Chemical olfactory signals and parenthood in mammals

This article is part of a Special Issue “Chemosignals and Reproduction”.In mammalian species, odor cues emitted by the newborn are essential to establish maternal behavior at parturition and coordinate early mother–infant interactions. Offspring odors become potent attractive stimuli at parturition promoting the contact with the young to ensure that normal maternal care develops. In some species odors provide a basis for individual recognition of the offspring and highly specialized neural mechanisms for learning the infant signals have evolved. Both the main and the accessory olfactory systems are involved in the onset of maternal care, but only the former contributes to individual odor discrimination of the young. Electrophysiological and neurochemical changes occur in the main olfactory bulb leading to a coding of the olfactory signature of the familiar young. Olfactory neurogenesis could also contribute to motherhood and associated learning. Parturition and interactions with the young influence neurogenesis and some evidence indicates a functional link between olfactory neurogenesis and maternal behavior. Although a simple compound has been found which regulates anogenital licking in the rat, studies identifying the chemical nature of these odors are lacking. Neonatal body odors seem to be particularly salient to human mothers who are able to identify their infant's odors. Recent studies have revealed some neural processing of these cues confirming the importance of mother–young chemical communication in our own species.     

鳄蜥对熟悉和陌生个体气味的辨别

个体辨别对于减少同种争斗以及配偶选择具有重要意义。我们用棉棒粘取鳄蜥(Shinisaurus crocodilurus)尿液作为气味源,以香水作为对照,测定鳄蜥对熟悉个体气味、陌生个体气味以及香水的舔舌次数和舔舌潜伏期,来探讨鳄蜥通过化学信息辨别熟悉和陌生个体的能力。结果显示,不论是雌性还是雄性,对不同个体尿液的舔舌次数均显著高于对香水的,舔舌潜伏期显著短于香水的;尽管雄性对陌生同性个体气味与熟悉同性个体气味的舔舌次数无显著差异,但对前者的舔舌潜伏期显著短于后者;雄性对陌生雌性气味的舔舌次数显著多于熟悉雌性气味的,对前者的舔舌潜伏期显著短于后者;雌性对陌生雄性气味的舔舌潜伏期显著短于对熟悉雄性气味的;雄鳄蜥对陌生雌性气味的舔舌次数显著多于雌鳄蜥对陌生雄性的。结果表明,鳄蜥能辨别同种个体的化学信息,并能通过化学信息来辨别熟悉和陌生个体,推测鳄蜥的这种辨别能力对其领域分配以及繁殖交配有重要作用。     

In Ovo Olfactory Experience Influences Post‐hatch Feeding Behaviour in Young Chickens

In several mammalian species, prenatal exposure to odours can elicit later positive consummatory behaviour in response to substrates bearing that odorant. In birds, the sense of smell has been considerably underestimated, and very little is known about the effects of early sensory experience on the regulation of feeding behaviour. We tested the hypothesis that the feeding behaviour of the domestic chicken could be regulated by olfactory learning during the embryonic life. To that end, chicken embryos were exposed to an olfactory stimulus (blend of essential oil of orange and nature identical vanillin) from embryonic day (ED) 12 to ED20, and chicks were tested between 4 and 9 d of age. In short‐term choice tests, at day 4 and 5, chickens previously exposed to a low concentration (LC) of the olfactory stimulus spent a higher proportion of time eating a familiar or an unfamiliar food bearing the olfactory stimulus compared to non‐exposed control chickens. Conversely, chickens previously exposed to a high concentration (HC) of the olfactory stimulus were found to avoid all foods bearing the olfactory stimulus. On a 24‐ h time scale at day 7–8, LC and HC birds, but not controls, ingest significantly less familiar food containing the olfactory stimulus. This result indicated a long‐term effect of the early olfactory experience on feeding preferences. We demonstrated that chickens can utilize information from their pre‐hatch chemosensory environment to guide their later feeding behaviour. A pre‐hatch effect of the intensity of odour signals in the regulation of feeding behaviour is reported here for the first time.     

Olfactory Predator Discrimination in Yellow‐Bellied Marmots

The mechanism underlying olfactory predator identification may be relatively experience‐independent, or it may rely on specific experience with predators. A mechanism by which prey might identify novel predators relies on the inevitable creation of sulfurous metabolites that are then excreted in the urine of carnivorous mammals. We tested whether free‐living, yellow‐bellied marmots (Marmota flaviventris) and mid‐sized herbivores that fall prey to a variety of carnivorous mammals could discriminate herbivore (elk—Cervus elephas) urine from predator (red fox—Vulpes vulpes, coyote—Canis latrans, mountain lion—Felis concolor, wolf—Canis lupus) urine, a novel herbivore (moose—Alces alces), and a distilled water control. We further asked how specific this assessment was by testing whether marmots responded differently to predators representing different levels of risk and to familiar vs. unfamiliar predators. We found that marmots responded more to urine from coyotes (a familiar predator on adults), mountain lions (a potentially unfamiliar predator that could kill adults) and wolves (a locally extinct predator that could kill adults) than to elk urine (a non‐predator). Red fox (a predator that poses a risk only to recently emerged marmot pups) urine elicited a less substantial (but not significantly so) response than coyote urine. Marmots can identify predators, even novel ones, using olfactory cues, suggesting that experience with a specific predator is not required to identify potential threats.     

Behavioural development of conspecific odour preferences in bank voles,Clethrionomys glareolus

Biological odours of conspecifics are known to have strong influences on behavioural interaction in bank voles Clethrionomys glareolus. This experiment tested two hypotheses. (1) Olfactory cues from familiar and unfamiliar mature opposite-sex conspecifics differ in their attractiveness to males and females, and their behavioural reactions change with age. (2) A genetically based mechanism is involved in female recognition of kin.In a two-choice preference test, prepubertal males and females were more attracted to familiar than to unfamiliar odours of opposite-sex conspecifics, as manifested by more time spent sniffing familiar voles. As the young reached sexual maturity they shifted their odour preferences. Mature males and females preferred the novel odour of unrelated opposite-sex conspecifics to that of relatives. The results of experiments testing the second hypothesis indicate that females use a genetically based mechanism to recognise their kin. Young and mature females were able to recognise the odour of their biological but socially unknown fathers, and showed the same pattern of behaviour as females in previous experiments.The possible biological functions of kin recognition in bank voles are discussed.     

Olfactory regulation of maternal behavior in mammals

In mammals, olfactory cues are extensively used in many aspects of maternal care to ensure the coordination of mother-infant interactions and consequently the normal development of the offspring. Outside the period of parturition and lactation, when the young are not a behavioral priority, olfactory cues play an inhibitory role on maternal responsiveness since in most mammalian species studied so far, nonpregnant females find the odor of young aversive. On the contrary at the time of parturition, a shift in the hedonic value of infantile odors occurs so that the young now become a very potent stimulus and this sensorial processing constitutes an important part of the maternal motivational system. Moreover, infants' odors provide a basis for individual recognition by their mothers and some species (ungulates) have developed highly specialized mechanisms for processing of the infant signals. Perception of the smell of the young also regulates various aspects of maternal behavior. Dodecyl propionate, a compound released by of pup's preputial glands, has been shown to influence anogenital licking behavior, a fundamental pattern of maternal behavior in rodents. While there is no functional specificity of either the main or the accessory olfactory systems in the development of maternal behavior amongst species, it appears that only the main olfactory system is implicated when individual odor discrimination of the young is required. Neural structures, such as the main olfactory bulb, undergo profound changes when exposed to offspring odors at parturition. These changes in synaptic circuitry contribute both to maternal responsiveness to these odors, to their memorization, and to effects of long-term maternal experience.     

Mechanisms of activation of maternal behaviour in mammals

In mammals, the activation of maternal behaviour depends on internal maternal factors related with parturition. The nature of these factors may vary between species, although oestradiol, foetus expulsion and intracerebral oxytocin are the most commonly encountered. They induce a period of specific receptivity to some sensory cues provided by the neonate. These cues (tactile, olfactory, auditory, ...) also vary between species. The interactions between the mother and her progeny during this period, known as the sensitive period, facilitate the maintenance of maternal responsiveness beyond the initial phase of activation by the factors internal to the mother. The ability of mothers to display a well-adapted maternal behaviour is also modulated by maternal experience gained at the first parturition. Furthermore, this capacity is also influenced by the nature of the interactions experienced in infancy with the own mother of the female, which can lead to a non-genomic transmission of some individual characteristics of maternal behaviour or sensitivity to stress across generations.     

Infanticide in male laboratory mice: Effects of social status,prior sexual experience,and basis for discrimination between related and unrelated young

Several aspects of infanticide, including effects of social status, prior sexual experience, and the basis for discrimination between related and unrelated young, were examined in Swiss-Webster laboratory mice (Mus musculus). Strange males introduced into the female's cage for 24 h on day 1 postpartum significantly reduced pup survival whereas the introduction of sires did not. Direct observations of infanticide were frequent, and the motor patterns used by males to kill pups are described. Males killed their own offspring when those young were in the nest of a strange female, whereas most males did not kill unrelated young in the nest of a familiar female. Thus, past association with the mother appears to be the single most important factor mediating male discrimination of young. Prior contact with a specific female's urine reduced a male's propensity for subsequently killing her young. The act of copulation itself also reduced infanticide. Infanticidal behaviour was correlated with the male's social status: most dominant males killed unrelated pups, whereas none of the subordinates engaged in infanticide. These results are discussed in terms of the population biology of this species.     

Pheromones from males of different familiarity exert divergent effects on adult neurogenesis in the female accessory olfactory bulb

Pheromones from urine of unfamiliar conspecific male animals can reinitiate a female's estrus cycle to cause pregnancy block through the vomeronasal organ (VNO)‐accessory olfactory bulb (AOB)‐hypothalamic pathway. This phenomenon is called the Bruce effect. Pheromones from the mate of the female, however, do not trigger re‐entrance of the estrus cycle because an olfactory memory toward its mate is formed. The activity of the VNO‐AOB‐hypothalamic pathway is negatively modulated by GABAergic granule cells in the AOB. Since these cells are constantly replenished by neural stem cells in the subventricular zone (SVZ) of the lateral ventricle throughout adulthood and adult neurogenesis is required for mate recognition and fertility, we tested the hypothesis that pheromones from familiar and unfamiliar males may have different effects on adult AOB neurogenesis in female mice. When female mice were exposed to bedding used by a male or lived with one, cell proliferation and neuroblast production in the SVZ were increased. Furthermore, survival of newly generated cells in the AOB was enhanced. This survival effect was transient and mediated by norepinephrine. Interestingly, male bedding‐induced newborn cell survival in the AOB but not cell proliferation in the SVZ was attenuated when females were subjected to bedding from an unfamiliar male. Our results indicate that male pheromones from familiar and unfamiliar males exert different effects on neurogenesis in the adult female AOB. Given that adult neurogenesis is required for reproductive behaviors, these divergent pheromonal effects may provide a mechanism for the Bruce effect. © 2013 Wiley Periodicals, Inc. Develop Neurobiol 73: 632–645, 2013     

Kin recognition by tadpoles and froglets of the wood frog Rana sylvatica

Summary We investigated kin recognition by the wood frog Rana sylvatica in blind laboratory experiments using spatial proximity as a recognition assay. Tadpoles were tested for the ability to discriminate between: 1) familiar full-sibs and unfamiliar non-kin, 2) unfamiliar paternal half-sibs and unfamiliar non-kin, and 3) familiar and unfamiliar full-sibs. Tadpoles discriminated full- and paternal half-sibs from unrelated conspecifics, but did not discriminate between familiar and unfamiliar full-sibs. Froglets from the same laboratory population were tested for the ability to discriminate between 1) familiar full-sibs and unfamiliar non-kin, and 2) unfamiliar paternal half-sibs and unfamiliar non-kin. Froglets preferentially associated with full- and half-sibs over unrelated conspecifics. Our results show that familiarity, i.e., prior association, is not necessary for kin recognition in tadpoles and froglets. The ability of tadpoles and froglets to recognize unfamiliar paternal half-sibs demonstrates that a common maternal factor is not necessary for kin recognition, and indicates that the recognition cue has a genetic component. Our results add to the increasing evidence that a variety of vertebrate and invertebrate animals have the ability to recognize unfamiliar kin by using genetically specified recognition cues.     

A pheromone to behave, a pheromone to learn: the rabbit mammary pheromone

Birth is part of a continuum and is a major developmental change. Newborns need to adapt rapidly to the environment in terms of physiology and behaviour, and ability to locate the maternal source of milk is vital. Mechanisms have evolved resulting in the emission of olfactory cues by the mother and the processing of these cues by the young. Here, we focus on some sensory, cognitive and behavioural strategies developed by the European rabbit (Oryctolagus cuniculus) that optimize the early development of offspring. In this species, chemosensory communication between the mother and young plays a critical role in eliciting adaptive neonatal responses. In particular, lactating females release a molecule, the mammary pheromone, which has several functional impacts. It triggers orocephalic responses involved in the quick localization of nipples and sucking. Moreover, this unconditioned signal promotes rapid appetitive learning of novel odorants, acting as a potent organizer of neonatal cognition. The mammary-pheromone-induced odour memory requires consolidation/reconsolidation processes to be maintained in the long term. Finally, as this mode of conditioning also promotes learning of mixtures of odorants, it supports investigations related to the capacity of neonatal olfaction to extract biological value from the complex environment.     

Encoding choosiness: female attraction requires prior physical contact with individual male scents in mice

Scents, detected through both the main and vomeronasal olfactory systems, play a crucial role in regulating reproductive behaviour in many mammals. In laboratory mice, female preference for airborne urinary scents from males (detected through the main olfactory system) is learnt through association with scents detected through the vomeronasal system during contact with the scent source. This may reflect a more complex assessment of individual males than that implied by laboratory mouse studies in which individual variation has largely been eliminated. To test this, we assessed female preference between male and female urine using wild house mice with natural individual genetic variation in urinary identity signals. We confirm that females exhibit a general preference for male over female urine when able to contact urine scents. However, they are only attracted to airborne urinary volatiles from individual males whose urine they have previously contacted. Even females with a natural exposure to many individuals of both sexes fail to develop generalized attraction to airborne male scents. This implies that information gained through contact with a specific male's scent is essential to stimulate attraction, providing a new perspective on the cues and olfactory pathways involved in sex recognition and mate assessment in rodents.     

Prenatal and early sucking influences on dietary preference in newborn, weaning, and young adult cats

Early experiences are of potential importance in shaping long-term behavior. This study examined the relative influence of prenatal and/or early postnatal experience of chemosensory stimuli on subsequent olfactory and dietary preferences of cats as newborns, at 9-10 weeks, and at 6 months. Cats were exposed to vanillin or 4-ethylguaiacol via their mother's diet either prenatally, postnatally, perinatally (prenatal and postnatal), or experienced no exposure to the stimuli (control). Newborns were given a two-choice olfactory test between the familiar "odor" and no odor; 9-10 week olds were tested for their preference between two food treats, one flavored with the familiar stimulus and the other unflavored; at 6 months, cats were given a choice of two bowls of food, one flavored with the familiar stimulus and the other unflavored. At all ages, cats preferred the familiar, and avoided the unfamiliar, stimulus. Perinatal exposure exerted the strongest influence on preference. Prenatal exposure influenced preference at all ages and postnatal exposure exerted a stronger effect as the cat aged. We conclude that long-term chemosensory and dietary preferences of cats are influenced by prenatal and early (nursing) postnatal experience, supporting a natural and biologically relevant mechanism for the safe transmission of diet from mother to young.     

Maternal olfaction differentially modulates oxytocin and prolactin release during suckling in goats

In postparturient goats, olfactory recognition of the young allows the establishment of a selective bond between the mother and her kids. Once this bond is formed, the mother rejects alien young that attempt to suckle. We tested whether the development of the maternal selective bond in goats modulates prolactin (PRL) and oxytocin (OT) release in response to suckling. On day 37 of lactation, serial blood samples were taken during nursing of the mother's own or alien kid(s) in 10 intact/selective goats and in 10 goats rendered anosmic/nonselective through prepartum peripheral ZnSO(4) irrigation. Spontaneous nursing behavior was also studied weekly from day 7 to 30 of lactation, at which time milk production was measured. Maternal selectivity had no effect on PRL release, in contrast to OT release, which was significantly affected by this factor. Intact mothers released OT only when nursing their own kids, but not with aliens, while anosmic/nonselective dams showed an increase in OT levels regardless of the identity of the kids. In addition to these effects on maternal selectivity, the amplitude of the response of both hormones was lower in anosmic mothers than in intact mothers. Finally, nursing behavior and milk production were not significantly affected by anosmia. We conclude that maternal selective behavior in goats, which relies on the individual olfactory signature of the kid, modulates the OT, but not the PRL, response to suckling. In addition, perception of the smell of the young appears to have a general facilitatory effect, independent of the kid's identity, on the release of both hormones.     

The use of olfactory and other cues for social recognition by juvenile pigs

Social recognition is essential for the maintenance of a stable group structure. Failure to recognise familiar conspecifics in social groups of juvenile pigs may initiate agonistic encounters that can compromise welfare and productivity. Current housing systems may allow build up of atmospheric ammonia that might, in turn, interfere with the olfactory system and compromise olfactory perception. In the present study, 16 juvenile pigs were housed in fresh air while another 16 pigs were kept in an ammoniated atmosphere (approximately 36ppm) for 1 week prior to test and another week during testing. We then assessed the role of olfaction in social recognition and determined whether chronic exposure to ammonia compromised discrimination based on olfactory perception by comparing the pigs' responses to selected cues from a familiar and an unfamiliar pig presented simultaneously in separate chambers of a modified Y-maze in each of two test situations (near, remote). Visual, auditory, olfactory, and tactile cues were all provided in the "near" test situation; here, the stimulus pigs were presented in two separate chambers behind clear perspex walls containing an aperture that allowed nose-to-nose contact between the test and stimulus pigs. On the other hand, the "remote" test provided only olfactory cues via air passed from the chambers containing the stimulus pigs into the test chamber. Each test lasted 5min and the pigs' behaviour was recorded via overhead video cameras; we then measured the accumulated times spent near and the numbers of visits made to the familiar and the unfamiliar stimulus pigs as well as the transitions between them. Overall, pigs made more visits to and spent significantly longer near both the stimulus pigs in the near test than in the remote one (ANOVA, P<0.001). They also made more transitions between the stimuli in the former test than the latter (P<0.001). Pigs from both the ammonia and the fresh-air treatment groups showed social discrimination. However, pigs that had received chronic exposure to ammonia visited the familiar pig more often and spent longer near it than the unfamiliar one regardless of the test situation (P<0.05) whereas those reared in fresh air spent longer near the unfamiliar animal (P<0.05). The present results suggest that pigs from both treatment groups employed olfactory cues in social recognition, but that chronic exposure to ammonia did not interfere with this ability. However, ammonia treatment seemingly affected social preferences, thus indicating an unknown and more fundamental effect of living in ammoniated atmospheres.     

Olfactory Communication and Neighbor Recognition in Giant Kangaroo Rats

We hypothesized that olfactory communication facilitates neighbor recognition in the giant kangaroo rat, Dipodomys ingens , and is therefore influential in coordinating social interactions in this solitary, desert rodent. We tested whether (i) D. ingens can discriminate between odors of same- and opposite-sex conspecifics; and (ii) the kangaroo rats exhibit scent preferences based on familiarity. In habituation-discrimination tests, we found that both genders distinguish differences between the scent of individuals of the same- and opposite-sex. In olfactory preference tests, both males and females spent significantly more time investigating the scent of their familiar cagemate than the scent of an unfamiliar conspecific. Giant kangaroo rats may be able to recognize familiar neighbors from olfactory cues, thus supporting a hypothesis of neighbor recognition. Neighbor recognition may be an important mechanism of social interactions in this endangered species.     

Cross-Fostering of Male Mice Subtly Affects Female Olfactory Preferences

The maternal environment has been shown to influence female olfactory preferences through early chemosensory experience. However, little is known about the influence of the maternal environment on chemosignals. In this study, we used two inbred mouse strains, C57BL/6 (C57) and BALB/c (BALB), and explored whether adoption could alter male chemosignals and thus influence female olfactory preferences. In Experiment 1, C57 pups were placed with BALB dams. Adult BALB females then served as the subjects in binary choice tests between paired male urine odours (BALB vs. C57, BALB vs. adopted C57 and C57 vs. adopted C57). In Experiment 2, BALB pups were placed with C57 dams, and C57 females served as the subjects in binary choice tests between paired male urine odours (C57 vs. BALB, C57 vs. adopted BALB, and BALB vs. adopted BALB). In both experiments, we found that females preferred the urine of males from different genetic backgrounds, suggesting that female olfactory preferences may be driven by genetic compatibility. Cross-fostering had subtle effects on female olfactory preferences. Although the females showed no preference between the urine odours of adopted and non-adopted males of the other strain, the BALB females preferred the urine odour of BALB males to that of adopted C57 males, whereas the C57 females showed no preference between the urine odour of C57 and adopted BALB males. Using gas chromatography-mass spectrometry (GC-MS) and stepwise discriminant analysis, we found that the ratios of volatile chemicals from urine and preputial gland secretions were altered in the fostered male mice; these changes may have resulted in the behavioural changes observed in the females. Overall, the results suggest that female mice prefer urine odours from males with different genetic backgrounds; this preference may be driven by genetic compatibility. The early maternal environment influences the chemosignals of males and thus may influence the olfactory preferences of females. Our study provides additional evidence in support of genotype-dependent maternal influences on phenotypic variability in adulthood.     

Young female pigs can discriminate individual differences in odours from conspecific urine

The ability to discriminate odour cues from different conspecifics has been demonstrated in a variety of small mammalian species. We used a habituation-dishabituation procedure to investigate whether 10-week-old female pigs,Sus scrofa , are able to discriminate between urinary odours from similar-aged conspecifics that were unfamiliar (not encountered for at least 7 weeks). We also examined whether environmental factors can affect the ease with which urine from different individuals is discriminated. Subjects receiving urine samples from the same unfamiliar individual in two successive 2-min exposures separated by a 15-min interval showed habituation in their investigation response to the urine in the second exposure. This habituation was maintained in a third 2-min exposure, 15 min later, if the urine sample was again from the same individual. However, if the urine sample was from a different unfamiliar individual, there was a dishabituation of the investigation response. This was taken to indicate an ability to discriminate the two samples. These data indicate that young pigs could use urinary cues to discriminate other individuals. Effective individual discrimination should facilitate the formation and maintenance of stable social groupings but could be disrupted if, for example, animals from the same group share common odour cues that mask individually distinctive scents. However, urine samples from individuals living in the same group appeared to be no more difficult to discriminate than those from individuals living in different groups. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Sexual behaviour and its olfactory control in the desert woodrat (Neotoma lepida lepida)

In studies 1 and 2 nine pairs of desert woodrats (Neotoma lepida lepida) were observed for copulatory behaviour when the female was in a state of naturally occurring oestrus (study 1) and following ovariectomy and oestrogen and progesterone replacement (study 2). Males and females respond in a similar way under conditions of natural and hormone-induced oestrus. Males show a consummatory pattern involving multiple mounts and ejaculations, with ejaculations occurring after single intromissions. Females show the lordosis reflex accompanied by hop-and-dart and ear-wiggling responses. In addition, both sexes show appetitive precopulatory behaviours; the male emits an audible rasping vocalization as he trails and mounts the female, following a period of intense sniffing of the female's anogenital region. The female also frequently approaches and sniffs the male. In study 3, the role of female odours in the sexual behaviour of the male was examined in eight of the nine pairs used in studies 1 and 2. This was done by applying to the anogenital region of ovariectomized females a combination of urine and vaginal secretions taken from familiar and unfamiliar, and oestrogen-primed or non-oestrogen-primed females. The results show that odours from oestrogen-primed females are not sufficient to elicit male sexual behaviour, if the female is not sexually active. In study 4 the eight males were tested for their preferences for urine and vaginal secretion odours taken from females in different reproductive states and applied to cotton swabs. These males spent more time sniffing unfamiliar oestrous odours than unfamiliar non-oestrous odours and more time sniffing oestrous odours from a familiar female over those taken from an unfamiliar female.In study 5, 12 sexually active males were tested with oestrogen-primed females before and after either olfactory bulb removal or sham-surgery. Bulbectomized animals ceased copulating with females although females showed precopulatory approaches.Taken together, these studies suggest that normal sexual behaviour in the male woodrat requires that the female both possess the attractive odours (of oestrus) and that she engage in appetitive precopulatory behaviour.     

Sex-specific responses to sexual familiarity,and the role of olfaction in Drosophila

Studies of mating preferences have largely neglected the potential effects of individuals encountering their previous mates (‘directly sexually familiar’), or new mates that share similarities to previous mates, e.g. from the same family and/or environment (‘phenotypically sexually familiar’). Here, we show that male and female Drosophila melanogaster respond to the direct and phenotypic sexual familiarity of potential mates in fundamentally different ways. We exposed a single focal male or female to two potential partners. In the first experiment, one potential partner was novel (not previously encountered) and one was directly familiar (their previous mate); in the second experiment, one potential partner was novel (unrelated, and from a different environment from the previous mate) and one was phenotypically familiar (from the same family and rearing environment as the previous mate). We found that males preferentially courted novel females over directly or phenotypically familiar females. By contrast, females displayed a weak preference for directly and phenotypically familiar males over novel males. Sex-specific responses to the familiarity of potential mates were significantly weaker or absent in Orco¹ mutants, which lack a co-receptor essential for olfaction, indicating a role for olfactory cues in mate choice over novelty. Collectively, our results show that direct and phenotypic sexual familiarity is detected through olfactory cues and play an important role in sex-specific sexual behaviour.