Female Sexual Signals Research Articles

Female blue tits sing frequently: a sex comparison of occurrence, context, and structure of song.

In species with mutual mate choice, we should expect adaptive signaling in both sexes. However, the role of female sexual signals is generally understudied. A case in point is female birdsong that has received considerably less attention than male song. This holds even for well-studied species such as the blue tit (Cyanistes caeruleus), an important model in evolutionary ecology. Although there have been anecdotal reports of female song from three populations, there are no quantitative studies on female song in this species. Here, we report systematic sampling from a population of individually marked blue tits over 3 years, revealing that females sang frequently throughout the sampling period. Notably, daytime singing of females occurred in functionally similar contexts as in males (agonistic, solo song, and alarm contexts) but females had lower song output than males and were not observed singing dawn song, while males showed long singing displays at dawn before copulations take place. Female and male song overlapped substantially in acoustic structure (i.e., same song types or peak frequency) but females had smaller individual song-type repertoires, shorter trills, and lower vocal consistency. Differential selection pressures related to functional differences in male and female song might explain the observed variation in acoustic structure. With the first quantitative study of female song in such a well-studied species, we hope to stimulate further investigations into the functions of female singing, especially in the Northern temperate zones where female song may have been overlooked, not only in this but perhaps in other monomorphic species.

Geographic variation in sexual communication in the cotton bollworm, Helicoverpa armigera.

BACKGROUNDGeographic variation in male response to sex pheromone lures has been studied in the field in a number of moth species. However, only a few studies have investigated geographic variation in female calling and sex pheromone under field conditions. For an effective field implementation of sex pheromone lures, it is essential to know the local sex pheromone blend and local timing of sexual communication. We investigated the level and extent of geographic variation in the sexual communication of the important agricultural pest Helicoverpa armigera (Lepidoptera, Noctuidae) in three continents.RESULTSWe found there is no genetic variation in the calling behavior of H. armigera. In the female sex pheromone, we found more between‐population variation than within‐population variation. In male response experiments, we found geographic variation as well. Strikingly, when adding the antagonistic compound Z11‐16:OAc to the pheromone blend of H. armigera, significantly fewer males were caught in Australia and China, but not in Spain. This variation is likely not only due to local environmental conditions, such as photoperiod and temperature, but also to the presence of other closely related species with which communication interference may occur.ConclusionFinding geographic variation in both the female sexual signal and the male response in this pest calls for region‐specific pheromone lures. Our study shows that the analysis of geographic variation in moth female sex pheromones as well as male responses is important for effectively monitoring pest species that occur around the globe. © 2020 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

On the evolution of visual female sexual signalling.

A long-standing evolutionary puzzle surrounds female sexual signals visible around the time of ovulation. Even among just primates, why do some species have substantial sexual swellings and/or bright colorations visible around females' genital regions, while other species are like humans, with no signs of ovulation visible? What is the evolutionary purpose behind not just these signs, but also this great variation seen among species? Here, we examine the evolutionary trade-offs associated with visual ovulation signalling using agent-based modelling. Our model predicts how various factors, including male genetic heterogeneity and reproductive inequality, female physiological costs, group size, and the weighting of genetic versus non-genetic benefits coming from males, each influence the strength of ovulation signalling. Our model also predicts that increasing the impacts of infanticide will increase ovulation signalling. We use comparative primate data to show that, as predicted by our model, larger group size and higher risk of infanticide each correlate with having stronger visual ovulation signs. Overall, our work resolves some old controversies and sheds new light on the evolution of visual female sexual signalling.

Nonadaptive female pursuit of extrapair copulations can evolve through hitchhiking.

Mounting evidence has indicated that engaging in extrapair copulations (EPCs) might be maladaptive or detrimental to females. It is unclear why such nonadaptive female behavior evolves. In this study, we test two hypotheses about the evolution of female EPC behavior using population genetic models. First, we find that both male preference for allocating extra effort to seek EPCs and female pursuit behavior without costs can be maintained and remain polymorphic in a population via frequency‐dependent selection. However, both behaviors cannot evolve when females with pursuit behavior suffer from a decline in male parental care. Second, we present another novel way in which female pursuit behavior can evolve; indirect selection can act on this behavior through a ratchet‐like mechanism involving oscillating linkage disequilibria between the target EPC pursuit locus and two other loci determining male mate choice and a female sexual signal. Although the overall positive force of such indirect selection is relatively weak, our results suggest that it may still play a role in promoting the evolution of female EPC behavior when this behavior is nonadaptive (i.e., it is neutral) or only somewhat maladaptive (e.g., males only occasionally lower parental care when their mates pursue EPCs).

Arching the Back (Lumbar Curvature) as a Female Sexual Proceptivity Signal: an Eye-Tracking Study

It is common in studies of human mate preference to have participants judge the attractiveness of photographs in which models adopt a neutral facial expression or a neutral body posture. However, i ...

Sex-specific consequences of an induced immune response on reproduction in a moth.

BackgroundImmune response induction benefits insects in combatting infection by pathogens. However, organisms have a limited amount of resources available and face the dilemma of partitioning resources between immunity and other life-history traits. Since males and females differ in their life histories, sex-specific resource investment strategies to achieve an optimal immune response following an infection can be expected. We investigated immune response induction of females and males of Heliothis virescens in response to the entomopathogenic bacterium Serratia entomophila, and its effects on mating success and the female sexual signal.ResultsWe found that females had higher expression levels of immune-related genes after bacterial challenge than males. However, males maintained a higher baseline expression of immune-related genes than females. The increased investment in immunity of female moths was negatively correlated with mating success and the female sexual signal. Male mating success was unaffected by bacterial challenge.ConclusionsOur results show that the sexes differed in their investment strategies: females invested in immune defense after a bacterial challenge, indicating facultative immune deployment, whereas males had higher baseline immunity than females, indicating immune maintenance. Interestingly, these differences in investment were reflected in the mate choice assays. As female moths are the sexual signallers, females need to invest resources in their attractiveness. However, female moths appeared to invest in immunity at the cost of reproductive effort.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0562-3) contains supplementary material, which is available to authorized users.

Multimodal Advertisement of Pregnancy in Free-Ranging Female Japanese Macaques (Macaca fuscata).

The role of multiple sexual signals in indicating the timing of female ovulation, and discrimination of this timing by males, has been particularly well studied among primates. However the exhibition of pregnancy signals, and how such signals might modulate male post-conception mating decisions, is still poorly understood. Here we aimed to determine if Japanese macaque males use changes in female sexual signals (behavioral, visual and auditory) to discriminate pregnancy and adjust their socio-sexual behaviors. We combined behavioral observations, digital photography and endocrinological (progestogen and estrogen) data, collected systematically during three one-month periods: the pre-conceptive period, the 1st month of pregnancy and the 2nd month of pregnancy. We analyzed variation in the probability of detecting male and female socio-sexual behaviors and estrus calls, as well as changes in female face color parameters, in relation to female reproductive state. Based on our focal observations, we found that males did not copulate during the pregnancy period, and that female socio-sexual behaviors generally decreased from the pre-conceptive to post-conceptive periods. Female face luminance decreased from the pre-conceptive month to the pregnancy period whereas face color only varied between the 1st and 2nd month of gestation. Our results suggest that Japanese macaque females display sexual cues of pregnancy that males might use to reduce energy wasted on non-reproductive copulations with pregnant females. We hypothesize that females advertize their pregnancy through changes in behavioral, visual and potential auditory signals that males can use to adjust their mating behaviors. We finish by discussing implications for male and female post-conception strategies.

Female behavioral proceptivity functions as a probabilistic signal of fertility, not female quality, in a New World primate

The interests of males and females in mating contexts often conflict, and identifying the information conveyed by sexual signals is central to understanding how signalers manage such conflicts. Research into the information provided by female primate sexual signals has focused on exaggerated anogenital swellings as either reliable-indicators of reproductive quality (reliable-indicator hypothesis) or probabilistic signals of fertility (graded-signal hypothesis). While these morphological signals are mostly confined to catarrhine primates, these hypotheses are potentially widely applicable across primates, but have not been tested in taxa that lack such morphological signals. Here, we tested these hypotheses in wild black capuchins (Sapajus nigritus), a species in which females lack morphological sexual signals but produce conspicuous behavioral estrous displays. Specifically, we examined the proportion of time different females spent producing these signals with respect to measures of female quality (dominance rank, parity, age-related fecundity and cycle type) and in relation to the timing of fertility, as determined by analysis of fecal progesterone. Time spent displaying did not vary across females based on measures of female quality, but increased with the approach of ovulation. Further, male mating effort varied according to the timing of female fertility. Proceptive behaviors in this species thus meet predictions of the graded-signal hypothesis, providing the first support for this hypothesis based solely on behavioral signals.

Intraspecific Variation in Female Sex Pheromone of the Codling Moth Cydia pomonella.

The codling moth, Cydia pomonella L. (Lepidoptera, Tortricidae), is a major pest of apple, pear and walnut orchards worldwide. This pest is often controlled using the biologically friendly control method known as pheromone-based mating disruption. Mating disruption likely exerts selection on the sexual communication system of codling moth, as male and female moths will persist in their attempt to meet and mate. Surprisingly little is known on the intraspecific variation of sexual communication in this species. We started an investigation to determine the level of individual variation in the female sex pheromone composition of this moth and whether variation among different populations might be correlated with use of mating disruption against those populations. By extracting pheromone glands of individual females from a laboratory population in Canada and from populations from apple orchards in Spain and Italy, we found significant between- and within-population variation. Comparing females that had been exposed to mating disruption, or not, revealed a significant difference in sex pheromone composition for two of the minor components. Overall, the intraspecific variation observed shows the potential for a shift in female sexual signal when selection pressure is high, as is the case with continuous use of mating disruption.

Multimodal signalling of ovulation in human and non-human primates

Communication in primates is based on multiple elements of signals, often expressed in different modalities. While some individual primate signals are relatively well described for a particular cue (e.g. copulation calls, sexual swellings) or for one specific dimension of a signal (e.g. the size of sexual swellings), few studies have simultaneously investigated the role of multiple signals and cues in the same communicative context. This paper reviews comparative evidence on primate sexual communication, specifically concerning multimodal sexual signalling of ovulation and mating strategies. A comparison is made across primate species, including humans, of the characteristics of different female sexual cues and signals (behavioural, visual, auditory and olfactory) and of their potential roles in the discrimination of the timing of ovulation. The possible selective reasons for such multimodal signalling are discussed.

Similar differentiation patterns between PBP expression levels and pheromone component ratios in two populations of Sesamia nonagrioides.

Pheromone-binding proteins (PBPs) are thought to contribute to the specificity of the pheromone detection system through an initial selective binding with pheromone molecules. Here, we report different expression levels of PBP transcripts in the antennae of two populations of the stemborer Sesamia nonagrioides (Lepidoptera: Noctuidae), one collected in Europe and one in sub-Saharan Africa. The three PBP transcripts previously identified in this species were found to be expressed in both male and female antennae. Whereas PBP3 did not show any differential expression, PBP1 and PBP2 appeared to be expressed differently according to the population origin and sex. Simultaneously, we measured and compared the ratio of the three components of the S. nonagrioides pheromone blend (Z11-16:Ac; Z11-16:OH; Z11-16:Ald) in females of the two populations. The ratio of Z11-16:OH and Z11-16:Ald varied significantly according to the population origin of this species. Cluster analyses revealed similar differentiation patterns between PBP1 and PBP2 expression levels and the ratios of Z11-16:OH and Z11-16:Ald. Different female sexual signals may thus correspond to different male reception systems, which are adjusted by the PBP expression levels, thereby ensuring optimal communication within populations.

Social Information Signaling by Neurons in Primate Striatum

Social decisions depend on reliable information about others. Consequently, social primates are motivated to acquire information about the identity, social status, and reproductive quality of others. Neurophysiological and neuroimaging studies implicate the striatum in the motivational control of behavior. Neuroimaging studies specifically implicate the ventromedial striatum in signaling motivational aspects of social interaction. Despite this evidence, precisely how striatal neurons encode social information remains unknown. Therefore, we probed the activity of single striatal neurons in monkeys choosing between visual social information at the potential expense of fluid reward. We show for the first time that a population of neurons located primarily in medial striatum selectively signals social information. Surprisingly, representation of social information was unrelated to simultaneously expressed social preferences. A largely nonoverlapping population of neurons that was not restricted to the medial striatum signaled information about fluid reward. Our findings demonstrate that information about social context and nutritive reward are maintained largely independently in striatum, even when both influence decisions to execute a single action.

Male mating behaviour in relation to female sexual swellings, socio-sexual behaviour and hormonal changes in wild Barbary macaques

In many cercopithecine primates females display probabilistic cues of fertility to indicate the periovulatory period to males. These cues may include female behaviour, acoustic signals, and morphological signs such as the anogenital swelling. However, the extent to which males can utilise this information varies between species. We describe male sexual behaviour in relation to changes in anogenital swelling size, timing of ovulation and female socio-sexual behaviour in wild Barbary macaques (Macaca sylvanus). We further compare male sexual behaviour during conception and post-conception cycles to evaluate if males differentiate between these qualitatively different cycle types. Our results show that during conception cycles male mating behaviour was concentrated around the fertile phase implying that males inferred information from more than swelling size alone. Male mating frequency increased in line with female socio-sexual behaviour, namely female presenting and the frequency of copulations with copulation calls. Most strikingly our results show that males invested equally in mating during fertile and non-fertile, i.e. post-conception, maximum swelling phases. Whether post-conception swellings were merely a result of changes in hormone concentrations during pregnancy or part of a female reproductive strategy remains elusive. In sum, this study adds to the body of research on the evolution of female sexual signals and how males may infer information from these cues.

Dressed for sex: red as a female sexual signal in humans.

BackgroundIn many non-human primate species, a display of red by a female serves as a sexual signal to attract male conspecifics. Red is associated with sex and romance in humans, and women convey their sexual interest to men through a variety of verbal, postural, and behavioral means. In the present research, we investigate whether female red ornamentation in non-human primates has a human analog, whereby women use a behavioral display of red to signal their sexual interest to men.Methodology/Principal FindingsThree studies tested the hypothesis that women use red clothing to communicate sexual interest to men in profile pictures on dating websites. In Study 1, women who imagined being interested in casual sex were more likely to display red (but not other colors) on their anticipated web profile picture. In Study 2, women who indicated interest in casual sex were more likely to prominently display red (but not other colors) on their actual web profile picture. In Study 3, women on a website dedicated to facilitating casual sexual relationships were more likely to prominently exhibit red (but not other colors) than women on a website dedicated to facilitating marital relationships.Conclusions/SignificanceThese results establish a provocative parallel between women and non-human female primates in red signal coloration in the mating game. This research shows, for the first time, a functional use of color in women's sexual self-presentation, and highlights the need to extend research on color beyond physics, physiology, and preference to psychological functioning.

Sexual signals and mating patterns in Syngnathidae

Male pregnancy in the family Syngnathidae (pipefishes, seahorses and seadragons) predisposes males to limit female reproductive success; sexual selection may then operate more strongly on females and female sexual signals may evolve (sex-role reversal). A bewildering array of female signals has evolved in Syngnathids, e.g. skin folds, large body size, colouration, markings on the body and elaborate courtship. These female sexual signals do not seem quantitatively or qualitatively different from those that evolve in males in species with conventional sex roles where males provide females or offspring with direct benefits. In several syngnathid species, males also evolve ornaments, females are choosy in addition to being competitive and males compete as well as choosing partners. Thus, sex roles form a continuum, spanning from conventional to reversed within this group of fishes. Cases are presented here suggesting that stronger sexual selection on females may be most extreme in species showing classical polyandry (one male mates with several females, such as many species where males brood their eggs on the trunk), intermediate in polygynandrous species (males and females both mate with more than one partner, as in many species where males brood their eggs on the tail) and least extreme, even exhibiting conventional sex roles, in monogamous species (one male mates solely with one female, as in many seahorses and tropical pipefishes). At the same time caution is needed before unanimously establishing this pattern: first, the connection between mating patterns, strength of sexual selection, sex roles and ornament expression is far from simple and straightforward, and second, knowledge of the actual morphology, ecology and behaviour of most syngnathid species is scanty. Basically only a few Nerophis, Syngnathus and Hippocampus species have been studied in any detail. It is known, however, that this group of fishes exhibits a remarkable variation in sex roles and ornamentation, making them an ideal group for the study of mating patterns, sexual selection and sexually selected signals.

Female–female aggression around mating: an extra cost of sociality in a multimale primate society

Multimale–multifemale groups, where both sexes mate promiscuously and the operational sex ratio is male biased, represent a classical mammalian society. Theory predicts low mating competition between females in such societies, but this is inconsistent with the frequent occurrence of female sexual signals. This study explores the determinants of female competition under such conditions by testing 3 hypotheses relating to patterns of aggression over the reproductive cycle in wild chacma baboons (Papio ursinus). Primarily, we expect the frequency of aggression to be highest among 1) lactating and pregnant females, who experience the greatest energetic demands, if females compete mainly over food, 2) lactating females, if females compete mainly over paternal care of infants, or 3) sexually active (swollen) females, if females compete mainly over mates. Data were collected from 27 females in 2 groups over 18 months and analyzed using mixed models. Our results provide most support for the mating competition hypothesis: aggression increases with the number of swollen females in a group, swollen females receive the most aggression, and mate-guarded swollen females receive more aggression than when unguarded. However, our analyses further indicate that such aggression rather than arising from direct mating competition, most likely reflects reproductive suppression and/or an increased exposure of swollen females to incidental aggression. These findings reveal the importance of sex in shaping social relationships among females in large primate groups where they were traditionally considered to be determined primarily by access to resources. Aggression associated with access to mates represents an extra cost of sociality to females. Key words: aggression, baboons, female–female competition, intrasexual selection, reproductive strategies, sociality. [Behav Ecol]

CORRELATED EVOLUTION OF FEMALE NEOTENY AND FLIGHTLESSNESS WITH MALE SPERMATOPHORE PRODUCTION IN FIREFLIES (COLEOPTERA: LAMPYRIDAE)

The beetle family Lampyridae (fireflies) encompasses ∼100 genera worldwide with considerable diversity in life histories and signaling modes. Some lampyrid males use reproductive accessory glands to produce spermatophores, which have been shown to increase female lifetime fecundity. Sexual dimorphism in the form of neotenic and flightless females is also common in this family. A major goal of this study was to test a hypothesized link between female flight ability and male spermatophore production. We examined macroevolutionary patterns to test for correlated evolution among different levels of female neoteny (and associated loss of flight ability), male accessory gland number (and associated spermatophore production), and sexual signaling mode. Trait reconstruction on a molecular phylogeny indicated that flying females and spermatophores were ancestral traits and that female neoteny increased monotonically and led to flightlessness within multiple lineages. In addition, male spermatophore production was lost multiple times. Our evolutionary trait analysis revealed significant correlations between increased female neoteny and male accessory gland number, as well as between flightlessness and spermatophore loss. In addition, female flightlessness was positively correlated with the use of glows as female sexual signal. Transition probability analysis supported an evolutionary sequence of female flightlessness evolving first, followed by loss of male spermatophores. These results contribute to understanding how spermatophores have evolved and how this important class of seminal nuptial gifts is linked to other traits, providing new insights into sexual selection and life-history evolution.

Can eggs in a cavity be a female secondary sexual signal? Male nest visits and modelling of egg visual discrimination in blue tits

Eggshell colouration is thought to function as a female-specific secondary sexual trait. While tests of this idea are rapidly accumulating in cavity-nesting birds, some fundamental underlying assumptions remain rarely investigated: namely, can males see eggshell coloration and perceive colour differences between the eggs of different females? We tested these two key assumptions in a natural population of blue tits (Cyanistes caeruleus). Using transponders, we tracked male nest visits and found that all males visited their nest-boxes while eggs were present and often visually accessible. Interestingly, some males also visited neighbouring nests. We then tested whether birds could detect eggshell coloration using models of avian colour vision; models were performed with and without limitations on visual performance owing to dim light. Both models found that differences in eggshell brightness were often easier to discriminate than differences in colour; there was more contrast in white eggshell background between clutches than within and its contrast against nest background was repeatable within clutches, suggesting these features could act as signals. Yet, the detectability of these contrasts depended entirely on model assumptions of visual limitations. Consequently, we need a better understanding of underlying visual mechanisms in dim-light environments and behavioural discrimination experiments before confirming the signalling potential of eggshell coloration.

Female Scent Signals Enhances Male Resistance to Influenza

AbstractScent of receptive females as signal to reproduction stimulate male mice to olfactory search of a potential breeding partner^1, 2^. This searching behavior is coupled with infection risk due to bacterial contamination of the fecal and urine scent marks^4^. The theoretical consideration of host evolution under inevitable parasitic pressures, including helminthes, bacteria, virus etc., predicts adaptations that help protect against parasites associated with breeding^7^. In this study, we propose that acceptation of female signals by male mice leads to adaptive redistribution of immune defense directed to protection against respiratory infection risks. Our results reveal migration of macrophages and neutrophils to upper airways upon exposure to female odor stimulus resulting in increased resistance to influenza virus in male mice. Contrary to widely accepted immunosuppressive function of female sexual signals, our data provide the first demonstration of the adaptive immunological response to female odor stimulus through induction of nonspecific immune response in upper airways.

Interactions between the sexes: new perspectives on sexual selection and reproductive isolation

Understanding the processes underlying the origin of new species is a fundamental problem in evolutionary research. Whilst it has long been recognised that closely related taxa often differ markedly in reproductive characteristics, only relatively recently has sexual selection been evoked as a key promoter of speciation through its ability to generate reproductive isolation (RI). Sexual selection potentially can influence the probability that individuals from the same or different populations will reproduce successfully since it shapes precisely those traits involved in mating and reproduction. If reproductive characters diverge along different trajectories, then sexual selection can impact on the evolution of reproductive barriers operating both before and after mating. In this perspective, we consider some new advances in our understanding of the coevolution of male and female sexual signals and receptors and suggest how these developments may provide heretofore neglected insights into the mechanisms by which isolating barriers may emerge. Specifically, we explore how selfish genetic elements (SGEs) can mediate pre- and post-copulatory mate choice, thereby influencing gene flow and ultimately population divergence; we examine evidence from studies of intracellular sperm–egg interactions and propose that intracellular gametic incompatibilities may arise after sperm entry into the egg, and thus contribute to RI; we review findings from genomic studies demonstrating rapid, adaptive evolution of reproductive genes in both sexes and discuss whether such changes are causal in determining RI or simply associated with it; and finally, we consider genetic, developmental and functional mechanisms that might constrain reproductive trait diversification, thereby limiting the scope for reproductive barriers to arise via sexual selection. We hope to stimulate work that will further the understanding of the role sexual selection plays in generating RI and ultimately speciation.