Differential use of sensory information in sexual behavior as a function of gender

Olfactory information is critical to mammalian sexual behavior. Based on parental investment theory the relative importance of olfaction compared with vision, touch, and hearing should be different for human males and females. In particular, because of its link to immunological profile and offspring viability, odor should be a more important determinant of sexual choice and arousal for females than for males. To test this hypothesis a questionnaire was developed and administered to 332 adults (166 males, 166 females). Subjects used a 1–7 scale to indicate how much they agreed with a series of statements concerning the importance of olfactory, visual, auditory, and tactile information for their sexual responsivity. The data reveal that males rated visual and olfactory information as being equally important for selecting a lover, while females considered olfactory information to be the single most important variable in mate choice. Additionally, when considering sexual activity, females singled out body odor from all other sensory experiences as most able to negatively affect desire, while males regarded odors as much more neutral stimuli for sexual arousal. The present results support recent findings in mice and humans concerning the relation of female preferences in body odor and major histocompatibility complex (MHC) compatibility and can be explained by an evolutionary analysis of sex differences in reproductive strategies. This work represents the first direct examination of the role of different forms of sensory information in human sexual behavior.     

Cross-modal associations of human body odour attractiveness with facial and vocal attractiveness provide little support for the backup signals hypothesis: A systematic review and meta-analysis

Assessing the attractiveness of potential mating partners typically involves multiple sensory modalities, including the integration of olfactory, visual, and auditory cues. However, predictions diverge on how the individual modalities should relate to each other. According to the backup signals hypothesis, multimodal cues provide redundant information, whereas the multiple messages hypothesis suggests that different modalities provide independent and distinct information about an individual's mating-related quality. The backup signals hypothesis predicts a positive association between assessments based on different modalities, whereas no substantial correlation across modalities is expected under the multiple messageshypothesis. Previous studies testing the two hypotheses have provided mixed results, and a systematic evaluation is currently missing.We performed a systematic review and a meta-analysis of published and unpublished studies to examine the congruence in assessments between human body odour and facial attractiveness, and between body odour and vocal attractiveness. We found positive but weak associations between ratings of body odours and faces (r = 0.1, k = 25), and between body odours and voices (r = 0.1, k = 9). No sex differences were observed in the magnitude of effects.Compared to judgments of facial and vocal attractiveness, our results suggest that assessment of body odour provides independent and non-redundant information about human mating-related quality. Our findings thus provide little support for the backup signals hypothesis and may be better explained by the multiple messages hypothesis.     

The use of chemical and visual cues in female choice in the butterfly Bicyclus anynana

Investigating the relative importance of multiple cues for mate choice within a species may highlight possible mechanisms that led to the diversification of closely related species in the past. Here, we investigate the importance of close-range pheromones produced by male Bicyclus anynana butterflies and determine the relative importance of these chemical cues versus visual cues in sexual selection by female choice. We first blocked putative androconial organs on the fore- and hindwings of males, while also manipulating the ability of females to perceive chemical signals via their antenna. We found that male chemical signals were emitted by both fore- and hindwing pairs and that they play an important role in female choice. We subsequently tested the relative importance of these chemical cues versus visual cues, previously identified for this species, and found that they play an equally important role in female choice in our laboratory setting. In addition, females will mate with males with only one signal present and blocking both androconial organs on males seems to interfere with male to male recognition. We discuss the possible functions of these signals and how this bimodal system may be used in intra- and interspecific mate evaluation.     

Male mate choice relies on major histocompatibility complex class I in a sex‐role‐reversed pipefish

Mate choice for compatible genes is often based on genes of the major histocompatibility complex (MHC). Although MHC‐based mate choice is commonly observed in female choice, male mate choice remains elusive. In particular, if males have intense paternal care and are thus the choosing sex, male choice for females with dissimilar MHC can be expected. Here, we investigated whether male mate choice relies on MHC class I genes in the sex‐role reversed pipefish Syngnathus typhle. In a mate choice experiment, we determined the relative importance of visual and olfactory cues by manipulating visibility and olfaction. We found that pipefish males chose females that maximize sequence‐based amino acid distance between MHC class I genotypes in the offspring when olfactory cues were present. Under visual cues, large females were chosen, but in the absence of visual cues, the choice pattern was reversed. The use of sex‐role reversed species thus revealed that sexual selection can lead to the evolution of male mate choice for MHC class I genes.     

Prosimian sensory capacities

This paper reviews laboratory research on sensory capacities of prosimians. Most investigations to date have concentrated on visual and auditory sensitivity with relatively little attention directed toward olfactory and gustatory sensitivity. Diurnal prosimians have at least rudimentary color vision and appear deficient to anthropoids in other visual measures such as acuity. The most striking difference between prosimian and anthropoid auditory sensitivity is the increased sensitivity of the former group to high frequencies. No psychophysical data have been published on olfactory sensitivity of prosimians, but the relatively large olfactory areas in their brains and their propensity for scent marking strongly suggest that they have acute olfactory sensitivity. Most data on gustatory thresholds in prosimians does not permit sensitivity estimation since the data are joint functions of sensitivity as well as preferences.     

Variation in female guppy preference for male olfactory and visual traits

Animals often use different sensory systems to assess different sexually selected signals from potential mates. However, the relative importance of different signals on mate choice is not well understood in many animal species. In this study, we examined the relative importance of male olfactory and visual cues on female preference in the guppy Poecilia reticulata. We used digitally modified male images to standardize visual stimuli. We found that, regardless of whether females were presented without male visual stimuli or with identical male visual stimuli, they preferred stimuli with the odor of males to those without. However, when females were allowed to choose between dull male visual stimuli with male odor, and brightly colored male visual stimuli without male odor, there was no clear preference for either. Some females preferred the dull male visual stimuli with male odor, whereas some other females preferred the brightly colored male visual stimuli without male odor. These results indicate that the relative importance of olfactory and visual cues in female mate preference varied between individuals.     

Sexual partner preference requires a functional aromatase (cyp19) gene in male mice

Sexual motivation, sexual partner preference, and sexual performance represent three different aspects of sexual behavior that are critical in determining the reproductive success of a species. Although the display of sexual behavior is under strict hormonal control in both sexes, the relative roles of androgen and estrogen receptors in activating the various components of male sexual behavior are still largely unknown. A recently developed mouse model that is deficient in estradiol due to targeted disruption of exons 1 and 2 of the Cyp19 gene (aromatase knockout (ArKO) mice) was used here to analyze the role of estradiol in the control of all three aspects of male sexual behavior. When tested in a Y-maze providing volatile olfactory cues, male ArKO mice did not show a preference for the odors from an estrous female over those from an intact male, whereas wild-type (WT) and heterozygous (HET) males clearly preferred to sniff estrous odors. When provided with visual and olfactory cues, male ArKO mice also failed to show a preference for an estrous female when given a choice between an estrous female and an empty arm. However, sexual partner preferences of male ArKO mice were not sex-reversed: they did not prefer to investigate an intact male over an estrous female or empty arm. Thus, male ArKO mice seemed to have general deficits in discriminating between conspecifics by using olfactory and visual cues. Male coital behavior was also severely impaired in male ArKO mice: they displayed significantly fewer mounts, intromissions, and ejaculations than WT and HET males. Latencies to first mount or intromission were also significantly longer in ArKO males compared to WT and HET males, in addition to them showing less interest in investigating olfactory and visual cues in a Y-maze, suggesting that they were sexually less motivated. However, three out of seven male ArKO mice were capable of siring litters provided they were housed with a female for a prolonged period of time. In conclusion, aromatization of testosterone to estradiol appears to be essential for sexual motivation and sexual partner preference. By contrast, estradiol may play only a limited role in the expression of male coital behaviors.     

Olfactory attractiveness of flowering plants to the parasitoid Microplitis mediator: potential implications for biological control

In agricultural landscapes, the lack of floral nectar can be a major difficulty for nectar feeding parasitoids. This problem can be reduced by the addition of suitable wildflowers. To date, flowers have mainly been studied in terms of effects on parasitoid fitness, not taking into account the essential role of flower attractiveness for foraging parasitoids. This study experimentally tested the olfactory attractiveness of five wildflowers (bishop’s weed, cornflower, buckwheat, candytuft, and oregano) to the parasitoid Microplitis mediator (Haliday) (Hymenoptera: Braconidae). We conducted choice experiments in a Y-tube olfactometer to test the attractiveness of flowers against air, and relative attractiveness in paired choice tests. Our results showed that all the flowers were highly attractive and that in paired choice tests cornflower and candytuft were equally attractive and more attractive than buckwheat. These results indicate that M. mediator has evolved innate preferences that could be effectively exploited in biological control.     

Behavioural plasticity and sex differences in host finding of a specialized bee species

Many animals feed on flowers, and visual as well as olfactory cues are considered as most important mediators in animal–plant interactions. However, the relative importance of these cues is not well understood. Bees are the most important animal pollinators worldwide and here, we determined the importance of decoupled and combined visual and olfactory cues of Lysimachia punctata (Primulaceae) for host plant location in both sexes of the specialized, solitary bee, Macropis fulvipes (Melittidae). Lysimachia-inexperienced female bees preferred olfactory over visual cues though visual cues increased the attractiveness of olfactory ones. In experienced females, the importance of visual cues was increased. Both Lysimachia-naive and -experienced males relied more on visual cues as compared to females. This study demonstrates that the relative weighting of cues used for host plant finding depends on the sex and experience of M. fulvipes. The latter finding reveals the presence of learning-induced behavioural plasticity in host plant finding for a bee species. It may allow the bee to forage highly efficient. Visually guided female detection on flowers by males is a likely functional explanation for the differences in the weighting of visual and olfactory cues between the sexes.     

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.     

The relative importance of the face and body in judgments of human physical attractiveness

A number of traits have been proposed to be important in human mate choice decisions. However, relatively little work has been conducted to determine the relative importance of these traits. In this study, we assessed the relative importance of the face and body in judgments of human physical attractiveness. One hundred twenty-seven men and 133 women were shown images of 10 individuals of the opposite sex. Participants rated the images for their attractiveness for either a short-term relationship or a long-term relationship. Images of the face and the body were rated independently before participants were shown and asked to rate the combined face and body images. Face ratings were found to be the best predictor of the ratings of combined images for both sexes and for both relationship types. Females showed no difference in ratings between short- and long-term conditions, but male ratings of female bodies became relatively more important for a short-term relationship compared with a long-term relationship. Results suggest that faces and bodies may be signaling different information about potential mates.     

Partner choice creates fairness in humans

Many studies demonstrate that partner choice has played an important role in the evolution of human cooperation, but little work has tested its impact on the evolution of human fairness. In experiments involving divisions of money, people become either over-generous or over-selfish when they are in competition to be chosen as cooperative partners. Hence, it is difficult to see how partner choice could result in the evolution of fair, equal divisions. Here, we show that this puzzle can be solved if we consider the outside options on which partner choice operates. We conduct a behavioural experiment, run agent-based simulations and analyse a game-theoretic model to understand how outside options affect partner choice and fairness. All support the conclusion that partner choice leads to fairness only when individuals have equal outside options. We discuss how this condition has been met in our evolutionary history, and the implications of these findings for our understanding of other aspects of fairness less specific than preferences for equal divisions of resources.     

Smelling right: the scent of male lemurs advertises genetic quality and relatedness

Sexual selection theory predicts that competitors or potential mates signal their quality or relatedness to conspecifics. Researchers have focused on visual or auditory modes of signal transmission; however, the importance of olfactory indicators is gaining recognition. Using a primate model and a new integrative analytical approach, we provide the first evidence relating male olfactory cues to individual genome-wide heterozygosity and to the genetic distance between individuals. The relationships between male semiochemical profiles and genetic characteristics are apparent only during the highly competitive and stressful breeding season. As heterozygosity accurately predicts health and survivorship in this population, we identify scrotal olfactory cues as honest indicators of male quality, with relevance possibly to both sexes. Beyond showing that semiochemicals could underlie kin recognition and nepotism, we provide a putative olfactory mechanism to guide male–male competition and female mate choice.     

Visible skin color distribution plays a role in the perception of age, attractiveness, and health in female faces

Evolutionary psychologists have proposed that preferences for facial characteristics, such as symmetry, averageness, and sexual dimorphism, may reflect adaptations for mate choice because they signal aspects of mate quality. Here, we show that facial skin color distribution significantly influences the perception of age and attractiveness of female faces, independent of facial form and skin surface topography. A set of three-dimensional shape-standardized stimulus faces—varying only in terms of skin color distribution due to variation in biological age and cumulative photodamage—was rated by a panel of naive judges for a variety of perceptual endpoints relating to age, health, and beauty. Shape- and topography-standardized stimulus faces with the homogeneous skin color distribution of young people were perceived as younger and received significantly higher ratings for attractiveness and health than analogous stimuli with the relatively inhomogeneous skin color distribution of more elderly people. Thus, skin color distribution, independent of facial form and skin surface topography, seems to have a major influence on the perception of female facial age and judgments of attractiveness and health as they may signal aspects of underlying physiological condition of an individual relevant for mate choice. We suggest that studies on human physical attractiveness and its perception need to consider the influence of visible skin condition driven by color distribution and differentiate between such effects and beauty-related traits due to facial shape and skin topography.     

Multimodal Floral Signals and Moth Foraging Decisions

Background

Combinations of floral traits – which operate as attractive signals to pollinators – act on multiple sensory modalities. For Manduca sexta hawkmoths, how learning modifies foraging decisions in response to those traits remains untested, and the contribution of visual and olfactory floral displays on behavior remains unclear.

Methodology/Principal Findings

Using M. sexta and the floral traits of two important nectar resources in southwestern USA, Datura wrightii and Agave palmeri, we examined the relative importance of olfactory and visual signals. Natural visual and olfactory cues from D. wrightii and A. palmeri flowers permits testing the cues at their native intensities and composition – a contrast to many studies that have used artificial stimuli (essential oils, single odorants) that are less ecologically relevant. Results from a series of two-choice assays where the olfactory and visual floral displays were manipulated showed that naïve hawkmoths preferred flowers displaying both olfactory and visual cues. Furthermore, experiments using A. palmeri flowers – a species that is not very attractive to hawkmoths – showed that the visual and olfactory displays did not have synergistic effects. The combination of olfactory and visual display of D. wrightii, however – a flower that is highly attractive to naïve hawkmoths – did influence the time moths spent feeding from the flowers. The importance of the olfactory and visual signals were further demonstrated in learning experiments in which experienced moths, when exposed to uncoupled floral displays, ultimately chose flowers based on the previously experienced olfactory, and not visual, signals. These moths, however, had significantly longer decision times than moths exposed to coupled floral displays.

Conclusions/Significance

These results highlight the importance of specific sensory modalities for foraging hawkmoths while also suggesting that they learn the floral displays as combinatorial signals and use the integrated floral traits from their memory traces to mediate future foraging decisions.     

Sexual Conflict and Gender Gap Effects: Associations between Social Context and Sex on Rated Attractiveness and Economic Status

Human mate choice research often concerns sex differences in the importance of traits such as physical attractiveness and social status. A growing number of studies indicate that cues to social context, including other people who appear in stimulus photographs, can alter that individual’s attractiveness. Fewer studies, however, consider judgements of traits other than physical attractiveness, such as wealth. Here we manipulate the presence/absence of other people in photographs of target models, and test the effects on judgments of both attractiveness and earnings (a proxy for status). Participants (N = 2044) rated either male or female models for either physical attractiveness or social/economic status when presented alone, with same sex others or with opposite sex others. We collectively refer to this manipulation as ‘social context’. Male and female models received similar responses for physical attractiveness, but social context affected ratings of status differently for women and men. Males presented alongside other men received the highest status ratings while females presented alone were given the highest status ratings. Further, the status of females presented alongside a male was constrained by the rated status of that male. Our results suggests that high status may not directly lead to high attractiveness in men, but that status is more readily attributed to men than to women. This divide in status between the sexes is very clear when men and women are presented together, possibly reflecting one underlying mechanism of the modern day gender gap and sexist attitudes to women’s economic participation. This adds complexity to our understanding of the relationship between attractiveness, status, and sex in the light of parental investment theory, sexual conflict and economic theory.     

Partner choice in Gobiid fish Myersina macrostoma living in association with the alpheid shrimp Alpheus rapax

Partner choice is an important selective force in mutualistic partnerships. Although several aspects of mutualism have been well-studied, partner choice remains a novel aspect in the study of marine mutualists. Previous research on the goby-shrimp mutualism suggested that visual cues affect the ability of gobies to discriminate between potential shrimp partners but small sample sizes limited the generalization of that result. Here, primary partner choice in Myersina macrostoma was investigated in a series of ex situ experiments. Results indicated that shrimp-associated gobies relied on visual cues in partner choice. The goby M. macrostoma was clearly able to discern between different shelter types, demonstrating a preference for burrows compared to rocks. While they were attracted to larger burrows, they were not visually attracted to larger shrimp partners. This indicates that in wild populations, intraspecific competition for larger burrows might be the driving factor in size assortment in associated partners. Myersina macrostoma could also discern between species of shrimps in laboratory experimental set-ups, indicating a clear preference for A. rapax which they naturally occur with, but not to A. lobidens, which occurs at the same locality but with which they do not naturally associate. These findings offer fundamental building blocks towards the broader understanding of partnership formations in marine mutualists.     

Ovulatory Shifts in Women��s Attractions to Primary Partners and Other Men: Further Evidence of the Importance of Primary Partner Sexual Attractiveness

Previous research has documented shifts in women’s attractions to their romantic partner and to men other than their partner across the ovulation cycle, contingent on the degree to which her partner displays hypothesized indicators of high-fitness genes. The current study set out to replicate and extend this finding. Forty-one couples in which the woman was naturally cycling participated. Female partners reported their feelings of in-pair attraction and extra-pair attraction on two occasions, once on a low-fertility day of the cycle and once on a high-fertility day of the cycle just prior to ovulation. Ovulation was confirmed using luteinizing hormone tests. We collected two measures of male partner sexual attractiveness. First, the women in the study rated their partner’s sexual attractiveness. Second, we photographed the partners and had the photos independently rated for attractiveness. Shifts in women’s in-pair attractions across the cycle were significantly moderated by women’s ratings of partner sexual attractiveness, such that the less sexually attractive women rated their partner, the less in-pair attraction they reported at high fertility compared with low fertility (partial r = .37, p _dir = .01). Shifts in women’s extra-pair attractions across the cycle were significantly moderated by third-party ratings of partner attractiveness, such that the less attractive the partner was, the more extra-pair attraction women reported at high relative to low fertility (partial r = −.33, p _dir = .03). In line with previous findings, we found support for the hypothesis that the degree to which a woman’s romantic partner displays indicators of high-fitness genes affects women’s attractions to their own partner and other men at high fertility.     

Divergence of premating behaviors in the closely related species Drosophila subquinaria and D. recens

Most animal species use distinctive courship patterns to choose among potential mates. Over time, the sensory signaling and preferences used during courtship can diverge among groups that are reproductively isolated. This divergence of signal traits and preferences is thought to be an important cause of behavioral isolation during the speciation process. Here, we examine the sensory modalities used in courtship by two closely related species, Drosophila subquinaria and Drosophila recens, which overlap in geographic range and are incompletely reproductively isolated. We use observational studies of courtship patterns and manipulation of male and female sensory modalities to determine the relative roles of visual, olfactory, gustatory, and auditory signals during conspecific mate choice. We find that sex‐specific, species‐specific, and population‐specific cues are used during mate acquisition within populations of D. subquinaria and D. recens. We identify shifts in both male and female sensory modalities between species, and also between populations of D. subquinaria. Our results indicate that divergence in mating signals and preferences have occurred on a relatively short timescale within and between these species. Finally, we suggest that because olfactory cues are essential for D. subquinaria females to mate within species, they may also underlie variation in behavioral discrimination across populations and species.     

Fisherian flies: benefits of female choice in a lekking sandfly

We experimentally investigated the fitness consequences of female mate choice in order to test the relative importance of three competing but non-exclusive hypotheses for the maintenance of pronounced female mating preferences on leks: that females benefit directly; that they gain indirect Fisherian benefits by producing more attractive sons; or that they benefit indirectly because preferred males possess ''good genes'' that confer increased viability on their sons and daughters. We allowed lekking female sandflies, Lutzomyia longipalpis, to choose between males of varying attractiveness to females, and monitored the consequences for their own survival and reproductive success as well as for their offspring. In contrast to the predictions of the direct-benefits model, we found no clear sire effect on the fecundity or survival of the females themselves; females mating with more attractive males did survive longer after oviposition, but never long enough to undertake a second batch of egg laying. We also found no evidence that females gained good-genes benefits in terms of enhanced offspring survival. However, we did find that generally attractive males fathered sons who were then chosen when they in turn formed leks. Although not completely precluding other benefits, our results indicate that Fisherian benefits are at least partly responsible for maintaining female choice at L. longipalpis leks. These findings indicate the importance of testing all putative benefits concurrently in exploring the maintenance of female mate choice.