Female Iberian wall lizards prefer male scents that signal a better cell-mediated immune response

In spite of the importance of chemoreception in sexual selection of lizards, only a few studies have examined the composition of chemical signals, and it is unknown whether and how chemicals provide honest information. Chemical signals might be honest if there were a trade-off between sexual advertisement and the immune system. Here, we show that proportions of cholesta-5,7-dien-3-ol in femoral secretions of male Iberian wall lizards (Podarcis hispanica) were related to their T-cell-mediated immune response. Thus, only males with a good immune system may allocate higher amounts of this chemical to signalling. Furthermore, females selected scents of males with higher proportions of cholesta-5,7-dien-3-ol and lower proportions of cholesterol. Thus, females might base their mate choice on the males' quality as indicated by the composition of their chemical signals.     

Preference for Male Traits Differ in Two Female Morphs of the Tree Lizard,Urosaurus ornatus

Non-random female mating preferences may contribute to the maintenance of phenotypic variation in color polymorphic species. However, the effect of female preference depends on the types of male traits used as signals by receptive females. If preference signals derive from discrete male traits (i.e., morph-specific), female preferences may rapidly fix to a morph. However, female preference signals may also include condition-dependent male traits. In this scenario, female preference may differ depending on the social context (i.e., male morph availability). Male tree lizards (Urosaurus ornatus) exhibit a dewlap color polymorphism that covaries with mating behavior. Blue morph males are aggressive and defend territories, yellow males are less aggressive and defend smaller territories, and orange males are typically nomadic. Female U. ornatus are also polymorphic in dewlap color, but the covariation between dewlap color and female behavior is unknown. We performed an experiment to determine how female mate choice depends on the visual and chemical signals produced by males. We also tested whether female morphs differ in their preferences for these signals. Female preferences involved both male dewlap color and size of the ventral color patch. However, the female morphs responded to these signals differently and depended on the choice between the types of male morphs. Our experiment revealed that females may be capable of distinguishing among the male morphs using chemical signals alone. Yellow females exhibit preferences based on both chemical and visual signals, which may be a strategy to avoid ultra-dominant males. In contrast, orange females may prefer dominant males. We conclude that female U. ornatus morphs differ in mating behavior. Our findings also provide evidence for a chemical polymorphism among male lizards in femoral pore secretions.     

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.     

Chemosensory exploration of male scent by female rock lizards result from multiple chemical signals of males

Multiple sexual signals may convey information on males' quality. However, most research focused on visual signals, ignoring chemical signals. In vertebrates, chemical signals are probably often a multicomponent mixture of several active compounds, but they are not well known. We examined the potential additive and interactive effects of 2 compounds (oleic acid and ergosterol) naturally found in femoral gland secretions of male rock lizards on chemosensory exploration behavior of females. Tongue-flick (TF) rates of females to male secretions may result from the combination of responses to multiple compounds. There may be an additive or synergetic effect because male secretions with the highest proportions of both compounds received the highest TF rates, suggesting that their scents were more intriguing. However, there might be an interactive effect too; female TF rates were higher to males' scent with high proportions of ergosterol alone, even if proportions of oleic acid were low, than to high proportions of oleic acid but with low proportions of ergosterol. Further bioassays testing TF behavior of females to standard compounds, presented alone or combined in different concentrations confirmed these findings. Variations in female TF behavior might be explained because different compounds signal different male traits of different importance for females. Our study suggested that femoral secretion of male rock lizards may act as a multicomponent chemical signal.     

A Drosophila male pheromone affects female sexual receptivity

Sex pheromones are chemical signals frequently required for mate choice, but their reciprocal role on mate preference has rarely been shown in both sexes. In Drosophila melanogaster flies, the predominant cuticular hydrocarbons (CHs) are sexually dimorphic: only females produce 7,11-dienes, whereas 7-tricosene (7-T) is the principal male CH. Males generally prefer females with 7,11-dienes, but the role of 7-T on female behaviour remains unclear. With perfumed males, control females mated faster and more often with males carrying increased levels of 7-T showing that this CH acts as a chemical stimulant for D. melanogaster females. Control females-but not antenna-less females-could detect small variation of 7-T. Finally, our finding that desat1 mutant female showed altered response towards 7-T provides an additional role for this gene which affects the production and the perception of pheromones involved in mate choice, in both sexes.     

Supplementation of male pheromone on rock substrates attracts female rock lizards to the territories of males: a field experiment

Background

Many animals produce elaborated sexual signals to attract mates, among them are common chemical sexual signals (pheromones) with an attracting function. Lizards produce chemical secretions for scent marking that may have a role in sexual selection. In the laboratory, female rock lizards (Iberolacerta cyreni) prefer the scent of males with more ergosterol in their femoral secretions. However, it is not known whether the scent-marks of male rock lizards may actually attract females to male territories in the field.

Methodology/Principal Findings

In the field, we added ergosterol to rocks inside the territories of male lizards, and found that this manipulation resulted in increased relative densities of females in these territories. Furthermore, a higher number of females were observed associated to males in manipulated plots, which probably increased mating opportunities for males in these areas.

Conclusions/Significance

These and previous laboratory results suggest that female rock lizards may select to settle in home ranges based on the characteristics of scent-marks from conspecific males. Therefore, male rock lizards might attract more females and obtain more matings by increasing the proportion of ergosterol when scent-marking their territories. However, previous studies suggest that the allocation of ergosterol to secretions may be costly and only high quality males could afford it, thus, allowing the evolution of scent-marks as an honest sexual display.     

Vitamin D supplementation increases the attractiveness of males' scent for female Iberian rock lizards

Evolutionary theory proposes that signals used in sexual selection can only be stable if they are honest and condition dependent. However, despite the fact that chemical signals are used by many animals, empirical research has mainly focused on visual and acoustic signals. Vitamin D is an essential nutrient for lizards, but in some lizards its precursor (cholesta-5,7-dien-3-ol=provitamin D) is found in femoral gland secretions, which males use for scent marking and intraspecific communication. By allocating provitamin D to secretions, males might need to divert vitamin D from metabolism. This might be costly and condition dependent. We tested whether diet quality affected chemical signals of male Iberian rock lizards (Lacerta monticola) and its consequences for sexual selection. After experimental supplementation of dietary vitamin D, males increased the proportion of provitamin D in femoral secretions. Further experiments showed that females detected these changes in males' signals by chemosensory cues, and discriminated provitamin D, and changes in its concentration, from similar steroids (i.e. cholesterol) found in secretions. Moreover, females preferred areas scent marked by males with more provitamin D in their secretions. This mechanism would confer honesty to chemical signals of male lizards, and, thus, females may rely on it to select high-quality males. We suggest that the allocation of vitamins and other essential nutrients to either visual (e.g. carotenoids) or chemical ornaments might be the common basis of honest sexual displays in many animals.     

Natural Variation in the Strength and Direction of Male Mating Preferences for Female Pheromones in Drosophila melanogaster

Many animal species communicate using chemical signals. In Drosophila, cuticular hydrocarbons (CHCs) are involved in species and sexual identification, and have long been thought to act as stimulatory pheromones as well. However, a previous study reported that D. melanogaster males were more attracted to females that were lacking CHCs. This surprising result is consistent with several evolutionary hypotheses but is at odds with other work demonstrating that female CHCs are attractive to males. Here, we investigated natural variation in male preferences for female pheromones using transgenic flies that cannot produce CHCs. By perfuming females with CHCs and performing mate choice tests, we found that some male genotypes prefer females with pheromones, some have no apparent preference, and at least one male genotype prefers females without pheromones. This variation provides an excellent opportunity to further investigate the mechanistic causes and evolutionary implications of divergent pheromone preferences in D. melanogaster males.     

Responses to Femoral Gland Secretions by Visually Adept Male and Female Collared Lizards

Although visually transmitted social signals are well documented in many diurnal iguanians, including collared lizards, secretory femoral glands also suggest a role of chemical signals in intraspecific communication. We conducted laboratory trials to test the extent to which male and female collared lizards responded by tongue‐flicking femoral gland secretions, neutral (water), and odoriferous (cologne) control substances, males distinguished self‐secretions from those produced by unfamiliar rival males, and females distinguish secretions from unfamiliar vs. familiar males. Both males and females spent similar amounts of time in four arena quadrants each with a Petri dish treated with one of the four test compounds. Males gave more tongue flicks/trial to secretions produced by unfamiliar rivals and cologne than they tongue‐flicked their own secretions and water. By contrast, the number of tongue flicks by females on control substances and familiar and unfamiliar males was similar. Results support the hypothesis that femoral gland secretions function in intrasexual signaling among male collared lizards, perhaps allowing them to distinguish unfamiliar rivals. Females tongue‐flicked secretions from familiar and unfamiliar males with similar frequency that was high relative to that of males, suggesting a possible role of secretions in assessment of males. Ours is the first evidence of a signaling role of femoral gland secretions in collared lizards and adds to a growing body of evidence that chemical signaling has evolved in diurnal lizards that also have highly developed visual‐based signaling.     

Female choice depends on size but not symmetry of dorsal eyespots in the butterfly Bicyclus anynana

The eyespots on the ventral wings of Bicyclus anynana butterflies are exposed when at rest and interact with predators. Those on the dorsal surface are not exposed in this way, and may be involved in courtship and mate choice. In this study, we examined whether the size and fluctuating asymmetry (FA) of dorsal eyespots are reliable signals of male quality. High developmental stability is considered to result in low FA, and to be associated with high quality. Individuals of high quality are predicted to produce sexually selected traits that are large and symmetrical, at a relatively low cost. In this study, we manipulated eyespot development to uncouple eyespot size and FA in order to examine their independent roles in signalling to the female. Individual females in cages were given the choice between two or three males differing in eyespot traits. The results indicate that although size per se of the eyespots is used as a signal, FA and wing size are not. We discuss the use of FA in studies of sexual selection and aspects of sexual selection on dorsal eyespot size.     

Spatial and temporal variations in nesting success and the causes of nest losses of the freshwater three-spined stickleback,Gasterosteus aculeatus

Synopsis Two experients were conducted to determine the effect of male color phenotype present during development on the mate choice of adult female guppies. Females were raised with either a colorful male, non-colorful male, or no male, and then measured for choice of a colorful or non-colorful male in a two-stimulus visual choice test. In the first experiment, adult females were measured for choice between the same male phenotypes used during the developmental exposure. Females raised with colorful males had significantly higher choice scores for colorful males than did females raised with non-colorful males or with no male. In the second experiment, an effect of developmental experience was observed when adult females were tested for choice with a general range of colorful and non-colorful males. However, this effect of experience during development was not detected when females were tested for choice between the same male phenotypes used during the developmental exposure. The predation regime of the source population, either high or low, showed no consistent effect on average female choice or on whether developmental experience changed female mate choice. Overall, these experiments show that experience with male phenotypes can affect the mate choice of adult guppies, but this effect was not observed under all developmental treatments or test conditions. Such an effect could significantly change the dynamics of the evolution of female preference due to sexual selection in the guppy.     

Spider sex pheromones: emission, reception, structures, and functions

Spiders and their mating systems are useful study subjects with which to investigate questions of widespread interest about sexual selection, pre- and post-copulatory mate choice, sperm competition, mating strategies, and sexual conflict. Conclusions drawn from such studies are broadly applicable to a range of taxa, but rely on accurate understanding of spider sexual interactions. Extensive behavioural experimentation demonstrates the presence of sex pheromones in many spider species, and recent major advances in the identification of spider sex pheromones merit review. Synthesised here are the emission, transmission, structures, and functions of spider sex pheromones, with emphasis on the crucial and dynamic role of sex pheromones in female and male mating strategies generally. Techniques for behavioural, chemical and electrophysiological study are summarised, and I aim to provide guidelines for incorporating sex pheromones into future studies of spider mating. In the spiders, pheromones are generally emitted by females and received by males, but this pattern is not universal. Female spiders emit cuticular and/or silk-based sex pheromones, which can be airborne or received via contact with chemoreceptors on male pedipalps. Airborne pheromones primarily attract males or elicit male searching behaviour. Contact pheromones stimulate male courtship behaviour and provide specific information about the emitter's identity. Male spiders are generally choosy and are often most attracted to adult virgin females and juvenile females prior to their final moult. This suggests the first male to mate with a female has significant advantages, perhaps due to sperm priority patterns, or mated female disinterest. Both sexes may attempt to control female pheromone emission, and thus dictate the frequency and timing of female mating, reflecting the potentially different costs of female signalling and/or polyandry to both sexes. Spider sex pheromones are likely to be lipids or lipid soluble, may be closely related to primary metabolites, and are not necessarily species specific, although they can still assist with species recognition. Newer electrophysiological techniques coupled with chemical analyses assist with the identification of sex pheromone compounds. This provides opportunities for more targeted behavioural experimentation, perhaps with synthetic pheromones, and for theorising about the biosynthesis and evolution of chemical signals generally. Given the intriguing biology of spiders, and the critical role of chemical signals for spiders and many other animal taxa, a deeper understanding of spider sex pheromones should prove productive.     

Chemosensory discrimination of male age by female Psammodromus algirus lizards based on femoral secretions and feces

Chemical communication plays an essential role in several social and reproductive behaviors of many animals. In lizards, the main sources of semiochemicals are femoral or pre‐anal gland secretions and feces. In male lizards Psammodromus algirus, there are age‐related differences in the chemical composition of femoral gland secretions and in the reproductive strategies, with older males defending territories and females, while younger males adopting sneak‐mating strategies. Females flee more often from mating advances of young males than from those of old males, which are more successful in obtaining matings. This suggests that age discrimination of males may be important for females. We tested here whether females showed differential chemosensory responses to chemical cues (femoral gland secretion and feces) of males of two age classes, and whether females use information from substrate scent marks of males of different ages to select where to stay. We found that females elicited more tongue‐flicks to the secretion and feces of old males than to control or secretion and feces of young males. Also, the time spent by females on a scented paper depended on the treatment, suggesting that females tended to spend more time on scent marks made with femoral secretions of old males. Adult females seemed capable to discriminate between young and old males based on chemical cues alone and showed more interest in scents of old males. However, substrate scent marks did not seem to entirely determine site selection by females, suggesting that females might need additional cues to perform the choice. These results can be explained by the different age‐dependent reproductive strategies of males, which can affect differentially to females.     

Scent marking and mate choice in the prairie vole, Microtus ochrogaster

Scent marking is common among male and female rodents and might be used in male-male competition and as a mechanism for mate attraction. I tested the hypotheses that females would choose males based on their frequency and placement of scent marks, and that a female would advertise interest in a particular male by placing her scent marks on or near those of a preferred mating partner. In a series of experiments conducted with prairie voles, Microtus ochrogaster, females did not choose mates based on the frequency or placement of scent marks by males nor did they advertise their interest in a particular male through the frequency or placement of scent marks. The number of males chosen that scent-marked more than their opponents did not differ significantly between females exposed (11 of 15) and not exposed (10 of 15) to scents of males. Females exposed and not exposed to scents of males preferred seven of the same males that had scent-marked more than their opponents. When a third group of females was exposed to four times more scent of the less preferred than preferred males, they still chose the preferred males. Thus, the frequency and placement of scent marks by males were not used to assess males for mate choice nor did female prairie voles use scent to advertise their preference for a mating partner. In that scent marking is common in male and female mammals, scent quality might be more important than quantity in male-male competition and mate attraction.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved .     

The role of olfaction during mating in the southern temperate spiny lobster Jasus edwardsii

Chemosensory communication may be crucial during mate choice and mating in the southern temperate spiny lobster Jasus edwardsii to ensure that females mate with large males capable of supplying adequate numbers of sperm during the short mating window. To clarify the role of pheromones during this process, three laboratory experiments were carried out. In an experiment where the output of urine, which contains sex-specific pheromones, from large and small catheterized males was switched, large post-molt females did not make a clear choice of mate. This indicates that while females distinguish among females, males, and juveniles using their chemosensory sense, they distinguish among males using visual and tactile senses in combination with olfaction. Further, two antennule-ablation experiments were carried out to determine if detection of pheromones by the antennules of females or males was critical for mate selection, courting, or mating. In both cases, we observed a (nonsignificant) trend of slightly delayed mating of treatment females. We found that disruption of female olfaction causes less impact on courtship or mating than ablation of male antennules which increased the variance in the length of the period between molting and mating and resulted in a systematic reduction in clutch size. This lesser impact of female ablation may be because females can still respond to their own internal cues about egg ripeness whereas males cannot. In J. edwardsii, unlike the American clawed lobster, Homarus americanus, one fully functional partner of either sex appears sufficient to initiate mating.     

Pheromone Blend Does not Explain Old Male Mating Advantage in a Butterfly

In several insect species, male mating success is higher in older than in younger males, although condition diminishes dramatically with age. Two hypotheses are under debate to explain the counterintuitive pattern of old male mating advantage: first, an increased eagerness of older males to mate, driven by their low residual reproductive value, and second female preference for older males based on chemical cues such as sex pheromones (female choice hypothesis). In a series of experiments, we manipulated female olfaction, male pheromone blend and female age to test whether old male mating advantage prevails when the influence of male sex pheromones is controlled for, using the tropical butterfly Bicyclus anynana as model. We found that older males had a higher mating success than younger ones irrespective of female scent‐sensitivity and irrespective of male pheromone blend. Interestingly, older males were found to court more often and for longer time bouts than younger males. These results were independent of female age, although younger males courted younger females more often and for longer bouts than older females. Taken together, our results indicate that male courtship activity (1) is higher in older compared to younger males and (2) increases the mating success of older males. Olfaction and sensing pheromones, in contrast, were not a necessary prerequisite for old male mating advantage to occur and may use other cues than pheromones to assess male quality.     

Chemical recognition of conspecifics in a neotropical lizard, <Emphasis Type="Italic">Liolaemus pacha</Emphasis> (Iguania: Liolaemidae): relation to visual displays,season and sex

Chemical cues play an important role in sexual recognition in several lizard species. Here, we investigated whether the neotropical lizard, Liolaemus pacha (Iguania: Liolaemidae) can discriminate between chemical information obtained from males or females. In addition, we also considered the effect of season (reproductive vs. post-reproductive) and the sex of the tested individual. We experimentally tested scent discrimination, using a terrarium previously occupied by a male, a female, and an untreated terrarium as control as sources of different chemical scents. We counted the number of tongue flicks, a measure of chemical exploratory behavior, and the visual displays triggered by these scents for 10 min. Males performed significantly more tongue flicks when female scent was present than when male and control scents were present, indicating sexual recognition. However, females did not show a significant difference in those same conditions, indicating a lack of sexual recognition. For visual displays, males showed significantly higher rates to female and male scents than to control, whereas females did not show any difference. During the reproductive season, the number of tongue flicks and visual displays were higher than during the post-reproductive season. Our results suggest that for male L. pacha, chemical cues play an important role in mate recognition. We discuss the apparent lack of recognition in females. We suggest that the observed seasonal behavioral differences might be associated with physiological changes related mainly to reproduction.     

Stronger convex (stabilizing) selection on homologous sexual display traits in females than in males: a multipopulation comparison in Drosophila serrata

Mutual mate choice for homologous sexual display traits has been demonstrated in several recent studies yet little attention has been given to quantitative comparison of the strength and form of mate preferences between the sexes. Such comparisons may provide important insight into the evolution of mate choice for honest signals. In particular, because females generally provide the majority of resources for initial offspring development, female displays may trade-off with fecundity, causing preference evolution to differ between the sexes. Recent theory suggests that adaptive male preferences for honest displays in females are possible under certain conditions and may result in preferences that are convex (i.e., stabilizing) in form. We compared sexual selection on a suite of contact pheromones arising from mutual mate choice using nine separate geographic populations of Drosophila serrata. We show that the convex selection is stronger on females than on males overall in these populations, and that convex selection is the predominate form of nonlinear selection on females but not males.     

Indirect female choice mediated by sex pheromones in the hermit crab Pagurus filholi

Males of the hermit crab Pagurus filholi perform precopulatory guarding behavior, and solitary males often show aggressive behavior to take away guarded females. Males behave coercively while guarding females, so direct mate choice by females seems difficult in such a situation. By performing several experiments we examined possible indirect female choice of hermit crab. Males were attached to a shell by their left cheliped to look like guarding pairs (fake guarding pairs). The shells were filled with cotton containing either seawater or pheromone water. The fake guarding pair with only seawater caused male–male combat in 60% of trials whereas with pheromone water combats occurred in 88% of trials. Mean duration of male–male combat was significantly longer in trials with drops of seawater containing pheromones than in those without pheromones. These results suggest guarding pairs themselves cause male–male combat by visual stimulation, that female sex pheromones have further significant function in the recognition of guarding pairs and intensification of male–male combat, and that females release sex pheromones while they are guarded. As a result of the combat, the larger male ended up guarding a female. This strongly suggests that females choose males indirectly by exploiting male–male competition induced by sex pheromones under male coercive behavior.     

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.