Honest olfactory ornamentation in a female‐dominant primate

Sexual selection theory predicts that potential mates or competitors signal their quality to conspecifics. Whereas evidence of honest visual or vocal signals in males abounds, evidence of honest signalling via scent or by females is scarce. We previously showed that scent marks in male lemurs seasonally encode information about individual heterozygosity – a reliable predictor of immunocompetence and survivorship. As female lemurs dominate males, compete over resources, and produce sexually differentiated scent marks that likely evolved via direct selection, here we tested whether females also advertise genetic quality via olfactory cues. During the breeding season specifically, individual heterozygosity correlated negatively with the diversity of fatty acids (FAs) expressed in labial secretions and positively with the diversity of heavy FA esters. As odour–gene relationships predictive of health and survivorship emerged during a period critical to mate choice and female competition, we posit that genital scent marks function as honest olfactory ornaments in females.     

Scent and the single male: ring-tailed lemurs produce honest signals

In mating systems that involve competing males and choosy females, males are expected to advertise their genetic quality to discriminating females. Most examples have focused on visual or acoustic signals, such as ornamentation or song; yet arguably, olfactory communication may be more important to the majority of vertebrates with the possible exception of birds. Fortunately, attention has begun to shift to the role of odours in mate choice, with most of that attention being directed at the major histocompatibility complex or more recently at the major urinary proteins. The study of male ring-tailed lemurs presented by Charpentier and colleagues in this issue adds a new dimension to investigations of the influence of genes on mate choice via odour production. By comparing genetic heterozygosity to the production of semiochemicals in the scrotal scent gland, they provide a link between genetic composition and scent-marking behaviour as a potential advertisement of male quality.     

Murine scent mark microbial communities are genetically determined

Scent marking in mice allows males to communicate information such as territory ownership, male competitive ability and current reproductive, nutritional, social and health status. It has been suggested that female mice eavesdrop on these olfactory cues, using them as a means of selecting mates with dissimilar major histocompatibility complex (MHC) genes, known as H2 in mice. The mechanisms underpinning MHC-dependent olfactory communication remain unresolved. Using congenic mouse strains and molecular methods we explore the involvement of the microbial communities, a known source of odourants, in scent marks to test the hypothesis that the microbial communities and hence the olfactory signals are genetically determined. Here we show that the indigenous microbial community of murine scent marks is genetically determined. Both background genotype and H2 haplotype influence the community structure of the scent mark flora, removing the possibility that community composition is solely orchestrated by the MHC. Qualitative and quantitative components of the bacterial community associated with MHC haplotype and background genotype were identified. The analyses confirm that the four groups of congenic mice tested are distinguishable on basis of the microbiology of their scent marks alone, strengthening the role of microorganisms in the development of MHC-dependent odours.     

Sex, age, and family differences in the chemical composition of owl monkey (Aotus nancymaae) subcaudal scent secretions

Numerous behavioral studies have shown that animals use olfactory cues as inbreeding avoidance or kin avoidance mechanisms, implying that scent is unique to families. However, few studies have analyzed the chemical profile of a scent and ascertained the messages that are conveyed in scent secretions. Owl monkeys (Aotus nancymaae) are socially monogamous primates that utilize scent when interacting with foreign conspecifics. This suggests there is a difference in the chemical composition of scent marks. We chemically analyzed sub-caudal gland samples from three families of captive owl monkeys (Aotus nancymaae). Samples were analyzed by capillary GC-MS and relative retention time and fragment pattern was compared with known standards. Gland samples were high in large plant-based shikikate metabolites and fatty ketones; alcohols, acids, and acetates were virtually absent. Gender, age, and family could be reliably classified using discriminant analysis (92.9, 100, and 100%, respectively). Female scent profiles were greater in concentration of aromatic plant metabolites, possibly the result of a different diet or physiological differences in female metabolism as compared to male. Offspring of adult age still living in their natal group showed a less complex chemical profile than their parents. Finally, each family had its own unique and complex chemical profile. The presence of family scent may play a role in mediating social interactions.     

Effect of B2m gene disruption on MHC-determined odortypes

 Major histocompatibility complex (MHC) genes confer individual olfactory identity that can be detected with exquisite accuracy by mice. The fact that MHC genes themselves generate the characteristic odortype, rather than dedicated odor-determining genes, was supported in studies of point mutations in H2K and HLA transgenic mice, which evinced distinct odor profiles in olfactory assays. In this article we provide further evidence for a central role of MHC genes themselves in odortype specification by demonstrating that mice that are unable to express their genomic class I MHC genes because they lack β₂-microglobulin are distinguishable by scent from otherwise identical mice which possess an intact B2m gene. This odortype disparity appears at 9–12 days of gestational age, the period in which the MHC is first detectable in fetal cells of normal mice. Received: 15 October 1999 / Revised: 30 December 1999     

Plumage microbiota covaries with the major histocompatibility complex in blue petrels

To increase fitness, a wide range of vertebrates preferentially mate with partners that are dissimilar at the major histocompatibility complex (MHC) or that have high MHC diversity. Although MHC often can be assessed through olfactory cues, the mechanism by which MHC genes influence odour remains largely unclear. MHC class IIB molecules, which enable recognition and elimination of extracellular bacteria, have been suggested to influence odour indirectly by shaping odour‐producing microbiota, i.e. bacterial communities. However, there is little evidence of the predicted covariation between an animal's MHC genotype and its bacterial communities in scent‐producing body surfaces. Here, using high‐throughput sequencing, we tested the covariation between MHC class IIB genotypes and feather microbiota in the blue petrel (Halobaena caerulea), a seabird with highly developed olfaction that has been suggested to rely on oduor cues during an MHC‐based mate choice. First, we show that individuals with similar MHC class IIB profiles also have similar bacterial assemblages in their feathers. Then, we show that individuals with high MHC diversity have less diverse feather microbiota and also a reduced abundance of a bacterium of the genus Arsenophonus, a genus in which some species are symbionts of avian ectoparasites. Our results, showing that feather microbiota covary with MHC, are consistent with the hypothesis that individual MHC genotype may shape the semiochemical‐producing microbiota in birds.     

MHC‐disassortative mate choice and inbreeding avoidance in a solitary primate

Sexual selection theory suggests that choice for partners carrying dissimilar genes at the major histocompatibility complex (MHC) may play a role in maintaining genetic variation in animal populations by limiting inbreeding or improving the immunity of future offspring. However, it is often difficult to establish whether the observed MHC dissimilarity among mates drives mate choice or represents a by‐product of inbreeding avoidance based on MHC‐independent cues. Here, we used 454‐sequencing and a 10‐year study of wild grey mouse lemurs (Microcebus murinus), small, solitary primates from western Madagascar, to compare the relative importance on the mate choice of two MHC class II genes, DRB and DQB, that are equally variable but display contrasting patterns of selection at the molecular level, with DRB under stronger diversifying selection. We further assessed the effect of the genetic relatedness and of the spatial distance among candidate mates on the detection of MHC‐dependent mate choice. Our results reveal inbreeding avoidance, along with disassortative mate choice at DRB, but not at DQB. DRB‐disassortative mate choice remains detectable after excluding all related dyads (characterized by a relatedness coefficient r > 0), but varies slightly with the spatial distance among candidate mates. These findings suggest that the observed deviations from random mate choice at MHC are driven by functionally important MHC genes (like DRB) rather than passively resulting from inbreeding avoidance and further emphasize the need for taking into account the spatial and genetic structure of the population in correlative tests of MHC‐dependent mate choice.     

The effects of olfactory stimulation on the behavior of captive ring‐tailed lemurs (Lemur catta)

Ring‐tailed lemurs reside in many animal collections worldwide. Lemur welfare may be a cause of concern due to some captive individuals exhibiting stereotypic behavior. Despite these concerns, there has been little exploration of methods of environmental enrichment for ring‐tailed lemurs. Olfactory stimulation can enhance captive animal welfare by encouraging species‐typical behaviors, enhancing behavioral diversity, and decreasing stereotypic behaviors. We aimed to investigate the effects of olfactory stimulation via lavender, peppermint, coconut, and prey odor upon the behavior of eight captive ring‐tailed lemurs. We exposed the lemurs to six individual odor conditions (odor control, novel object control, lavender, peppermint, coconut, and Morio worms) and observed them for 4 hr a day for 3 days with an intervening period of 4 days between conditions. We recorded the lemurs’ behavior under each condition using instantaneous scan sampling. We found significant effects of olfactory stimulation on the ring‐tailed lemurs’ behavior in the initial analysis but these did not survive correction for multiple testing. Overall, while our findings are suggestive of a general effect of olfactory stimulation on the captive ring‐tailed lemurs they did not indicate a marked influence of olfactory condition. However, further investigation with a larger sample size and more biologically relevant odors may be beneficial to fully examine potential effects of olfactory stimulation in captive lemurs.     

Chemical composition of scent marks in the ringtailed lemur (Lemur catta): glandular differences, seasonal variation, and individual signatures

The apocrine and sebaceous scent glands of ringtailed lemurs (Lemur catta) appear to serve different social functions. In behavioral experiments, lemurs modulate their responses to scent marks based on the type of odorant, their own physiological state, the signaler's physiological state, and prior social experience. To examine variation in odorant chemistry relative to olfactory behavior, we used gas chromatography and mass spectrometry to analyze over 86 samples of glandular secretion collected over 2 years from 15 adult lemurs. Labial and scrotal secretions contained organic acids and esters, whereas male brachial secretions were composed almost entirely of squalene and cholesterol derivatives. Principal component and linear discriminant analyses revealed glandular, individual-specific, and seasonal variation in chemical profiles but no relationship to the signaler's social status. The chemical composition of the various secretions provides further clues about the function of the different glands: the higher molecular weight compounds in genital and brachial secretions may increase signal longevity and provide lasting information to conspecifics, consistent with a role in advertising resource ownership or reproductive state. Conversely, the lower molecular weight compounds of antebrachial secretions produce ephemeral signals used primarily in social dominance displays and require integration of multiple sensory modalities for effective signal transmission.     

The role of uropygial gland on sexual behavior in domestic chicken Gallus gallus domesticus

Recent studies have indicated that avian social behavior is influenced by olfactory cues. During the reproductive season a change in the chemical composition of uropygial gland secretion has been reported in some species and the hypothesis that olfactory signals may be produced by this gland has been proposed. To examine this hypothesis we performed two behavioral experiments to determine whether a female’s uropygial gland produce chemical signals that stimulate mating behaviors in domestic chickens. In Experiment 1 the role of the female’s uropygial gland in male mating behavior was examined by removing and examining the female’s uropygial gland. The frequency of mounts and copulations of intact male birds with sham-operated female birds was significantly higher than with uropygial glandectomized female birds. With respect to the number of waltzing that is one of the courtship displays intact males showed no significant difference between sham-operated female birds and uropygial glandectomized female birds. In Experiment 2 the relationship between male olfaction and the female’s uropygial gland was investigated using olfactory bulbectomized male birds. The number of mounts and copulations of sham-operated male birds with sham-operated female bird was significantly higher than with uropygial glandectomized female birds. In contrast olfactory bulbectomized male birds showed no significant differences in the number of mounts and copulations between sham-operated female birds and uropygial glandectomized female birds. These results indicate that intact and sham-operated male birds prefer to mate with female birds with the uropygial gland. The number of courtship waltzing of sham-operated male birds showed no significant difference. However olfactory bulbectomized male birds significantly courted to uropygial glandectomized female birds. Summarizing our results show that while anosmic males did not have any preference both intact and sham-operated male birds chose to mate with female birds having an intact uropygial gland suggesting that mate preference involves in male olfaction and that the female’s uropygial gland acts as a source of social odor cues in domestic chickens.     

Smelling wrong: hormonal contraception in lemurs alters critical female odour cues

Animals, including humans, use olfaction to assess potential social and sexual partners. Although hormones modulate olfactory cues, we know little about whether contraception affects semiochemical signals and, ultimately, mate choice. We examined the effects of a common contraceptive, medroxyprogesterone acetate (MPA), on the olfactory cues of female ring-tailed lemurs (Lemur catta), and the behavioural response these cues generated in male conspecifics. The genital odorants of contracepted females were dramatically altered, falling well outside the range of normal female variation: MPA decreased the richness and modified the relative abundances of volatile chemicals expressed in labial secretions. Comparisons between treatment groups revealed several indicator compounds that could reliably signal female reproductive status to conspecifics. MPA also changed a female''s individual chemical ‘signature’, while minimizing her chemical distinctiveness relative to other contracepted females. Most remarkably, MPA degraded the chemical patterns that encode honest information about genetic constitution, including individual diversity (heterozygosity) and pairwise relatedness to conspecifics. Lastly, males preferentially investigated the odorants of intact over contracepted females, clearly distinguishing those with immediate reproductive potential. By altering the olfactory cues that signal fertility, individuality, genetic quality and relatedness, contraceptives may disrupt intraspecific interactions in primates, including those relevant to kin recognition and mate choice.     

Parasite diversity,patterns of MHC II variation and olfactory based mate choice in diverging three-spined stickleback ecotypes

Ecological speciation has been the subject of intense research in evolutionary biology but the genetic basis of the actual mechanism driving reproductive isolation has rarely been identified. The extreme polymorphism of the major histocompatibility complex (MHC), probably maintained by parasite-mediated selection, has been proposed as a potential driver of population divergence. We performed an integrative field and experimental study using three-spined stickleback river and lake ecotypes. We characterized their parasite load and variation at MHC class II loci. Fish from lakes and rivers harbor contrasting parasite communities and populations possess different MHC allele pools that could be the result of a combined action of genetic drift and parasite-mediated selection. We show that individual MHC class II diversity varies among populations and is lower in river ecotypes. Our results suggest the action of homogenizing selection within habitat type and diverging selection between habitat types. Finally, reproductive isolation was suggested by experimental evidence: in a flow channel design females preferred assortatively the odor of their sympatric male. This demonstrates the role of olfactory cues in maintaining reproductive isolation between diverging fish ecotypes.     

MHC odours are not required or sufficient for recognition of individual scent owners

To provide information about specific depositors, scent marks need to encode a stable signal of individual ownership. The highly polymorphic major histocompatibility complex (MHC) influences scents and contributes to the recognition of close kin and avoidance of inbreeding when MHC haplotypes are shared. MHC diversity between individuals has also been proposed as a primary source of scents used in individual recognition. We tested this in the context of scent owner recognition among male mice, which scent mark their territories and countermark scents from other males. We examined responses towards urine scent according to the scent owner's genetic difference to the territory owner (MHC, genetic background, both and neither) or genetic match to a familiar neighbour. While urine of a different genetic background from the subject always stimulated greater scent marking than own, regardless of familiarity, MHC-associated odours were neither necessary nor sufficient for scent owner recognition and failed to stimulate countermarking. Urine of a different MHC type to the subject stimulated increased investigation only when this matched both the MHC and genetic background of a familiar neighbour. We propose an associative model of scent owner recognition in which volatile scent profiles, contributed by both fixed genetic and varying non-genetic factors, are learnt in association with a stable involatile ownership signal provided by other highly polymorphic urine components.     

Odor supported place cell model and goal navigation in rodents

Experiments with rodents demonstrate that visual cues play an important role in the control of hippocampal place cells and spatial navigation. Nevertheless, rats may also rely on auditory, olfactory and somatosensory stimuli for orientation. It is also known that rats can track odors or self-generated scent marks to find a food source. Here we model odor supported place cells by using a simple feed-forward network and analyze the impact of olfactory cues on place cell formation and spatial navigation. The obtained place cells are used to solve a goal navigation task by a novel mechanism based on self-marking by odor patches combined with a Q-learning algorithm. We also analyze the impact of place cell remapping on goal directed behavior when switching between two environments. We emphasize the importance of olfactory cues in place cell formation and show that the utility of environmental and self-generated olfactory cues, together with a mixed navigation strategy, improves goal directed navigation.     

Sensory Basis of Food Detection in Wild <Emphasis Type="BoldItalic">Microcebus murinus</Emphasis>

Very little is known about how nocturnal primates find their food. Here we studied the sensory basis of food perception in wild-caught gray mouse lemurs (Microcebus murinus) in Madagascar. Mouse lemurs feed primarily on fruit and arthropods. We established a set of behavioral experiments to assess food detection in wild-born, field-experienced mouse lemurs in short-term captivity. Specifically, we investigated whether they use visual, auditory, and motion cues to find and to localize prey arthropods and further whether olfactory cues are sufficient for finding fruit. Visual cues from motionless arthropod dummies were not sufficient to allow reliable detection of prey in choice experiments, nor did they trigger prey capture behavior when presented on the feeding platform. In contrast, visual motion cues from moving prey dummies attracted their attention. Behavioral observations and experiments with live and recorded insect rustling sounds indicated that the lemurs make use of prey-generated acoustic cues for foraging. Both visual motion cues and acoustic prey stimuli on their own were sufficient to trigger approach and capture behavior in the mouse lemurs. For the detection of fruit, choice experiments showed that olfactory information was sufficient for mouse lemurs to find a piece of banana. Our study provides the first experimental data on the sensory ecology of food detection in mouse lemurs. Further research is necessary to address the role of sensory ecology for food selection and possibly for niche differentiation between sympatric Microcebus species.     

Conspecific olfactory preferences and interspecific divergence in odor cues in a chickadee hybrid zone

Understanding how mating cues promote reproductive isolation upon secondary contact is important in describing the speciation process in animals. Divergent chemical cues have been shown to act in reproductive isolation across many animal taxa. However, such cues have been overlooked in avian speciation, particularly in passerines, in favor of more traditional signals such as song and plumage. Here, we aim to test the potential for odor to act as a mate choice cue, and therefore contribute to premating reproductive isolation between the black‐capped (Poecile atricapillus) and Carolina chickadee (P. carolinensis) in eastern Pennsylvania hybrid zone populations. Using gas chromatography–mass spectrometry, we document significant species differences in uropygial gland oil chemistry, especially in the ratio of ester to nonester compounds. We also show significant preferences for conspecific over heterospecific odor cues in wild chickadees using a Y‐maze design. Our results suggest that odor may be an overlooked but important mating cue in these chickadees, potentially promoting premating reproductive isolation. We further discuss several promising avenues for future research in songbird olfactory communication and speciation.     

D'scent of man: A comparative survey of primate chemosignaling in relation to sex

This article is part of a Special Issue (Chemosignals and Reproduction).As highly visual animals, primates, in general, and Old World species (including humans), in particular, are not immediately recognized for reliance in their daily interactions on olfactory communication. Nevertheless, views on primate olfactory acuity and the pervasiveness of their scent signaling are changing, with increased appreciation for the important role of body odors in primate social and sexual behavior. All major taxonomic groups, from lemurs to humans, are endowed with scent-producing organs, and either deposit or exude a wealth of volatile compounds, many of which are known semiochemicals. This review takes a comparative perspective to illustrate the reproductive context of primate signaling, the relevant information content of their signals, the sexually differentiated investigative responses generated, and the behavioral or physiological consequences of message transmission to both signaler and receiver. Throughout, humans are placed alongside their relatives to illustrate the evolutionary continuum in the sexual selection of primate chemosignals. This ever-growing body of evidence points to a critical role of scent in guiding the social behavior and reproductive function throughout the primate order.     

Gibt es einen „Duft der MHC‐Gene“?

MHC‐Genes: Do they influence the choice of partners via olfactory signals? Behavioral experiments in mice and humans suggest that genes of the major histocompatibilty complex (MHC) may be important for the differentiation of self and non‐self during mate choice. While this correlation is well documented for certain mouse strains, it is controversial for humans. Signal transfer between potential partners is considered to occur via the production of MHC‐dependent olfactory cues by a sender and their recognition by olfaction in the recipient. It is shown that in mice and humans the overall bouquet of volatiles is not and the pattern of peptides in mice is only marginally influenced by the MHC genes. However, in mice, olfactory cues without MHC contribution appear to play a role in mate choice, in that the profile learned from the parents during rearing is compared with the distinct profile of a potential partner, which is in turn selected for mating. Such olfactory differentiation between close relatives and potential mates without MHC‐contribution may also operate unconsciously in humans.     

The major histocompatibility complex and the chemosensory signalling of individuality in humans

The chemosensory identity of mice and rats is determined partly by polymorphic genes of the major histocompatibility complex (MHC). In inbred strains of mice, as well as in seminatural populations, MHC‐associated mating preferences selectively influence reproductive success, thus serving to promote heterozygocity in the MHC. In order to determine whether MHC‐associated chemosignals are present in humans, two studies were conducted. In a first study, olfactory identification of MHC‐associated chemosignals was conducted on 12 trained rats' responses to the urine odors of humans. In a second study, MHC‐associated olfactory cues in humans were analyzed by means of gas chromatography. The results indicate that the urine odors of humans are associated with the MHC and demonstrate that the profile of volatile components in the urine odors shows some association with the MHC. Furthermore, results show that a profile of some specific components, as well as a few ubiquitous volatiles, constitutes MHC‐associated odor signals in humans. This revised version was published online in July 2006 with corrections to the Cover Date.     

Olfaction and human kin recognition

Humans, like other mammals, are capable of discriminating between kin and non‐kin by olfactory cues alone. Shortly after birth, breastfed infants become familiar with, and respond preferentially to, their mother' unique odor signature. Mothers likewise recognize the characteristic scent of their newborn infant. Close biological relatives share somewhat similar odor signatures (presumably resulting from genetically mediated similarities in bodily biochemistry and metabolism) that could facilitate kin recognition. This revised version was published online in July 2006 with corrections to the Cover Date.