known to evoke different behaviors when detected by either sex. In males it suppresses courtship behavior at high concentrations and initiates male–male aggression at lower

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

• of special interest
•• of outstanding interest

Acknowledgements

We would like to thank T. Kimchi, T. Holy, and S. Dey, for helpful comments on the text. L.S. is supported by grants from the NIH-NIDCD and the Skaggs Foundation; D.W.L. is the recipient of a Wellcome Trust Career Development Fellowship.

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Sexual dimorphism in olfactory signaling

Introduction

Section snippets

Sexually dimorphic olfactory ligands

Sexually dimorphic olfactory circuits

Drosophila: from odor ligands to sex-specific behavior

References and recommended reading

Acknowledgements

Science

BMC Biol

Cell

Epigenetics

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Science

Neuron

Cell

Nat Neurosci

Horm Behav

Behav Neurosci

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Hum Brain Mapp

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Reproductive skew and selection on female ornamentation in social species

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Loss of sex discrimination and male-male aggression in mice deficient for TRP2

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A functional circuit underlying male sexual behaviour in the female mouse brain

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Altered sexual and social behaviors in trp2 mutant mice

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Deficits in sexual and aggressive behaviors in Cnga2 mutant mice

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Pheromone detection in male mice depends on signaling through the type 3 adenylyl cyclase in the main olfactory epithelium

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Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila

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A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone

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V2R gene families degenerated in primates, dog and cow, but expanded in opossum

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Comparative genomic analysis identifies an evolutionary shift of vomeronasal receptor gene repertoires in the vertebrate transition from water to land

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