Effects of testosterone supplementation on chemical signals of male Iberian wall lizards: consequences for female mate choice

In some lizards, female mate choice is influenced by chemicals secreted by males, e.g., via the femoral glands. Secretions of the femoral glands are under direct androgenic control and vary seasonally with androgen production. However, whether increased testosterone (T) levels affect the concentration and chemical composition of secretions or their attractiveness to females is unknown. We manipulated T levels of male Iberian wall lizards, Podarcis hispanica, with silastic implants. Differential tongue-flick rates indicated that females detected and discriminated between femoral secretions of control and T-implanted males based on chemical cues alone. Females showed greater responses to secretions of T-males, which might suggest that T increased the concentration of chemical signals. Further analyses by gas chromatography–mass spectrometry indicated that T supplementation induced qualitative changes in lipid composition of femoral secretions. T-males had decreased relative proportions of cholesta-5,7-dien-3-ol in secretions, which might be related to the negative effects of T on the immune system and on lipid metabolism. However, experiments of choice of males’ scent showed that females neither preferred nor avoided the scent marks of T-males but preferred males that maintained higher proportions of cholesta-5,7-dien-3-ol in secretions, independently of the experimental manipulation. Thus, because this steroid is negatively affected by T, there might be trade-offs among increasing T levels to increase the production of chemical secretions, maintain metabolism, and attract females.     

Interpopulational variation in chemosensory responses to selected steroids from femoral secretions of male lizards, Podarcis hispanica, mirrors population differences in chemical signals

Chemical signals are important for mate and species recognition. If variation in chemical signals occurs between populations of the same species, these differences could later preclude mating between populations and lead to speciation. In the Iberian wall lizard, Podarcis hispanica, the lipophilic fraction of femoral secretions of males is mainly a mix of steroids and fatty acids. Among steroids, the most abundant compounds are cholesterol and cholesta-5,7-dien-3-ol, which are implicated in intraspecific communication and sexual selection. Interpopulational differences in chemical signals of males, and in response to these chemicals, could contribute to reproductive isolation between populations, which would explain the known genetic differences between these populations. Chemical analyses indicated that five distinct populations of this lizard from Madrid (Central Spain) differed in the proportions of two steroids (cholesterol and cholesta-5,7-dien-3-ol) in femoral secretions. Moreover, lizards discriminated and had high chemosensory responses (i.e., high tongue-flick rates) to these steroids, but showed interpopulational differences. Lizards from populations with cold temperatures and high relative humidity (i.e., northern Madrid) elicited higher responses to these steroids, whereas the converse occurred for lizards from populations occupying dry and hot habitats (i.e., southern Madrid). Interestingly, the magnitude of the chemosensory responses to cholesta-5,7-dien-3-ol in each population mirrored the abundance of this compound in secretions of males of that population. These results suggest that the importance of cholesta-5,7-dien-3-ol in males’ secretions might be lower for lizards from the southern populations. These differences in the relative importance of chemical signals could explain reproductive isolation and cryptic speciation between populations of this lizard.     

Sex differences in olfactory communication in a primate, the moustached tamarin, Saguinus mystax (Callitrichinae)

This study examines the hypothesis that sexual selection has shaped patterns of olfactory communication in wild moustached tamarins, Saguinus mystax. Do sex differences exist in frequencies and in the intensity of scent marking, in the use of different scent-marking types, and in behavioural responses to scent marks? Scent marking (anogenital, suprapubic, sternal) and behavioural responses (sniffing and overmarking) were recorded in four groups (ten adult and subadult males, seven adult and subadult females in all groups combined) in north-eastern Peru. Frequencies and intensity of scent marking were significantly higher in female tamarins. Males and females did not differ in the use of anogenital marking, but suprapubic marking was employed significantly more often by females. Only 10% of scent marks were monitored by another group member, and only 5% were overmarked by another group member. Most sniffing of scent marks was done by males, and males sniffed at marks produced by females significantly more often than at marks produced by males. Both sexes overmarked scent marks with similar frequency, but females overmarked scent marks produced by males significantly more often than those produced by females. An increase in frequencies of scent marking was observed in two females of one group after the death of the reproducing female, but frequencies of scent marking remained the same in the males of this group. The female-biased rates of scent marking are consistent with predictions made by sexual selection theory for species with substantial male care for offspring and strong reproductive competition between females. However, a decisive test of the proposed role of sexual selection will only be possible with more field data on patterns of olfactory communication in other callitrichine species.     

Male Iberian rock lizards may reduce the costs of fighting by scent matching of the resource holders

Animals should adopt strategies to minimize the costs of intraspecific aggressive interactions. For example, individuals should be able to identify resource holders in advance and avoid fighting with them because residents are generally more likely than intruders escalate aggression. It has been suggested that scent marks function mainly to allow competitor assessment by conveying the costs of entering a scent-marked area. Individuals may identify territory owners by comparing the scent of substrate marks with the scent of any conspecific they encounter nearby, assessing whether these two scents match or not, a mechanism known as scent matching. Here, we examined the response of male Iberolacerta cyreni lizards to areas scent-marked by other males and the potential role of scent matching in agonistic interactions. We designed a laboratory experiment where we allowed a male to explore the scent-marked substrate of another male, and then we immediately staged agonistic encounters in a nearby clean neutral area with either the male that had produced the scent marks (matching treatment) or with a different non-matching individual male. The higher chemosensory exploratory rates of substrate scent marks in comparison to clean substrates suggested that males detected and spent more time exploring scent marks to obtain information on the donor male. Moreover, this information was later used to decide the fighting strategy. Intruding males delayed time until the first agonistic interaction, reduced the intensity of fights and the number of aggressive interactions, and won less interactions with males which scent matched that of scent marks (because they would be considered as the territory owners) than with other non-matching individuals. Our results show that male I. cyreni lizards use scent matching as a mechanism to assess the ownership status of other males, which could contribute to modulate intrasexual aggression, reducing costs of agonistic interactions.     

Countermarking by male pygmy lorises (<Emphasis Type="Italic">Nycticebus pygmaeus</Emphasis>): do females use odor cues to select mates with high competitive ability?

Competitive countermarking occurs when animals compete to ensure that their scent marks are in the top-most position and more recently deposited than those of rivals. Because it takes a great deal of time and energy, and perhaps dominant or territorial status, to patrol the area and rapidly countermark rivals' marks, assessors may use the presence of countermarks as a reliable cue of the signaler's competitive ability. Selection on assessors, therefore, should favor the evolution of mechanisms to determine which scent is the countermark. Sexual selection theory predicts that females select high-quality males with whom to mate; therefore, females should mate preferentially with countermarking males. We examined the role of countermarking in intra-male competition and female mate choice in the pygmy loris. In experiment 1, we found that males deposit significantly more urine when countermarking other males' urine, but countermark female urine no more than control stimuli. In experiment 2, we exposed females to the urine of two males for several weeks. One male always deposited his urine first, whereas the second male always deposited his urine later and on top of the first male's urine. When reaching peak estrus, females were given a simultaneous choice test between the two males, and showed a significant preference for the countermarking male with regard to: (1) her location and orientation to the male, (2) her chemosensory interest in the male and his cage, and (3) her affiliative socio-sexual behaviors. These results are consistent with predictions from the competitive countermarking hypothesis, and demonstrate that chemosignals play a profound role in governing female reproductive behavior in the species.     

Chemical ornaments of male lizards <Emphasis Type="Italic">Psammodromus algirus</Emphasis> may reveal their parasite load and health state to females

Evidence for parasite-mediated sexual selection has been found in many species that use visual ornaments to attract females. However, in many animals, variation in female responses to scents of parasitized males suggests that parasitic infections might also affect information conveyed by pheromones (i.e., chemical ornaments). Thus, pheromones might also function in parasite-mediated sexual selection. We show here that female lizards Psammodromus algirus responded differently to femoral gland secretions of males according to the parasite load and health of these males. Scents of healthier males elicited more tongue flicks (a chemosensory behavior) by females, suggesting that these scents were more attractive. Chemical analyses showed that parasite load and the T-cell-mediated immune response were related to the variability in the proportions of some lipids in secretions of males. Further trials testing the chemosensory responses of females to chemical standards indicated that females actually discriminated the chemicals related to males’ health from other chemicals found in secretions. We suggest that these chemical ornaments may provide reliable information on the health and degree of parasitic infection of a male.     

Chemosensory cues allow male lizards<Emphasis Type="Italic"> Psammodromus algirus</Emphasis> to override visual concealment of sexual identity by satellite males

Males of many species of lizards show conspicuous breeding colors but, in some species, young competitively inferior males conceal their sexual identity by a female-like dull coloration that allows them to evade aggression from dominant males and to adopt an alternative satellite-sneaking mating tactic. However, large males of the lizard Psammodromus algirus reacted aggressively to young intruder males despite their female-like coloration, suggesting that they might have the ability to recognize competitor males by chemosensory cues. We experimentally manipulated the head coloration (brown vs orange) and scents (male vs female) of small young males. For staged agonistic encounters, we compared the response of resident unmanipulated large males to the different manipulated small males. When we manipulated only the color of small males, the response of resident large males was independent of the paint manipulation; brown and orange males elicited a similar aggressive response. However, when we also manipulated the scent, small males painted orange or brown, but bearing the scent of males, received a significantly higher number of aggressive responses than small males painted orange or brown, but bearing the scent of females. The results showed that, at close range, the reaction of large males to manipulated individuals was dependent on the scent, whereas color seemed to be less important. Coloration may be, however, more important in long-distance communication as shown by the outcome of the first encounters. Also, orange coloration may increase the intensity of the aggressive response. Effective sex recognition by territorial large males is important in natural situations to avoid sneak matings by young male competitors. Thus, even if small males visually conceal their sexual identity, chemosensory cues allow large males to identify them at close range.     

The scent of sun worship: basking experience alters scent mark composition in male lizards

Signals used in female choice should honestly advertise the benefits that males can provide, with direct benefits often argued as being more important than indirect benefits. However, the nature of direct benefits in species without paternal care or nuptial gifts is poorly understood. Previous studies on lizards suggest that females decide where to settle and assumedly who to mate with based on information contained in scent marks from territorial males. Access to high-quality thermal resources is crucial for female reproductive success. Females may therefore be able to detect and exploit thermal-induced variation in the chemical composition of male scent marks when assessing the quality of his territory. We show that the amount of time male wall lizards (Podarcis muralis) are allowed to bask significantly alters the chemical composition of their femoral secretions used in scent marking. The direction of the change is consistent with adaptive plasticity to maintain signalling efficacy under warm conditions that increase evaporation of femoral secretions. The compounds affected by basking experience included those previously associated with male quality or shown to mediate male–male competition in lizards. However, whilst female lizards could discriminate between scent marks of males that had experienced different basking conditions, they did not preferentially associate with the scent from males from high-quality thermal conditions. These results highlight the potential importance of a previously neglected environmental effect on chemical signalling. We suggest thermal effects may have significant consequences for scent-mark composition in variable environments, with potential repercussions on olfactory communication in lizards.     

Manipulation of Olfactory Signaling and Mate Choice for Conservation Breeding: a Case Study of Harvest Mice

Abstract:  Mate choice by females can introduce difficulties to captive breeding programs because there may be a conflict between the conservation manager's choice of mate (based on random allocation or maximizing heterogeneity) and the females' own preferences, often resulting in incompatibility and aggression. Similar effects are caused by inappropriate social contexts at the time of pairing. We manipulated the social experience of male and female harvest mice ( Micromys minutus ) to investigate whether we could enhance compatibility between randomly allocated mates by altering female preferences. In one experiment, we used a choice test to identify female preferences between two males and then varied the competitive context of unpreferred males by transferring competitor's scent marks into their cages. The manipulation caused them to increase their investment in a form of olfactory signaling (scent marking), which female rodents use as an indicator of male quality when choosing mates. The manipulation increased their attractiveness relative to the initially preferred male when the choice test was repeated. In a second experiment, we tested the effect of females' familiarity with the odor of males by transfer of male scent marks to female cages. Females preferred familiar males in choice tests and were less aggressive toward them when pairs were introduced than females paired with unfamiliar males. This kind of approach can influence mate choice, and transferring scent marks between cages or collections is an effective and practical behavioral means of improving success in conservation breeding programs.     

Chemosensory mate recognition may facilitate prolonged mate guarding by male snow skinks, Niveoscincus microlepidotus

We provide evidence that male lizards can use chemosensory cues to identify individual females and probably therefore maintain long-term associations with these females in the wild. In the laboratory, males preferentially followed the scent trail of their vitellogenic female “partner” rather than that of another vitellogenic female. Our 5-year field study of the small viviparous scincid lizard (Niveoscincus microlepidotus) in alpine Tasmania showed that sexually mature males and females commonly formed “pairs” for long periods (on average 29 days). These pairs occurred primarily during the mating season, always involved one adult male and one adult female, and usually involved vitellogenic rather than gravid females. Our laboratory experiments suggest that a significant factor in maintaining those prolonged partnerships is male scent trailing of partners. Received: 28 October 1997 / Accepted after revision: 28 May 1998     

Female territoriality and the function of scent-marking in a monogamous antelope (Oreotragus oreotragus)

In monogamous species, females often choose between males according to the quality of the territories they defend, but the extent to which females themselves contribute to territory defence is frequently underestimated. Here we test for differences in male and female roles during paired scent-marking bouts, a key component of territorial defence, in a monogamous antelope. In two populations (Kenya, Zimbabwe) of klipspringer, Oreotragus oreotragus, both males and females usually scent-marked at the same site, but there were significant differences between sexes in terms of investment within bouts. Females initiated most bouts, thus dictating the marking strategy of the pair. Males initiated relatively few bouts, but deposited more scent marks per bout than females and were usually the last to scent-mark before leaving the site; they marked on the same branches as the female and thus overmarked her scent. Both sexes deposited more marks during paired than solo visits. Immediately preceding and following scent-marking bouts, males approached females and females left males more often than expected. Female scent-marking rates were higher when they were receptive than at other times, and this increase was matched by elevated marking rates of males. Females may increase marking rates when they are receptive in order to test the quality of their mate or to incite male competition. However, these ideas are unlikely to explain female scent-marking behaviour outside the mating season, which appears to be related primarily to territorial defence. We suggest that these differences in investment in scent-marking bouts are consistent with predictions that females may be autonomously territorial and that overmarking of female scent by males is a form of mate-guarding. Received: 17 November 1999 / Received in revised form: 24 February 2000 / Accepted: 13 March 2000     

Lack of innate preference for morph and species identity in mate-searching <Emphasis Type="Italic">Enallagma</Emphasis> damselflies

Insect mate recognition is often viewed as stereotypic, innate, and species-specific. However, male damselflies can learn to identify female-specific color morphs as potential mates. A suite of male mimicry hypotheses assume that heteromorphic females, which differ from males in color pattern, are more easily recognized as “female” and thus lack the inherent, anti-harassment advantage that the more male-like signal provides for andromorphs. Using two measures of male preference, we investigated whether naïve males have a preexisting sensory bias for a given morph color in Enallagma civile, a species that appeared to exhibit extreme plasticity in morph expression across generations within a breeding season. E. civile males raised in the absence of females exhibited no preference for either morph, whereas males raised with one female type exhibited a learned sensory bias for that morph. Male Enallagma also lacked a bias toward conspecific females over a congeneric sister species. In a naturally naïve population of Enallagma ebrium, males reacted sexually to both morphs of Enallagma hageni as often as they did to conspecific females, whose thoracic spectra were nearly identical with those of E. hageni. Moreover, despite the similar thoracic spectra of males and andromorphs, both of which reflected UV, males rarely reacted sexually to other males. Our results falsified implicit assumptions of male mimicry hypotheses, supported learned mate recognition, and suggested a scenario for speciation via sexual conflict.     

Male mate choice favors more colorful females in the gift-giving cabbage butterfly

While the phenomenon of male mate choice has attracted considerable attention in the last two decades, whether this sexual selection mechanism could drive the evolution of female ornaments remains poorly understood. Here, we used experimental manipulation of female wing coloration to investigate male mate choice in Pieris rapae, a gift-giving butterfly. Further, we tested whether males’ nutritional status influenced their mating preferences by subjecting larvae to short periods of starvation. We found that males showed significantly more mating approaches toward control females with more colorful wings (higher pteridine content), and that this preference was strongest in low-nutrition males. Additionally, a study of field-collected females revealed that pteridine-based wing coloration was positively correlated with female egg load, which suggests such ornaments may signal female quality. Pteridine-based ornaments are widespread in nature, however their potential as honest signals in male mate choice remains largely unexplored. This work furthers our understanding of how male mate choice and female ornamentation may evolve in species whose mating systems include nutritional nuptial gifts.     

To whom it may concern: the transmission and function of chemical signals in Lemur catta

The goals of this study were to investigate the transmission and possible functions of chemical signals in intragroup communication among ring-tailed lemurs, Lemur catta. In particular, I examined the effects of sex on these processes because sexual selection theory predicts specific functions for chemical signals. I recorded all interactions with 214 scent marks of 11 male and 9 female ring-tailed lemurs during the first 10 min following their deposition. I found that 62% of these scent marks were investigated with a median latency of 30 s and that 89% of investigated scents were also counter-marked by the receiver. The type of focal scent mark (male or female anogenital and male antebrachial mark) had a significant effect on both the timing and type of response. Males investigated and counter-marked female scents more often than vice versa, but significant second-order transitions suggested that the behavior of an animal was not only influenced by the immediately preceding scent mark and that a scent is not completely masked by a counter-mark. There was no evidence for an audience effect, and only social rank of female senders had an effect on receivers. Variation in the response of receivers across reproductive seasons as a function of senders' sex indicated that female scents may function in mate attraction and competition among females, whereas male scents may be primarily used in intrasexual competition. Three main conclusions emerged. First, the exchange of olfactory signals within groups was highly structured and surprisingly efficient. Second, olfactory signals may constitute general mesasages whose transfer is partly controlled by the receiver. Finally, sexual selection theory provides a useful theoretical framework for functional examinations of mammalian olfactory communication. Received: 13 June 1997 / Accepted after revision: 20 March 1998     

Olfactory cues,genetic relatedness and female mate choice in the agile antechinus (<Emphasis Type="Italic">Antechinus agilis</Emphasis>)

Females show mate preferences for males that are genetically dissimilar to themselves in a variety of taxa, but how females choose these males is not clearly understood. In this study, we examined the effects of olfactory stimuli and genetic relatedness on female mate choice in a small carnivorous marsupial, the agile antechinus (Antechinus agilis), during two breeding seasons. Captive female antechinus in oestrus were provided with a combination of male urine and body scent from two novel males, one more genetically similar and one more dissimilar to the females, in a Y-maze olfactometer. Genetic relatedness between females and pairs of males was determined using highly polymorphic, species-specific, microsatellite markers. Females consistently chose to visit the scents of males that were genetically dissimilar to themselves first, spent significantly more time near the source of those scents and showed more sexual and non-exploratory behaviours near those scents. These data demonstrate that chemosensory cues are important in mate choice in the agile antechinus and that females prefer males that are genetically dissimilar to themselves.     

Dominant male red junglefowl (Gallus gallus) test the dominance status of other males

In sexual selection, honest signals are maintained by a variety of mechanisms. In red junglefowl (Gallus gallus), health, condition and social status affect comb size, a well-documented predictor of female choice. The comb size of subordinate male junglefowl appears to be suppressed when in the company of other males. One hypothesis for how social status could affect ornament expression in this way involves punishment of cheaters. Under this scenario, dominant males periodically challenge similar males signalling putative high status. For subordinate males, the risk of fighting a high-ranked male could make it prohibitively costly to develop ornamentation signalling dominance. We asked if dominance signals influenced the direction of aggression by dominant males. To address this issue, we conducted experiments in which 19 dominant-acting, large-combed male junglefowl were allowed to choose to fight one of two opponents. The two potential fight opponents differed in comb size, dominance behaviour, or in both traits. In 15 of 19 trials, dominant-acting males chose to fight large-combed, dominant-acting opponents rather than small-combed, subordinate-acting opponents. This is the first demonstration that aggression of dominant male birds is directed at other males based on the display of an ornament known to be attractive to females. However, males did not discriminate between fight opponents when potential opponents differed in only one of the two status indicators (large-combed males chosen in 11 of 19 trials, dominant-acting males chosen in 10 of 19 trials).     

Chemical aposematism

Discussions of aposematism traditionally have focused on the visual displays of prey that denote unpalatability or toxicity to predators. However, the construct of aposematism accommodates a spectrum of unprofitable traits signaled through various sensory modalities, including contact and distance chemoreception. Aposematism, involving learned aversions by signal receivers or selection for their unlearned avoidances, arises in predator–prey or other interspecific interactions where a mutually beneficial avoidance of signal emitters by signal receivers exists. Aposematism evolves by selection against signal receivers, e.g., predators, imposed by signal emitters, e.g., unprofitable prey, and vice versa, where both nondiscriminating signal receivers and unrecognized signal emitters are imperiled. Chemical aposematism entails concurrent reciprocal selection where signal emitters select for chemosensory avoidance responses in signal receivers, and where signal receivers select for the emission of identifiable (distinctive) chemicals in signal emitters.     

Correlational evidence of a sexually-selected handicap

Handicap models of sexual selection predict that ornaments must be costly to produce and/or to wear and maintain; only then can they evolve as reliable signals of genetic quality. We investigated in the laboratory one potential cost of possessing ornaments, using the viviparous fish Girardinichthys multiradiatus and its natural predator, the snake Thamnophis melanogaster. We found that female G. multiradiatus show preferences for males with larger fins, as measured from body correlates. Males with a morphology attractive to females, however, were more likely to be captured by snakes than were other males (Fig. 5). Greater vulnerability to snakes cannot be explained as a result of snake visual preferences, because snakes responded similarly to males and females (Fig. 6). Finally, males, particularly dominant ones, were more likely to inspect foraging snakes than were females (Fig. 7). We conclude that male Girardinichthys multiradiatus experience a sexually-selected handicap due to reduced mobility resulting from having enlarged fins.     

Mate attraction by females in a sexually cannibalistic praying mantis

We studied mate attraction by females of the praying mantid, Tenodera aridifolia sinensis, testing honest signaling of mate availability versus deceptive signaling to attract males for sexual cannibalism. We experimentally varied female diet and mating history and measured the rate of attraction of a wild population of males to caged females. Honest signaling theory predicts that virgin females will attract males at the greatest rate whereas deceptive signaling predicts that hungry females (which are more likely to cannibalize males) will attract more males, particularly among non-virgin females. Our results show that hungry females did not attract more males than well-fed females. Indeed, the opposite was true: hungry females attracted significantly fewer males. Moreover, hungry females were no more likely than well-fed females to attract males subsequent to mating, and mated females attracted males at a lower rate than did virgin females. We also observed female T. aridifolia sinensis and male Mantis religiosa arriving at the caged females and we discuss the significance of these observations. The results refute the hypothesis of deceptive signaling and show that mate attraction signals of female T. aridifolia sinensis are honest indicators of female mate availability and a lower risk of sexual cannibalism.     

Carotenoid-derived ornaments reflect parental quality in male and female yellow-eyed penguins (<Emphasis Type="Italic">Megadyptes antipodes</Emphasis>)

The handicap principle suggests that ornamental traits that function as honest signals in mate selection must be costly to be effective. We evaluated in the sexually monochromatic yellow-eyed penguin (Megadyptes antipodes) whether the carotenoid-derived plumage and eye coloration predicts parental quality and whether males and females within pairs mate assortatively in relation to these carotenoid-derived ornaments. In addition, we investigated whether age or body condition was related to the coloration of the ornamental traits. In yellow-eyed penguins, parental quality of males and females was predicted by eye and head plumage coloration. Even when we controlled for gender- and age-specific differences, eye and head plumage coloration reflected honestly parental quality. Males and females mated assortatively in relation to these ornamental traits. While age influenced coloration of both the eye and head plumage, body condition was related only to the saturation of plumage coloration. These results provide evidence that the carotenoid-derived ornaments in yellow-eyed penguins reflect the parental abilities of birds and, therefore, may be costly signals. Potentially, female and male yellow-eyed penguins could use eye and plumage coloration as an indirect cue in assessing age and quality of individual birds during mate choice. This is only the second study to examine plumage coloration in relation to sexual selection in penguins, while conspicuous ornamental traits in other species of penguin beg the question whether they also play a role in sexual selection.Electronic Supplementary Material Supplementary material is available in the online version of this article at Communicated by C.R. Brown