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In this innovative celebration of diversity and affirmation of individuality in animals and humans, Joan Roughgarden challenges accepted wisdom about gender identity and sexual orientation. A distinguished evolutionary biologist, Roughgarden takes on the medical establishment, the Bible, social science—and even Darwin himself. She leads the reader through a fascinating discussion of diversity in gender and sexuality among fish, reptiles, amphibians, birds, and mammals, including primates. Evolution's Rainbow explains how this diversity develops from the action of genes and hormones and how people come to differ from each other in all aspects of body and behavior. Roughgarden reconstructs primary science in light of feminist, gay, and transgender criticism and redefines our understanding of sex, gender, and sexuality. Witty, playful, and daring, this book will revolutionize our understanding of sexuality. Roughgarden argues that principal elements of Darwinian sexual selection theory are false and suggests a new theory that emphasizes social inclusion and control of access to resources and mating opportunity. She disputes a range of scientific and medical concepts, including Wilson's genetic determinism of behavior, evolutionary psychology, the existence of a gay gene, the role of parenting in determining gender identity, and Dawkins's \"selfish gene\" as the driver of natural selection. She dares social science to respect the agency and rationality of diverse people; shows that many cultures across the world and throughout history accommodate people we label today as lesbian, gay, and transgendered; and calls on the Christian religion to acknowledge the Bible's many passages endorsing diversity in gender and sexuality. Evolution's Rainbow concludes with bold recommendations for improving education in biology, psychology, and medicine; for democratizing genetic engineering and medical practice; and for building a public monument to affirm diversity as one of our nation's defining principles.

Mating drive is balanced by a need to safeguard resources for offspring, yet the neural basis for negative regulation of mating remains poorly understood. In rodents, pheromones critically regulate sexual behavior. Here, we observe suppression of adult female sexual behavior in mice by exocrine gland-secreting peptide 22 (ESP22), a lacrimal protein from juvenile mice. ESP22 activates a dedicated vomeronasal receptor, V2Rp4, and V2Rp4 knockout eliminates ESP22 effects on sexual behavior. Genetic tracing of ESP22-responsive neural circuits reveals a critical limbic system connection that inhibits reproductive behavior. Furthermore, V2Rp4 counteracts a highly related vomeronasal receptor, V2Rp5, that detects the male sex pheromone ESP1. Interestingly, V2Rp4 and V2Rp5 are encoded by adjacent genes, yet couple to distinct circuits and mediate opposing effects on female sexual behavior. Collectively, our study reveals molecular and neural mechanisms underlying pheromone-mediated sexual rejection, and more generally, how inputs are routed through olfactory circuits to evoke specific behaviors. Sex pheromones that increase mating have been reported across a number of different species, yet there is little known about pheromones that suppress female mating drive. This study reports that juvenile female mice release a pheromone, ESP22, which suppresses sexual receptivity of adult female mice by evoking a robust rejection behavior upon male mounting.

If food be the food of love... Courtship is a costly business in terms of both time and energy, so animals must make sure that they've found a willing partner before making the effort — a job often done through pheromone communication. Now Richard Benton and colleagues have discovered that fruitfly males also need the proximity of good food before they commit to a courtship routine. They identify a member of a recently described chemosensory ion-channel family — Ionotropic receptor 84a — as key to sensing fruit-derived aromatics and gating pheromone-sensing neuronal pathways that control courtship routines. Such cross-talk between olfactory and pheromonal circuits constitutes a previously unrecognized evolutionary mechanism coupling reproductive behaviour to good feeding and oviposition sites. Many animals attract mating partners through the release of volatile sex pheromones, which can convey information on the species, gender and receptivity of the sender to induce innate courtship and mating behaviours by the receiver 1 . Male Drosophila melanogaster fruitflies display stereotyped reproductive behaviours towards females, and these behaviours are controlled by the neural circuitry expressing male-specific isoforms of the transcription factor Fruitless (FRU M ) 2 , 3 , 4 , 5 . However, the volatile pheromone ligands, receptors and olfactory sensory neurons (OSNs) that promote male courtship have not been identified in this important model organism. Here we describe a novel courtship function of Ionotropic receptor 84a (IR84a), which is a member of the chemosensory ionotropic glutamate receptor family 6 , in a previously uncharacterized population of FRU M -positive OSNs. IR84a-expressing neurons are activated not by fly-derived chemicals but by the aromatic odours phenylacetic acid and phenylacetaldehyde, which are widely found in fruit and other plant tissues 7 that serve as food sources and oviposition sites for drosophilid flies 8 . Mutation of Ir84a abolishes both odour-evoked and spontaneous electrophysiological activity in these neurons and markedly reduces male courtship behaviour. Conversely, male courtship is increased—in an IR84a-dependent manner—in the presence of phenylacetic acid but not in the presence of another fruit odour that does not activate IR84a. Interneurons downstream of IR84a-expressing OSNs innervate a pheromone-processing centre in the brain. Whereas IR84a orthologues and phenylacetic-acid-responsive neurons are present in diverse drosophilid species, IR84a is absent from insects that rely on long-range sex pheromones. Our results suggest a model in which IR84a couples food presence to the activation of the fru M courtship circuitry in fruitflies. These findings reveal an unusual but effective evolutionary solution to coordinate feeding and oviposition site selection with reproductive behaviours through a specific sensory pathway.

Puberty is a crucial phase for the development of female sexual behavior. Growing evidence suggests that stress during this period may interfere with the development of sexual behavior. However, the neural circuits involved in this alteration remain elusive. Here, we demonstrated in mice that pubertal stress permanently disrupted sexual performance without affecting sexual preference. This was associated with a reduced expression and activation of neuronal nitric oxide synthase (nNOS) in the ventrolateral part of the ventromedial hypothalamus (VMHvl). Fiber photometry revealed that VMHvl nNOS neurons are strongly responsive to male olfactory cues with this activation being substantially reduced in pubertally stressed females. Finally, treatment with a NO donor partially restored sexual performance in pubertally stressed females. This study provides insights into the involvement of VMHvl nNOS in the processing of olfactory cues important for the expression of female sexual behavior. In addition, exposure to stress during puberty disrupts the integration of male olfactory cues leading to reduced sexual behavior. Evidence suggests that stress during development might lead to sexual dysfunction. Here, authors show that pubertal stress disrupted female sexual behavior by reducing activation of nitric oxide synthase-expressing neurons in response to male cues.

Scent's different directions Despite dramatic behavioural differences between the sexes, surprisingly few anatomic features have been observed that differentiate the male and female brain in any species. Work in the Drosophila fruit fly has now uncovered a striking difference in male and female responses to the insect pheromone cVA ( cis -vaccenyl acetate). Males release the pheromone, which is detected by both sexes via apparently identical neural circuits in their antennae. The scent induces females to become receptive to males, but in rival males it inhibits courtship behaviour. The single neuron tracing technique developed to make this discovery should be applicable to study the nervous systems of other genetically tractable species, such as the mouse. Despite marked behavioural differences between the sexes, surprisingly few anatomic features have been observed that differentiate the male and female brain in any species. But this study unveils a sexual dimorphism in the neuronal circuit responding to a pheromone, which induces different courtship behaviours in male and female fruitflies. The single neuron tracing technique that has been developed to do so should be useful to study the nervous systems of other genetically tractable species. Courtship is an innate sexually dimorphic behaviour that can be observed in naive animals without previous learning or experience, suggesting that the neural circuits that mediate this behaviour are developmentally programmed 1 . In Drosophila , courtship involves a complex yet stereotyped array of dimorphic behaviours that are regulated by Fru M , a male-specific isoform of the fruitless gene 2 , 3 , 4 , 5 . Fru M is expressed in about 2,000 neurons in the fly brain, including three subpopulations of olfactory sensory neurons and projection neurons (PNs). One set of Fru + olfactory neurons expresses the odorant receptor Or67d and responds to the male-specific pheromone cis -vaccenyl acetate (cVA) 6 , 7 , 8 , 9 , 10 . These neurons converge on the DA1 glomerulus in the antennal lobe. In males, activation of Or67d + neurons by cVA inhibits courtship of other males, whereas in females their activation promotes receptivity to other males 7 . These observations pose the question of how a single pheromone acting through the same set of sensory neurons can elicit different behaviours in male and female flies. Anatomical or functional dimorphisms in this neural circuit might be responsible for the dimorphic behaviour. We therefore developed a neural tracing procedure that employs two-photon laser scanning microscopy to activate the photoactivatable green fluorescent protein 11 . Here we show, using this technique, that the projections from the DA1 glomerulus to the protocerebrum are sexually dimorphic. We observe a male-specific axonal arbor in the lateral horn whose elaboration requires the expression of the transcription factor Fru M in DA1 projection neurons and other Fru + cells. The observation that cVA activates a sexually dimorphic circuit in the protocerebrum suggests a mechanism by which a single pheromone can elicit different behaviours in males and in females.

In mammals, especially rodents, social behaviours, such as parenting, territoriality or mate attraction, are largely based on olfactory communication through chemosignals. These behaviours are mediated by species-specific chemosignals, including small organic molecules and proteins that are secreted in the urine or in various fluids from exocrine glands. Chemosignal detection is mainly ensured by olfactory neurons in two specific sensory organs, the vomeronasal organ (VNO) and the main olfactory epithelium (MOE). This study aimed to characterise the olfactory communication in the fossorial ecotype of the water voles, Arvicola terrestris. We first measured the olfactory investigation of urine and lateral scent gland secretions from conspecifics. Our results showed that water voles can discriminate the sex of conspecifics based on the smell of urine, and that urinary male odour is attractive for female voles. Then, we demonstrated the ability of the VNO and MOE to detect volatile organic compounds (VOCs) found in water vole secretions using live-cell calcium imaging in dissociated cells. Finally, we evaluated the attractiveness of two mixtures of VOCs from urine or lateral scent glands in the field during a cyclical outbreak of vole populations.

Sexual behavior requires animals to distinguish between the sexes and to respond appropriately to each of them. In Drosophila melanogaster, as in many insects, cuticular hydrocarbons are thought to be involved in sex recognition and in mating behavior, but there is no direct neuronal evidence of their pheromonal effect. Using behavioral and electrophysiological measures of responses to natural and synthetic compounds, we show that Z-7-tricosene, a Drosophila male cuticular hydrocarbon, acts as a sex pheromone and inhibits male-male courtship. These data provide the first direct demonstration that an insect cuticular hydrocarbon is detected as a sex pheromone. Intriguingly, we show that a particular type of gustatory neurons of the labial palps respond both to Z-7-tricosene and to bitter stimuli. Cross-adaptation between Z-7-tricosene and bitter stimuli further indicates that these two very different substances are processed by the same neural pathways. Furthermore, the two substances induced similar behavioral responses both in courtship and feeding tests. We conclude that the inhibitory pheromone tastes bitter to the fly.

We show that reproductively mature male sea lampreys release a bile acid that acts as a potent sex pheromone, inducing preference and searching behavior in ovulated female lampreys. The secreted bile acid 7α,12α,24-trihydroxy-5α-cholan-3-one 24-sulfate was released in much higher amounts relative to known vertebrate steroid pheromones and may be secreted through the gills. Hence, the male of this fish species signals both its reproductive status and location to females by secreting a pheromone that can act over long distances.

Neuronal nitric oxide synthase (nNOS) neurons are ubiquitously spread in the mouse brain. Data using knockouts and pharmacology have revealed that nNOS is essential for the display of sexual and aggressive behavior. Yet, the specific neuronal populations regulating those behaviors remain elusive. Here, we aim to study the role of the ventromedial hypothalamus (VMHvl)-nNOS neurons in social behaviors in both sexes. First, we evaluate whether the expression of nNOS overlaps with the well characterized estrogen receptor alpha (ERα + )-VMHvl population. Next, we assess how different social stimuli affected VMHvl-nNOS neurons’ activity. Lastly, we use transgenic mice and viral approaches to ablate VMHvl-nNOS neurons and evaluate their impact on behavior. Our findings suggest that nNOS neurons constitute a small cluster within the VMHvl-ERα+ population that regulates social behaviors in a sex-specific manner. In males, those neurons seem to be essential for aggression, whereas in females for sexual behavior and social motivation. In the mouse, hypothalamic nNOS neurons modulate social behaviors in a sex-specific manner. In females, those neurons are involved in mating and social motivation, whereas in males, they regulate sexual and aggressive behavior.

Sexual reproduction can lead to major conflicts between sexes and within genomes1, 2, 3, 4. Here we report an extreme case of such conflicts in the little fire ant Wasmannia auropunctata. We found that sterile workers are produced by normal sexual reproduction, whereas daughter queens are invariably clonally produced. Because males usually develop from unfertilized maternal eggs in ants and other haplodiploid species, they normally achieve direct fitness only through diploid female offspring. Hence, although the clonal production of queens increases the queen's relatedness to reproductive daughters, it potentially reduces male reproductive success to zero. In an apparent response to this conflict between sexes, genetic analyses reveal that males reproduce clonally, most likely by eliminating the maternal half of the genome in diploid eggs. As a result, all sons have nuclear genomes identical to those of their father. The obligate clonal production of males and queens from individuals of the same sex effectively results in a complete separation of the male and female gene pools. These findings show that the haplodiploid sex-determination system provides grounds for the evolution of extraordinary genetic systems and new types of sexual conflict