Encoding choosiness: female attraction requires prior physical contact with individual male scents in mice

Scents, detected through both the main and vomeronasal olfactory systems, play a crucial role in regulating reproductive behaviour in many mammals. In laboratory mice, female preference for airborne urinary scents from males (detected through the main olfactory system) is learnt through association with scents detected through the vomeronasal system during contact with the scent source. This may reflect a more complex assessment of individual males than that implied by laboratory mouse studies in which individual variation has largely been eliminated. To test this, we assessed female preference between male and female urine using wild house mice with natural individual genetic variation in urinary identity signals. We confirm that females exhibit a general preference for male over female urine when able to contact urine scents. However, they are only attracted to airborne urinary volatiles from individual males whose urine they have previously contacted. Even females with a natural exposure to many individuals of both sexes fail to develop generalized attraction to airborne male scents. This implies that information gained through contact with a specific male's scent is essential to stimulate attraction, providing a new perspective on the cues and olfactory pathways involved in sex recognition and mate assessment in rodents.     

Female reproductive behaviour,ovarian hormones and vaginal cytology of the induced ovulator, <Emphasis Type="Italic">Ctenomys talarum</Emphasis>

In the present study, we evaluated whether reproductive condition affects female reproductive behaviour in the induced ovulator Ctenomys talarum. We also explored the effect of the interaction with a male on the reproductive condition of females. To evaluate this, we arranged mating trials and evaluated female reproductive behaviour. Reproductive status of females was evaluated using a combined approach of vaginal smears, urinary progesterone and oestradiol, and ovarian histology. Behaviours denoting attraction (‘male sniff’ and ‘mount attempts’) and mutual courtship behaviours (‘spin’ and copula) were correlated with vaginal cytology before and oestradiol and progesterone levels in urine 12 h after male–female encounter. After 24 h of the interaction, oestradiol levels and vaginal epithelization increased while progesterone levels decreased in soliciting females. C. talarum females’ reproductive behaviour was related to its physiological reproductive state and vaginal cytology. The kind of male interaction, whether couples copulated or remained indifferent affected the later status of females. Females are induced ovulators by mating but male presence and interaction also affected other components of their reproductive physiology such as ovarian hormones and vaginal cytology.     

The identification of attractive volatiles in aged male mouse urine

In many species, older males are often preferred mates because they carry "good" genes that account for their viability. In some animals, including mice, which rely heavily on chemical communication, there is some indication that an animal's age can be determined by its scent. In order to identify the attractants in aged male mouse urine, chemical and behavioral studies were performed. We herein show that aged mice have higher levels of 3,4-dehydro-exo- brevicomin (DB), 2-sec-butyl-4,5-dihydrothiazole (BT), and 2-isopropyl-4,5-dihydrothiazole (IT) and a lower level of 6-hydroxy-6-methyl-3-heptanone relative to adult male mice. We also demonstrate that the attraction of females to the odor of male mouse urine is greater when the urine is from aged males. However, the attraction of aged urine odor was offset by the ultrafiltration of adult and aged mouse urine. When DB, BT, and IT were added to adult urine, the attraction of the urine was enhanced. Our results suggest that inbred aged male mice develop an aging odor that is attractive to female mice in an experimental setting and that this attraction is due to increased mouse pheromone signaling.     

Species-specific releaser effect of urine from ovulated female masu salmon and rainbow trout

MT (17α-methyltestosterone)-treated immature masu salmon Oncorhychus masou and rainbow trout Oncorhynchus mykiss , exposed to the urine of ovulated females in their non-reproductive season, made significantly more entries into the channel, of a Y-maze preference trough, conditioned by the urine of conspecific females than by heterospecifics. Immature, non-treated controls in both species showed no preference for the urine of ovulated females. These results suggest that, for both species, the releaser pheromones that attract males in the urine are species-specific. Therefore, utilization of species-specific chemical signals may be one of the mechanisms of the reproductive isolation in Oncorhynchus species.     

Schistosoma mansoni: Adult worm chemoattraction,with and without barriers

Heterosexual and homosexual chemoattraction studies were done with 8- to 12-week-old Schistosoma mansoni adults in linear chambers containing Earle's saline, in the absence and presence of both perforated and unperforated dialysis sac chimney barriers. In the absence of barriers attraction was seen in all heterosexual and homosexual combinations. After 90 min of observation at 37 C, organisms maintained at 4 or 37 C for at least 1 hr prior to the assay showed heterosexual attraction similar to those used immediately after perfusion. There was significantly more heterosexual attraction between worms from same than different pairs. In the presence of perforated barriers the greatest attraction was heterosexual, with males moving toward females; heterosexual attraction with females moving toward males was approximately equal to homosexual female attraction, and male homosexual attraction was not seen. In the presence of unperforated barriers the greatest attraction of females toward males occurred during the first 0.5 hr; within 3 to 4 hr females were no longer significantly attracted to males. However, after 0.5 hr males were more significantly attracted to females in unperforated than perforated chimneys. These studies demonstrate that adult schistosomes attract each other in vitro, and that there is a chemical basis for this attraction.     

Cross-Fostering of Male Mice Subtly Affects Female Olfactory Preferences

The maternal environment has been shown to influence female olfactory preferences through early chemosensory experience. However, little is known about the influence of the maternal environment on chemosignals. In this study, we used two inbred mouse strains, C57BL/6 (C57) and BALB/c (BALB), and explored whether adoption could alter male chemosignals and thus influence female olfactory preferences. In Experiment 1, C57 pups were placed with BALB dams. Adult BALB females then served as the subjects in binary choice tests between paired male urine odours (BALB vs. C57, BALB vs. adopted C57 and C57 vs. adopted C57). In Experiment 2, BALB pups were placed with C57 dams, and C57 females served as the subjects in binary choice tests between paired male urine odours (C57 vs. BALB, C57 vs. adopted BALB, and BALB vs. adopted BALB). In both experiments, we found that females preferred the urine of males from different genetic backgrounds, suggesting that female olfactory preferences may be driven by genetic compatibility. Cross-fostering had subtle effects on female olfactory preferences. Although the females showed no preference between the urine odours of adopted and non-adopted males of the other strain, the BALB females preferred the urine odour of BALB males to that of adopted C57 males, whereas the C57 females showed no preference between the urine odour of C57 and adopted BALB males. Using gas chromatography-mass spectrometry (GC-MS) and stepwise discriminant analysis, we found that the ratios of volatile chemicals from urine and preputial gland secretions were altered in the fostered male mice; these changes may have resulted in the behavioural changes observed in the females. Overall, the results suggest that female mice prefer urine odours from males with different genetic backgrounds; this preference may be driven by genetic compatibility. The early maternal environment influences the chemosignals of males and thus may influence the olfactory preferences of females. Our study provides additional evidence in support of genotype-dependent maternal influences on phenotypic variability in adulthood.     

Female preference in the context of male–male interactions in Maylandia zebra of Lake Malawi

The mbuna cichlids of Lake Malawi are a diverse, monophyletic, and recently derived clade. Sexual selection is thought to have accelerated their rapid diversification, though the mechanism by which this has occurred remains unknown. In this study, we examine the effect that male–male interactions have on female preference. We first used a short interaction experiment as a proxy for male dominance. We then measured female preference for (1) a single, isolated male; (2) a group of three, highly ranked males, relative to a group of lower ranked males; and (3) a group of three, mixed-ranked males against a similar group of mixed-rank males. We found that male dominance was highly correlated with male standard length. Female preference for male standard length and for dominance rank was significant in both isolated and group interactions. However, females only showed preference for groups of interacting males when males were segregated by dominance rank, not when groups were composed of both dominant and subordinate males. The results suggest that male–male contests influence female mating decisions. By investigating the rules that dictate the outcomes of such interactions we can elucidate the role that behavior plays in the diversification of this species-rich lineage.     

Male mate choice in a sexually cannibalistic species: male escapes from hungry females in the praying mantid <Emphasis Type="Italic">Tenodera angustipennis</Emphasis>

While competing males and choosy females may be common in animal mating systems, male choice can evolve under certain conditions. Sexual cannibalism is such a condition because of the high mortality risk for males. In mantids, female body condition is associated with male mate preference, with fat females preferred, due to at least two reasons: females in poor nutritional condition are likely to attack and predate males, and fat females can potentially increase the number of offspring. Thus, the risk of cannibalism and female fecundity can influence male mating behavior. In this study, we attempted to separate these factors by using the praying mantid Tenodera angustipennis to examine whether male preference for fat female mantids was based on avoiding sexual cannibalism (cannibalism avoidance hypothesis) or preference for female fecundity (fecundity preference hypothesis). The feeding regimes were experimentally manipulated to discriminate between the effects of female fecundity and female hunger status on male and female mating behaviors. We found that recently starved females more frequently locomoted toward the male, and that male abdominal bending was less intensive and escape was sooner from recently starved females. These female and male behavioral responses to female hunger condition may reveal male avoidance of dangerous females in this mantid.     

The influence of male dominance on social interactions in black ducks and mallards

The influence of male dominance on male-female social interactions was examined in black ducks, Anas rubripes, and mallards, A. platyrhynchos, that were raised from hatch in four different groups (male and female mallards; male and female black ducks; male mallards and female black ducks; male black ducks and female mallards). The mate preference of females, independent of the influence of male dominance, was determined by exposing females to four caged, isolated males, one from each different group. All females preferred the type of male they had been raised with since hatch. Females were then exposed to the same four males, now free-swimming, to determine how male dominance influenced the initial preference. Under these conditions, each female associated primarily with the most dominant of the four males, regardless of her initial mate preference. Mallards were the most dominant males in all tests. These results demonstrate that male dominance influences social interactions and is one factor contributing to hybridization between these two species.     

The Effects of Age and Previous Mating Experience on Pre- and Post-copulatory Mate Choice in Female House Crickets (<Emphasis Type="Italic">Acheta domesticus</Emphasis> L.)

Although females’ mating preferences are influenced by male characteristics, there are a number of factors intrinsic to females and unrelated to male phenotype that can modulate female choice. We assessed the effects of age and mating experience on mechanisms of pre- and post-copulatory mate choice in female house crickets, Acheta domesticus L., by randomly assigning males to females, but independently varying the age and number of previous matings of females at the time of experimental matings. Latency to mating, a measure of a female’s pre-copulatory preference, was influenced by female age at the time of mating, with older females mating sooner than younger females. The reduced selectivity of older females appears consistent with life-history theory, which predicts that the reproductive value of females should decline with age. The length of time that females retained the spermatophore after mating, a measure of a female’s post-copulatory mating preference, was not influenced by female age at the time of mating, the number of previous matings, or any interaction between the two main effects. Contrary to previous reports, male mass had no effect on either the latency to mating or female retention of the spermatophore in A. domesticus. We conclude that female age and mating experience can moderate female selectivity, but that their impact varies according to the mechanism by which females favor particular sires.     

Urine-marking activity of female mice under the influence of male urine odors

We conducted a study of the urine-marking activity of female mice when simultaneously exposed to urine odors from 2 kinds of males. Females, deposited a greater number of urine spots when presented with urine of normal, rather than castrated, males. Two androgen-dependent compounds known to be present in normal male urine enhanced female urine-marking when mixed with castrated male urine. These results are consistent with previous results concerning odor preference of females. However, females showed no marking preference between normal male urine and preputialectomized male urine, in spite of their preference for the former in our previous odor-preference study. Further experiments with various combinations of male urine revealed that females showed no marking preference when 1 of the 2 presented urine samples was from preputialectomized males, regardless of the other presented stimulus. We concluded that female urine marking is not a simple reflection of sexual preference, but possibly a phenomenon of a complex motivational system.     

Attraction thresholds and sex discrimination of urinary odorants in male and female aromatase knockout (ArKO) mice

We previously found that both male and female aromatase knockout (ArKO) mice, which cannot synthesize estrogens due to a targeted mutation of the aromatase gene, showed less investigation of volatile body odors from anesthetized conspecifics of both sexes in Y-maze tests. We now ask whether ArKO mice are in fact capable of discriminating between and/or responding to volatile odors. Using habituation/dishabituation tests, we found that gonadectomized ArKO and wild-type (WT) mice of both sexes, which were tested without any sex hormone replacement, reliably distinguished between undiluted volatile urinary odors of either adult males or estrous females versus deionized water as well as between these two urinary odors themselves. However, ArKO mice of both sexes were less motivated than WT controls to investigate same-sex odors when they were presented last in the sequence of stimuli. In a second experiment, we compared the ability of ArKO and WT mice to respond to decreasing concentrations of either male or female urinary odors. We found a clear-cut sex difference in urinary odor attraction thresholds among WT mice: WT males failed to respond to urine dilutions higher than 1:20 by volume, whereas WT females continued to respond to urine dilutions up to 1:80. Male ArKO mice resembled WT females in their ability to respond to lower concentrations of urinary odors, raising the possibility that the observed sex difference among WT mice in urine attraction thresholds results from the perinatal actions of estrogen in the male nervous system. Female ArKO mice failed to show significant dishabituation responses to two (1:20 and 1:80) dilutions of female urine, perhaps, again, because of a reduced motivation to investigate less salient, same-sex urinary odors. Previously observed deficits in the preference of ArKO male and female mice to approach volatile body odors from conspecifics of either sex cannot be attributed to an inability of ArKO subjects to discriminate these odors according to sex but instead may reflect a deficient motivation to approach same-sex odors, especially when their concentration is low.     

Sex attraction in Bactericera cockerelli (Hemiptera: Triozidae)

The potato psyllid, Bactericera (=Paratrioza) cockerelli (?ulc) (Hemiptera: Triozidae), is a major pest of potato. We examined the role of chemical signals in sex attraction, assessing male and female response to male- and female-produced volatile chemicals. In laboratory olfactometer assays, potato psyllid males were attracted to odorants emitted from live females and from solvent extract of females. These results indicate that the female-produced chemicals responsible for attracting males may be isolated by means of insect extractions. Males were also attracted to volatile chemicals from males and extracts of males, providing the first example of male-male attraction in the Psylloidea. Males exposed simultaneously to odorants from conspecific females and males were preferentially attracted to female odorants, suggesting the presence of a female-specific sex attractant for males. Potato psyllid females avoided volatile chemicals emitted by females and extracts of females and by volatile chemicals emitted by males and extracts of males. Possible explanations for avoidance of conspecifics by females are discussed. This study is the first report of male attraction to volatile chemicals emitted by females and female extracts in the Triozidae and more specifically in the potato psyllid.     

Sex recognition in zebrafish (<Emphasis Type="Italic">Danio rerio</Emphasis>)

We investigated sex recognition in female zebrafish (Danio rerio) to better understand the underlying sensory mechanisms and identify male secondary sexual traits. Females were simultaneously presented with two fish, a male and a female, in a flow-chamber apparatus, and females’ relative attraction towards males was observed under different conditions. With domesticated fish, females were more attracted to males when presented with both visual and chemosensory cues from stimulus fish. They still discriminated the sexes when only visual cues were provided, but not when white ambient light was changed to yellow, indicating that colour plays a role. Sex discrimination under yellow light was improved when chemosensory cues were also provided. Surprisingly, females’ attraction to males was not more pronounced in the morning when mating occurs. Domesticated females discriminated the sexes when presented with wild-derived, as well as domesticated fish, whereas wild-derived females did not show any biases for domesticated or wild-derived males. Behavioural observations indicated that the wild-derived females were distressed, which explains their lack of attraction to males. In summary, domesticated female zebrafish discriminated the sexes using both visual (body colour) and olfactory cues; however, wild-derived zebrafish were too distressed for behavioural experiments under these laboratory conditions.     

Postnatal differentiation of sexual preference in male pigs

Attraction to sexually mature males and the immobilization response were evaluated after postpubertal estrogen treatment of ovariectomized females and of males castrated within 48 hr after birth or at 4 or 8 months of age. The time spent in the end of an evaluation pen which housed a mature intact male, the proportion of animals that showed the immobilization response, and the latency to onset and the duration of this response were similar in ovariectomized females and males castrated within 48 hr after birth. These two groups spent more time in the male end of the evaluation pen as opposed to the opposite end which housed an ovariectomized female, showed a shorter latency to the onset of the immobilization response, and expressed this response for a greater number of days than males castrated either at 4 or 8 months of age. Males castrated at 4 or 8 months did not show a strong preference for either a mature male or an ovariectomized female. The immobilization response in estrogen-treated males castrated at 4 or 8 months of age diminished as these animals became older. On the basis of the observations made in this study, attraction to a mature, intact male is a sexually dimorphic behavioral trait in pigs, and defeminization of this trait in male pigs is associated with the pubertal increase in testicular steroid secretion. Presently, pigs are the only mammalian species in which a role has been identified for pubertal, testicular steroid secretion in the defeminization process.     

Repeatability of Male Mate Choice in the Mosquitofish, Gambusia holbrooki

Male mate choice has evolved in many species in which female fecundity increases with body size. In these species, males are thought to have been selected to favour mating with large females over smaller ones, thereby potentially increasing their reproductive success. While male mate choice is known to occur, it is less well studied than female mate choice and little is known about variation in mating preference among individual males. Here, we presented individual male eastern mosquitofish ( Gambusia holbrooki ) with paired females that differed in body size, and we quantified their mate preference on two consecutive days, allowing us to assess repeatability of preferences expressed. When males were allowed to view paired stimulus females, but not to acquire chemical or tactile cues from them, they exhibited a strong preference for large females over smaller ones. However, individual males were not consistent in the strength of their preference and repeatability was not significant. When individual males were allowed to fully interact with pairs of females, the males again exhibited a preference for large females over smaller ones, as revealed by a greater number of attempted copulations with large females than with smaller ones. In the latter social context, individual male preference was significantly repeatable. These results indicate that male eastern mosquitofish from our Florida study population possess, on average, a mating preference for larger females and that this preference is repeatable when males socially interact freely with females. The significant repeatability for mating preference, based on female body size, obtained for male mosquitofish in the current study is consistent with the presence of additive genetic variation for such preferences in our study population and thus with the opportunity for the further evolution of large body size in female mosquitofish through male mate choice.     

The trade-off between feeding, mate seeking and predator avoidance in copepods: behavioural responses to chemical cues

The behavioural responses of adult Temora longicornis to chemicalsignals from predators and potential sexual partners was studiedusing an automated three-dimensional (3-D) tracking system anda 2-D high-resolution filming set-up. The animals adapted theirswimming speed and turning behaviour in reaction to chemicalsignals to increase or decrease encounter probability with otherorganisms. Female copepods were shown to react to the smellof males with little ‘hops’, quite distinct fromboth their normal smooth swimming motion and escape responses.These hops are likely to be signals intended to increase theencounter probability with males. Swimming behaviour was shownto be a trade-off between conflicting motivations such as predatoravoidance on the one hand, and the search for food and sexualpartners on the other.     

Male and female preference for conspecifics in a fish with male parental care (Percidae: Catonotus)

Speciation by sexual selection is commonly modeled as the divergent co-evolution of male signals and female preferences in geographically isolated populations. Upon secondary contact, females fail to recognize divergent males as suitable mates and exhibit a strong preference for their own type. The result is behavioral isolation and, if behavioral isolation is strong enough, there is an absence of gene flow between two species. Growing evidence of both mutual and male choice challenges the conventional role of females as primary regulators of species boundaries; however, to date, few studies have explicitly compared males and females for conspecific preference. The relative contribution of the two sexes to species boundaries therefore remains poorly understood. We examined the strength of preference for conspecifics in both males and females using two closely related species of darters. Males in these species exhibit substantial parental investment; therefore, we hypothesized that selection for male choosiness would result in male preference for conspecifics comparable to females’. Results show that females exhibited strong and significant preference for conspecific males; whereas, male preference for conspecific females was highly variable. Some males showed a strong preference for conspecifics while others preferred heterospecifics or showed no preference, resulting in a non-significant mean preference for conspecifics. Therefore, despite considerable parental investment by males in this system, our results suggest females play a larger role in regulating species boundaries.     

Female Cowbird Song Perception: Evidence for Plasticity of Preference

The goal of the research reported here was to look for evidence of modifiability of preference for male song in female cowbirds, Molothrus ater. To this end, we investigated whether social experience affected the breadth and consistency of females’ playback preferences for geographic variants of male song. In three experiments, we varied female cowbirds’ exposure to males. Wild‐caught juvenile females showed a preference for local song in their first year when housed without males in sound‐attenuating chambers, as we had found previously with adult females. But we found that neither adult nor juvenile females showed a preference for local over distant song after they had been housed in large, outdoor aviaries with other females but without male residents. Aviary housing with local males did lead to preferences for local songs. These data represent the first unqualified evidence that adult and juvenile female cowbird preferences for song are modifiable. These data add to the growing body of literature suggesting that receivers, as well as signalers, rely on learning during development of their communication system.     

Reproductive biology of captive male cottontop tamarin monkeys as a function of social environment

The cottontop tamarin, Saguinus oedipus oedipus, is a cooperatively breeding monkey in which mature male and female offspring serve as helpers to assist in rearing younger siblings. Generally, only one female per social group reproduces; breeding restriction is mediated in postpubertal female offspring through low and acyclic levels of reproductive hormones. We investigated (1) reproductive activity of postpubertal male offspring, and (2) whether aggression towards male offspring and a cortisol-mediated stress response might restrict breeding of male offspring in the natal group. We examined sexual behaviour, olfactory communication and urinary hormone levels (testosterone, dihydrotestosterone, luteinizing hormone, cortisol) of the subject males while we manipulated their social environment from housing in natal groups to pairing with a novel female, and after the production of their own offspring. Mounting and erection rates of the male subjects were as high in the natal group as when paired with a novel female. However, most mounts in the natal group were directed towards other males, and complete copulation sequences did not occur with natal-group females. Social environment had no significant effect on olfactory investigation of breeding females. Although hormone levels increased significantly after the subjects were removed from the natal group, the elevation was transient; the hormone levels of subjects in their natal groups did not differ from the levels shown by the same males when successfully producing their own offspring. Male offspring received more contact aggression in the natal group than when paired with the novel female. However, most of the aggression was received from siblings rather than the breeding pair, and levels of cortisol did not correspond with levels of aggression. Thus, at both a behavioural and endocrine level, mature male offspring in captive natal groups were potentially fertile, but sexual activity with natal-group females appeared to be behaviourally restricted and directed instead towards group males. In wild cottontop tamarin groups, this reproductive potential may allow male helpers flexibility to respond to breeding opportunities. Copyright 2001 The Association for the Study of Animal Behaviour.