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.     

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.     

Male heterozygosity predicts territory size, song structure and reproductive success in a cooperatively breeding bird

Recent studies of non-social animals have shown that sexually selected traits signal at least one measure of genetic quality: heterozygosity. To determine whether similar cues reveal group quality in more complex social systems, we examined the relationship between territory size, song structure and heterozygosity in the subdesert mesite (Monias benschi), a group-living bird endemic to Madagascar. Using nine polymorphic microsatellite loci, we found that heterozygosity predicted both the size of territories and the structure of songs used to defend them: more heterozygous groups had larger territories, and more heterozygous males used longer, lower-pitched trills in their songs. Heterozygosity was linked to territory size and song structure in males, but not in females, implying that these traits are sexually selected by female choice and/or male-male competition. To our knowledge, this study provides the first direct evidence in any animal that territory size is related to genetic diversity. We also found a positive association between seasonal reproductive success and heterozygosity, suggesting that this heritable characteristic is a reliable indicator of group quality and fitness. Given that heterozygosity predicts song structure in males, and can therefore be determined by listening to acoustic cues, we identify a mechanism by which social animals may assess rival groups, prospective partners and group mates, information of potential importance in guiding decisions related to conflict, breeding and dispersal.     

Genetic diversity revealed in human faces

From an evolutionary perspective, human facial attractiveness is proposed to signal mate quality. Using a novel approach to the study of the genetic basis of human preferences for facial features, we investigated whether attractiveness signals mate quality in terms of genetic diversity. Genetic diversity in general has been linked to fitness and reproductive success, and genetic diversity within the major histocompatibility complex (MHC) has been linked to immunocompetence and mate preferences. We asked whether any preference for genetic diversity is specific to MHC diversity or reflects a more general preference for overall genetic diversity. We photographed and genotyped 160 participants using microsatellite markers situated within and outside the MHC, and calculated two measures of genetic diversity: mean heterozygosity and standardized mean d(2). Our results suggest a special role for the MHC in female preferences for male faces. MHC heterozygosity positively predicted male attractiveness, and specifically facial averageness, with averageness mediating the MHC-attractiveness relationship. For females, standardized mean d(2) at non-MHC loci predicted facial symmetry. Thus, attractive facial characteristics appear to provide visual cues to genetic quality in both males and females, supporting the view that face preferences have been shaped by selection pressures to identify high-quality mates.     

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.     

Olfactory kin recognition in a songbird

The ability to recognize close relatives in order to cooperate or to avoid inbreeding is widespread across all taxa. One accepted mechanism for kin recognition in birds is associative learning of visual or acoustic cues. However, how could individuals ever learn to recognize unfamiliar kin? Here, we provide the first evidence for a novel mechanism of kin recognition in birds. Zebra finch (Taeniopygia guttata) fledglings are able to distinguish between kin and non-kin based on olfactory cues alone. Since olfactory cues are likely to be genetically based, this finding establishes a neglected mechanism of kin recognition in birds, particularly in songbirds, with potentially far-reaching consequences for both kin selection and inbreeding avoidance.     

Female preference for conspecific males based on olfactory cues in a Lake Malawi cichlid fish

Research on reproductive isolation in African cichlid fishes has largely focused on the role of nuptial colours, but other sensory modes may play an important role in mate choice. Here, we compare the relative importance of visual and olfactory cues in mate recognition by females of a Lake Malawi cichlid species. Female Pseudotropheus emmiltos were given a choice of spawning next to a conspecific male or a male of the closely-related sympatric Pseudotropheus fainzilberi. Significant preference for conspecific males only occurred when olfactory cues were present. This suggests that divergence of olfactory signals may have been an important influence on the explosive radiation of the East African species flock.     

Multiple sexual ornaments signal heterozygosity in male blue tits

Higher individual genetic quality has been hypothesized to be associated with the expression of conspicuous ornaments. However, the relationship between multicomponent sexual signals and heterozygosity is poorly understood. In this study, we examined whether different ornaments, including song (repertoire size and bout length) and plumage coloration (yellow breast and blue crown), reflect individual genetic diversity in male blue tits (Aves: Cyanistes caeruleus). We estimated genetic diversity using 26 microsatellite markers that were classified as putatively functional (12 loci) and neutral (14 loci). We found that yellow breast carotenoid chroma, blue crown brightness, bout length and body condition were positively associated with heterozygosity at functional loci, but not with genetic diversity estimated at all typed loci or the subset of neutral markers. The lack of strong single‐locus effects and the presence of identity disequilibrium in our population suggest that the observed heterozygosity‐phenotype associations are driven by loci widely distributed across the genome. The predominant role of putatively functional loci evidences that the expression of secondary sexual characters is more tightly reflected by heterozygosity at genomic regions containing coding genes that are being actively expressed, a fact that may make ornamental traits more reliable indicators of the genetic quality of individuals. Overall, this study shows that multiple secondary sexual characters reflect male genetic diversity and lends support to the good‐genes‐as‐heterozygosity hypothesis. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 362–375.     

Sex-specific genotype-by-environment interactions for cuticular hydrocarbon expression in decorated crickets, Gryllodes sigillatus: implications for the evolution of signal reliability

Phenotypic traits that convey information about individual identity or quality are important in animal social interactions, and the degree to which such traits are influenced by environmental variation can have profound effects on the reliability of these cues. Using inbred genetic lines of the decorated cricket, Gryllodes sigillatus, we manipulated diet quality to test how the cuticular hydrocarbon (CHC) profiles of males and females respond across two different nutritional rearing environments. There were significant differences between lines in the CHC profiles of females, but the effect of diet was not quite statistically significant. There was no significant genotype-by-environment interaction (GEI), suggesting that environmental effects on phenotypic variation in female CHCs are independent of genotype. There was, however, a significant effect of GEI for males, with changes in both signal quantity and content, suggesting that environmental effects on phenotypic expression of male CHCs are dependent on genotype. The differential response of male and female CHC expression to variation in the nutritional environment suggests that these chemical cues may be under sex-specific selection for signal reliability. Female CHCs show the characteristics of reliable cues of identity: high genetic variability, low condition dependence and a high degree of genetic determination. This supports earlier work showing that female CHCs are used in self-recognition to identify previous mates and facilitate polyandry. In contrast, male CHCs show the characteristics of reliable cues of quality: condition dependence and a relatively higher degree of environmental determination. This suggests that male CHCs are likely to function as cues of underlying quality during mate choice and/or male dominance interactions.     

A Preliminary Investigation of Parent–Progeny Olfactory Recognition and Parental Investment

The role of olfaction in kin recognition and parental investment is documented in many mammalian/vertebrate species. Research on humans, however, has only focused on whether parents are able to recognize their children by smell, not whether humans use these cues for investment decisions. Here we show that fathers exhibit more affection and attachment and fewer ignoring behaviors toward children whose smell they can identify than toward those whose smell they cannot recognize. Thus, olfaction might serve as a means for males to determine their genetic relatedness to purported offspring. We also demonstrate that mothers’ olfactory recognition and hedonistic ratings are linked with the use of physical punishment. Mothers report using more punishment with children whose odor they cannot recognize and less with children whose odor they rated as more pleasant. These results provide the first preliminary evidence in humans that olfactory cues may guide parents in the allocation of care.     

Integration of Visual and Olfactory Cues in Host Plant Identification by the Asian Longhorned Beetle,Anoplophora glabripennis (Motschulsky) (Coleoptera: Cerambycidae)

Some insects use host and mate cues, including odor, color, and shape, to locate and recognize their preferred hosts and mates. Previous research has shown that the Asian longicorn beetle, Anoplophora glabripennis (Motschulsky), uses olfactory cues to locate host plants and differentiate them from non-host plants. However, whether A. glabripennis adults use visual cues or a combination of visual and olfactory cues remains unclear. In this study, we tested the host location and recognition behavior in A. glabripennis, which infests a number of hardwood species and causes considerable economic losses in North America, Europe and Asia. We determined the relative importance of visual and olfactory cues from Acer negundo in host plant location and recognition, as well as in the discrimination of non-host plants (Sabina chinensis and Pinus bungeana), by female and male A. glabripennis. Visual and olfactory cues from the host plants (A. negundo), alone and combined, attracted significantly more females and males than equivalent cues from non-host plants (S. chinensis and P. bungeana). Furthermore, the combination of visual and olfactory cues of host plants attracted more adults than either cue alone, and visual cues alone attracted significantly more adults than olfactory cues alone. This finding suggests that adult A. glabripennis has an innate preference for the visual and/or olfactory cues of its host plants (A. negundo) over those of the non-host plant and visual cues are initially more important than olfactory cues for orientation; furthermore, this finding also suggests that adults integrate visual and olfactory cues to find their host plants. Our results indicate that different modalities of host plant cues should be considered together to understand fully the communication between host plants and Asian longhorned beetles.     

The importance of olfactory signals in the gasterosteid mating system: sticklebacks go multimodal

Stickleback fishes are renowned for the complexity of their nuptial colour signal. In this paper I show that the nuptial signal is in fact multimodal: male-based olfactory cues also transmit information to receptive females. Both female three-spined and brook sticklebacks recognized the scent from each other's males, but discriminated in favour of their own males when asked to choose between conspecific and heterospecific odours. Although females were not attracted to scent from the more distantly related guppy, Poecilia reticulata , changes in their baseline behaviours indicated that they perceived its presence. Olfactory cues act as long distance messages, allowing a female to detect the 'I am here' message from the male before she can actually see him. Studies of interactions between temporally displaced signals indicate that the first cue (in this case chemical) functions to alert the receiver to the presence of the second cue (visual), increasing the probability of its detection and recognition. So, although olfactory cues do not appear to be as species-specific as visual cues, their function as alerting stimuli may not require such fine-tuning. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 555–572.     

Song Choice Is Modulated by Female Movement in Drosophila Males

Mate selection is critical to ensuring the survival of a species. In the fruit fly, Drosophila melanogaster, genetic and anatomical studies have focused on mate recognition and courtship initiation for decades. This model system has proven to be highly amenable for the study of neural systems controlling the decision making process. However, much less is known about how courtship quality is regulated in a temporally dynamic manner in males and how a female assesses male performance as she makes her decision of whether to accept copulation. Here, we report that the courting male dynamically adjusts the relative proportions of the song components, pulse song or sine song, by assessing female locomotion. Male flies deficient for olfaction failed to perform the locomotion-dependent song modulation, indicating that olfactory cues provide essential information regarding proximity to the target female. Olfactory mutant males also showed lower copulation success when paired with wild-type females, suggesting that the male’s ability to temporally control song significantly affects female mating receptivity. These results depict the consecutive inter-sex behavioral decisions, in which a male smells the close proximity of a female as an indication of her increased receptivity and accordingly coordinates his song choice, which then enhances the probability of his successful copulation.     

Responses of Cyprinodon maya and C. labiosus females to visual and olfactory cues of conspecific and heterospecific males

Premating isolating mechanisms, based on visual and olfactory cues, were studied in two members of a young species flock which is endemic to Lake Chichancanab in Mexico. The two species, Cyprinodon maya and C. labiosus, differ in morphological traits that may be associated with trophic differentiation, but show little genetic change. Female C. maya strongly preferred conspecific males over C. labiosus males, based on visual as well as olfactory cues. C. labiosus females discriminated between conspecific and heterospecific males based on olfactory cues but not visual ones. Asymmetries in the strength of female preferences for conspecific males in this species pair suggest that mate recognition systems based on visual and olfactory cues evolve at different rates and track the degree of genetic differentiation.     

Female mate choice across mating stages and between sequential mates in flour beetles

Few studies have examined how female premating choice correlates with the outcome of copulatory and post-copulatory processes. It has been shown that polyandrous Tribolium castaneum females discriminate among males before mating based on olfactory cues, and also exert cryptic choice during mating through several mechanisms. This study tested whether a male's relative attractiveness predicted his insemination success during copulation. Bioassays with male olfactory cues were used to rank two males as more and less attractive to females; each female was then mated to either her more attractive male followed by less attractive male, or vice versa. Dissections immediately after second copulations revealed a significantly higher percent of successful inseminations for females that remated with more attractive males compared with those that remated with less attractive males. These results indicate that cryptic female choice during copulation reinforces precopulatory female choice in T. castaneum, and suggest that females could use cryptic choice to trade up to more attractive males, possibly gaining better phenotypic or genetic quality of sires.     

Female preferences based on olfactory cues in the guppy (Poecilia reticulata)

Guppies are highly sexually dimorphic and females have been shown to mate preferentially with males with various visible traits. Guppies, however, have been shown to respond behaviourally to odour cues from conspecifics. Using a specially designed olfactory choice tank, we tested whether females (1) could detect other guppies on the basis of their olfactory cues alone, (2) preferred to associate with males or with females and (3) could distinguish between different males. Female guppies were found to associate preferentially with other guppies when given a choice between water containing cues from another fish and water containing no cues. When females were presented with olfactory cues from a male or a female, they preferred the female initially but most then reversed their decision and swam to the male. Females associated preferentially with certain males based upon olfactory cues alone. Males, however, preferred on the basis of olfactory cues were the least preferred for visual cues.     

Premating Avoidance of Inbreeding Absent in Female Guppies (Poecilia reticulata)

The recognition and avoidance of kin during mating can be an important means of reducing the potential for inbreeding depression in offspring. We report here that premating mechanisms to avoid inbreeding, either innate or learnt through juvenile experience, are at best weak in female guppies (Poecilia reticulata). Guppies are small, ovoviviparous, neo‐tropical freshwater fish, with a polygamous mating system where males actively court females and females are selective of their mates. In a series of mate‐choice experiments, naïve, virgin females of the Quare River population in Trinidad were given a choice between a brother and a non‐sib male from the same population. Initially, females were only provided olfactory cues upon which to base their choice and then subsequently both olfactory and visual cues. Despite the females displaying mate choice, we found no evidence of them discriminating between the male types in either experiment. There was thus no indication of inbreeding avoidance, suggesting that experiences after maturation or with mature males (e.g. rare male preference), dispersal and/or post‐mating mechanisms may be evolutionarily more important avoidance mechanisms.     

Sex differences in dogfish behaviour: alternative activity patterns and habitat choice

Guppies are highly sexually dimorphic and females have been shown to mate preferentially with males with various visible traits. Guppies, however, have been shown to respond behaviourally to odour cues from conspecifics. Using a specially designed olfactory choice tank, we tested whether females (1) could detect other guppies on the basis of their olfactory cues alone, (2) preferred to associate with males or with females and (3) could distinguish between different males. Female guppies were found to associate preferentially with other guppies when given a choice between water containing cues from another fish and water containing no cues. When females were presented with olfactory cues from a male or a female, they preferred the female initially but most then reversed their decision and swam to the male. Females associated preferentially with certain males based upon olfactory cues alone. Males, however, preferred on the basis of olfactory cues were the least preferred for visual cues.     

Pheromones and body coloration affect mate recognition in the Japanese nine-spotted moth Amata fortunei (Lepidoptera: Arctiidae)

Adults of the Japanese nine-spotted moth, Amata fortunei, are diurnal and have white-spotted black wings and a black-and-yellow striped body pattern. We evaluated whether this species uses sex pheromones and whether visual cues from the female body are used in mate recognition. We introduced extracts of potentially scent-bearing abdominal tips of females to males. Males responded more to the extracts than to dried female specimens, suggesting the presence of sex pheromones in the extracts. Indeed, no males responded to the dried female specimens. To evaluate the importance of visual cues, we conducted the experiments with crude extract and an additional model stimulant. Males responded more to model females with the same number and similar area of yellow bands to the original conspecific females than to those with more bands and greater total band area, suggesting that dissimilarity in band number and area to conspecific females could interrupt male mating behavior. Males of A. fortunei likely find mating partners using olfactory cues over relatively long distances, while using both olfactory and visual cues over short distances. These results suggest that olfactory cues play a major role in mate recognition, whereas visual cues play a supplementary role.     

Sex recognition by odour and variation in the uropygial gland secretion in starlings

1.?Although a growing body of evidence supports that olfaction based on chemical compounds emitted by birds may play a role in individual recognition, the possible role of chemical cues in sexual selection of birds has been only preliminarily studied. 2.?We investigated for the first time whether a passerine bird, the spotless starling Sturnus unicolor, was able to discriminate the sex of conspecifics by using olfactory cues and whether the size and secretion composition of the uropygial gland convey information on sex, age and reproductive status in this species. 3.?We performed a blind choice experiment during mating, and we found that starlings were able to discriminate the sex of conspecifics by using chemical cues alone. Both male and female starlings preferred male scents. Furthermore, the analysis of the chemical composition of the uropygial gland secretion by using gas chromatography-mass spectrometry (GC-MS) revealed differences between sexes, ages and reproductive status. 4.?In conclusion, our study reveals for first time that a passerine species can discriminate the sex of conspecifics by relying on chemical cues and suggests that the uropygial gland secretion may potentially function as a chemical signal used in mate choice and/or intrasexual competition in this species.