Females Preferred Males Research Articles

Carotenoids, oxidative stress and female mating preference for longer lived males

Some of the most spectacular exaggerated sexual ornaments are carotenoid dependent. It has been suggested that such ornaments have evolved because carotenoid pigments are limiting for both signal expression and in their role as antioxidants and immunostimulants. An implicit assumption of this hypothesis is that males which can afford to produce more elaborate carotenoid-dependent displays are signalling their enhanced ability to resist parasites, disease or oxidative stress and hence would be predicted to live longer. Therefore, in species with carotenoid-dependent ornaments where a parent's future longevity is crucial for determining offspring survival, there should be a mating preference for partners that present the lowest risk of mortality during the breeding attempt, as signalled by the ability to allocate carotenoids to sexual displays. In an experimental study using three-spined sticklebacks (Gasterosteus aculeatus), we show that when dietary carotenoid intake is limited, males attempt to maintain their sexual ornament at the expense of body carotenoids and hence suffer from reduced reproductive investment and a shorter lifespan. These males also suffer from an increased susceptibility to oxidative stress, suggesting that this may constitute the mechanism underlying the increased rate of ageing. Furthermore, in pairwise mate-choice trials, females preferred males that had a greater access to carotenoids and chance of surviving the breeding season, suggesting that females can make adaptive mate choice decisions based on a male's carotenoid status and potential future longevity.

Preferences of female barking treefrogs, Hyla gratiosa, for larger males: univariate and composite tests

Body size is an important determinant of male mating success, and acoustic signals often contain information about size. Most playback experiments that have tested for female preferences for larger males have manipulated only single characteristics, even though size is often correlated with multiple signal attributes. We first determined which characteristics of the advertisement calls of male barking treefrogs were correlated with body size, then we used two-choice playback experiments to determine whether female choice for larger males was influenced by these characteristics. In univariate tests, we varied only one of three size-correlated call parameters (fundamental frequency, call amplitude, call duration) at a time. In composite tests, we varied all three characteristics simultaneously, using univariate regressions of each parameter on size to predict the values expected for each characteristic for small, medium and large males. In univariate tests, females preferred large over small males for call amplitude and duration, medium over small males for amplitude and fundamental frequency, and large over medium males for call amplitude. In composite playbacks, females preferred large males over medium and small males, and medium males over small males. Females thus showed clear preferences for larger males, especially in the composite tests. Comparisons between the results of the univariate and composite tests indicated that female preferences for larger males are mediated by a combination of call characteristics rather than any single trait. Reliance on a combination of traits may function to increase the probability that females select larger males despite weak correlations between body size and individual call characteristics.

Multimodal signalling: structural ultraviolet reflectance predicts male mating success better than pheromones in the butterfly Colias eurytheme L. (Pieridae)

In sexual selection, multimodal signals elicit mate choice when more than one sensory modality is activated. However, determining the relative use of each signal is difficult because it requires a comprehensive understanding of the mating system and how this system works under natural conditions. We examined the role of structural ultraviolet (UV) reflectance and pheromones in the butterfly Colias eurytheme. Both traits are important in mediating interspecific interactions and pheromones have been implicated in intraspecific mate choice. UV reflectance, which arises from the presence of a multilayer thin-film interference array, has potential as an honest indicator of male condition, viability and/or age. We investigated the relevance of these signal traits to courtship success by releasing virgin females in the path of free-flying males until each female had rejected and accepted at least one male. This design facilitated a within-subjects (females) analysis of mate choice, thus controlling for potentially confounding variation in intrinsic female receptivity. Principal component analysis indicated that variation across males in UV brightness and pheromones was essentially orthogonal. Females preferred younger males (as subjectively adjudged by wing wear), and while age covaried with UV brightness and almost all pheromone descriptors, UV brightness emerged as the best and most general predictor of male mating success. Our results suggest that this trait serves as an important intraspecific sexual signal in C. eurytheme, and they provide the clearest evidence to date regarding the functional relevance of structural coloration to female mate choice in butterflies. We discuss the preferential use of one secondary sexual characteristic (UV reflectance) over another (pheromones) with regard to evolutionary strategies.

Stabilizing function of sexual selection in relation to male aggressiveness in rodents

A series of experiments on water voles ( Arvicola terrestris L.) and outbred (Swiss) and inbred (BALB/c and C57BL/6) strains of house mice was performed to estimate the dependence of the attractiveness of male rodents on their aggressiveness. The results showed that females preferred males with intermediate aggressiveness indices, which proved to have higher reproductive capacity. The aggressiveness (aggressiveness index) was measured as the mean ratio of aggressive acts to the total number of social interactions between males placed in the same cage. The males were divided into four groups according to their aggressiveness indices: low-aggressive (with aggressiveness indices varying in different series from 0.00‐0.20, M = 0.13), mediumaggressive (0.45‐0.65, M = 0.55), aggressive (0.65‐0.85, M = 0.75), and high-aggressive (0.85‐1.00, M = 0.93). Olfactory attractiveness was estimated by attractiveness index calculated as the proportion of tests in which the stimulus of the given male (the bedding from its cage) was preferred by a female. The stimulus was considered preferred if a receptive female (at the late proestrus or estrus stage) explored it for a longer time than other stimuli. From 17 to 112 males were studied in individual experimental series. The dependence of the olfactory attractiveness of males on their aggressiveness was not monotonic (figure). Low-aggressive males were the least attractive for females (their mean attractiveness index was M = 0.14), and aggressive males were the most attractive ( M = 0.86). The attractiveness of high-aggressive males ( M = 0.51) was significantly lower than that of aggressive and about the same as that of medium-aggressive ( M = 0.49). Although linear approximation can be applied to the observed dependence of attractiveness on aggressiveness ( r 14 = 0.63, R 2 = 0.40, t = 3.07, p = 0.001), which explains the widespread opinion that it is monotonic, a fourth-degree polynomial approximation considerably better fits the observed dependence ( r 14 = 0.93, R 2 = 0.87, t = 9.81, p < 0.000001).

Mate Choice and Spawning Success in the Fighting FishBetta splendens: the Importance of Body Size, Display Behavior and Nest Size

AbstractCourtship displays should be exaggerated enough to attract mates and yet tempered so as not to deter them. We tested this hypothesis in the fighting fishBetta splendensby studying courtship displays and body size and their relationships with male parental quality and female fecundity, as well as the effects of display behavior and body size on mate choice decisions and spawning success. Because of their high degree of parental investment, males are expected to be discriminating in their choice of mates. Males who displayed more frequently built larger nests, a measure of parental quality, but larger males did not. When females were paired with males with high display rates, however, the pair had fewer eggs in their nest, even when accounting for female body mass. In a mate choice test using computer‐generated male stimuli that differed only in display behavior, females showed no preferences for displaying males vs. non‐displaying males, or for males with higher display rates vs. lower display rates. In similar tests in which the computer‐generated males differed only in size, females preferred larger males, but also preferred males that differed with respect to body size (negative assortative mating). Males preferred computer‐generated females that performed courtship displays over non‐displaying females, but showed no preferences for female body size. Neither a female's body size nor her display behavior was a significant predictor of her fecundity as estimated by the number of eggs released during spawning. Thus, our results suggest that femaleB. splendensmust balance male parental quality (nest size) with the risk of potentially disruptive or dangerous behavior during spawning, and that females may minimize these risks through negative size‐assortative mating. Female display behavior, while unrelated to fecundity in our study, may attract males because it indicates reproductive readiness or serves a species‐recognition function.

CALLING IS AN HONEST INDICATOR OF PATERNAL GENETIC QUALITY IN POISON FROGS

Several competing hypotheses have been put forward to explain why females of many species mate preferentially with males possessing the most conspicuous signals (e.g., ornaments, displays, or songs). We performed a laboratory experiment using two species of poison frogs, Dendrobates leucomelas and Epipedobates tricolor, to test the hypothesis that male calling performance is an honest indicator of parental quality. Our analyses are based on data from behavioral observations of mating activities of captive-reared individuals (and their offspring) that were housed in terraria for four consecutive breeding seasons. Male mating success increased with male calling rate and chirp duration in both species, suggesting that females preferred males with more elaborate calls. Because calling performance improved with age in D. leucomelas, female poison frogs that prefer males with more elaborate calls in the wild may end up mating with older males that have already proven their ability to survive. Females that mated with good callers obtained higher quality offspring. Eggs fertilized by males with high calling rates and long chirp durations had higher hatching success and produced tadpoles that were more likely to metamorphose into surviving frogs. As a consequence, females that mated with males with high calling performance obtained more surviving offspring per egg, compared to females that mated with poor callers. Collectively, our findings comply with the notion that female poison frogs prefer to mate with good callers because calling performance is a reliable predictor of offspring quality. The possible influence of maternal allocation and reasons for the strong effect size compared to previous studies are discussed.

AN EYE FOR DETAIL: SELECTIVE SEXUAL IMPRINTING IN ZEBRA FINCHES

To investigate the idea that sexual imprinting creates incipient reproductive isolation between phenotypically diverging populations, I performed experiments to determine whether colony-reared zebra finches would imprint on details of artificial white crests. In the first experiment, adults in one breeding colony wore white crests with a vertical black stripe, while in another colony adults wore crests having a horizontal black stripe; except for their crests, breeders possessed wild-type plumage and conformation. Offspring of both sexes reared in these colonies developed mate preferences for opposite-sexed birds wearing the crest type with which they were reared; neither sex developed a social preference for crested individuals of the same sex. In a second experiment, females reared by crested parents preferred crested males versus males with red leg bands, while control females (reared in a colony of wild-type, uncrested birds) preferred red-banded males in the same test. Results of a third experiment that used sexually dimorphic crest phenotypes indicate that both sexes of offspring imprinted on maternal crest patterns. Results support the hypothesis that sexual imprinting can facilitate isolation both by engendering a preference for population-typical traits and by prioritizing such an imprinting-based preference over species-typical preferences for other traits used in mate choice. Comparison with results of other recent studies indicates that imprinting tendencies of both sexes vary with the characteristics of traits presented as an imprinting stimuli. Tendency to imprint may vary with the perceived information content (e.g., kin, sex, or population indicator) of parental traits, a process dubbed selective sexual imprinting.

AN EYE FOR DETAIL: SELECTIVE SEXUAL IMPRINTING IN ZEBRA FINCHES

To investigate the idea that sexual imprinting creates incipient reproductive isolation between phenotypically diverging populations, I performed experiments to determine whether colony-reared zebra finches would imprint on details of artificial white crests. In the first experiment, adults in one breeding colony wore white crests with a vertical black stripe, while in another colony adults wore crests having a horizontal black stripe; except for their crests, breeders possessed wild-type plumage and conformation. Offspring of both sexes reared in these colonies developed mate preferences for opposite-sexed birds wearing the crest type with which they were reared; neither sex developed a social preference for crested individuals of the same sex. In a second experiment, females reared by crested parents preferred crested males versus males with red leg bands, while control females (reared in a colony of wild-type, uncrested birds) preferred red-banded males in the same test. Results of a third experiment that used sexually dimorphic crest phenotypes indicate that both sexes of offspring imprinted on maternal crest patterns. Results support the hypothesis that sexual imprinting can facilitate isolation both by engendering a preference for population-typical traits and by prioritizing such an imprinting-based preference over species-typical preferences for other traits used in mate choice. Comparison with results of other recent studies indicates that imprinting tendencies of both sexes vary with the characteristics of traits presented as an imprinting stimuli. Tendency to imprint may vary with the perceived information content (e.g., kin, sex, or population indicator) of parental traits, a process dubbed selective sexual imprinting.

Tactile contact is required for early estrogen treatment to alter the sexual partner preference of female zebra finches

Sex steroid actions during early development appear to play a role in the development of sex differences in sexual partner preference (SPP, preference for males vs. females) in several species of mammals and in the socially monogamous pair bonding zebra finch ( Taeniopygia guttata). Female finches treated with estrogen as nestlings exhibit varying degrees of masculinized SPP as adults, but only if they have been housed in all-female groups during the juvenile and young adult period, suggesting that the estrogen effect may involve social experience and possibly sexual imprinting. Because tactile contact is important for consolidation of imprinted preferences in this species, it was predicted that early estrogen treatment would alter preferences of females only if they were allowed to have tactile contact with other females. Subjects were injected with estradiol benzoate or with oil (normal controls) daily for the first 2 weeks post-hatching. At age 45 days, they were housed in a mixed sex aviary (normal controls), in an all-female aviary allowing tactile contact (group EB-TC), or in an all-female aviary with no tactile contact (group EB-NTC). At 100+ days, birds were given two-choice SPP tests followed by aviary tests of SPP. EB-TC females did not show the sex-typical preference for male stimuli, and differed significantly from the controls on several measures. EB-NTC females preferred males and never differed significantly from controls. These results show that tactile contact after age 45 days is essential for an EB effect on SPP, supporting the hypothesis that hormones and sexual imprinting together contribute to SPP.

The role of ultraviolet wavelengths in the mate-choice decisions of female three-spined sticklebacks

Female three-spined sticklebacks have been found to use visual cues when responding sexually towards courting males, often preferring more intensely red-coloured males, and males with blue rather than silver irises. However, traditionally the literature has failed to test preference across the full spectral range to which females might be sensitive, limiting analysis to the human-visible wavelengths of the electromagnetic spectrum. We studied the effects that the addition of ultraviolet wavelengths has on the mate-choice preferences of female sticklebacks using a two-choice paradigm. We found that females preferred males that were viewed across the full spectrum to males whose display lacked an ultraviolet component. Using suitable controls we were able to establish that female preference was sexually motivated and was not caused by a general preference for the manipulated light conditions. Our results indicate that female preference may be due to an enhancement in visual contrast when males are viewed in full spectrum conditions.

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.

Effects of male body size on mating activity and female mate refusal in the yellow-spotted longicorn beetle, Psacothea hilaris (Pascoe) (Coleoptera: Cerambycidae): Are small males inferior in mating?

In the yellow-spotted longicorn beetle, Psacothea hilaris (Pascoe), variation in body size is conspicuous, especially in males. Size-related difference in male response to females and dummies treated with female extract were examined in the laboratory. Smaller males more frequently located and mounted females than did larger males when introduced to females. Smaller males responded to dummies treated with lower doses of female extract. This result indicates that small males were more sensitive to female sex pheromone and more active in their mating search and pre-copulatory behavior. However, females preferred large males to small ones. They displayed mate refusal behavior to small males much more frequently than to large males. A higher sensitivity to sex pheromone and subsequently higher copulatory activity in small males may compensate for the disadvantage of lower female choice. This hypothesis was supported by a field investigation: body size distributions were not significantly different between mounting males and solitary males.

Vocal mimicry by the Black‐browed Reed Warbler Acrocephalus bistrigiceps: objective identification of mimetic sounds

Vocal mimicry by the Black‐browed Reed Warbler Acrocephalus bistrigiceps was investigated. To identify mimicry objectively, we measured similarities between the sounds of models and those of Warblers by means of Principal Component Analysis (PCA) using a set of acoustic parameters. Of the sounds suspected of being mimicry according to visual inspection of sonagrams, only 57% were identifiable as mimicry according to PCA. Previous studies have not included quantitative criteria for assessing vocal mimicry, and our results suggest that judgements might not be reliable in the absence of objective criteria. Male Warblers incorporated the mimetic sounds into their songs, and each male mimicked 2–5 species. We found no evidence that females preferred males with large mimetic repertoires. This suggests that vocal mimicry has not evolved in response to selection by females in this species, although our analysis did not reveal entire mimetic repertoires in the Warbler songs.

Courtship in fast water currents by a male stream goby ( Rhinogobius brunneus ) communicates the parental quality honestly

The stream goby Rhinogobius sp. DA (dark color type) shows exclusive paternal care of the eggs. Males court females in the stream current and previous field observations suggest that females favor males that perform their courtship display in faster water currents, and that such males may have high parental ability because of good physical condition. To validate these observations we examined female choice under controlled laboratory conditions. Mate choice experiments indicated clearly that females preferred males that courted in the faster currents, whereas neither sexually different morphological traits, such as body size, nor the water current alone were important. The experiments with food supply treatments indicated that only males of high physical condition are able to court in the fast currents. Furthermore, males that courted in the fast currents achieved good egg survival, whereas males that were unable to court in the currents did not, due to cannibalism of their egg clutch. Thus, the maximum speed of the water current in which a male courts should be indicative of his quality and of the subsequent survival of eggs under his care. We conclude that Rhinogobius sp. DA females utilize the male courtship display in the water current as an honest indicator of parental quality.

Female sticklebacks Gasterosteus aculeatus use self-reference to optimize MHC allele number during mate selection

Theoretical and empirical studies suggest that an optimal resistance to pathogens and parasites requires an optimal number of MHC alleles per individual. Here we argue that three-spined sticklebacks (Gasterosteus aculeatus) achieve this goal by applying a strategy that involves a self-referential process. According to this model, females complement their own set of alleles with a more or less diverse set of male alleles such that the combined diversity reaches an optimum. In previous experiments, we have identified allele counting as a major mate-choice strategy in large populations. The self-referential allele-counting hypothesis predicts that MHC-based mate choice favors dissimilar MHC alleles in small populations facing the risk of inbreeding. Therefore, we conducted an experiment that simulated a small effective population size with low MHC class-II diversity. Our experiments are based on the analysis of MHC class-IIB alleles that explain a major part of the overall MHC diversity in sticklebacks, as determined by mathematical modeling. The results show that females preferred males with dissimilar alleles. Our present and the previous studies (which we reanalyzed with respect to our new predictions) show that irrespective of high or low population diversity faced by female sticklebacks for their mate choice, they use information about their own and their potential mate's MHC polymorphism for optimal complementation of their own set of alleles. From combining the data of the previous and the present experiment we found that female sticklebacks try to achieve an optimum number of MHC class-IIB alleles for their offspring through mate choice. The chosen MHC diversity is close to the most frequent diversity found naturally in individual fish, which in addition have the lowest parasite burden.

Environmental variation and the maintenance of polymorphism: the effect of ambient light spectrum on mating behaviour and sexual selection in guppies

AbstractThe intensity of sexual selection is influenced by environmental conditions because these conditions influence signal propagation and the risks of the signal being exploited by predators and parasites. We explore the possibility that spatial or temporal heterogeneity in environmental signalling conditions (in this case light spectrum) may induce fluctuating sexual selection on male behaviour and ornamentation in guppies. We used shade cloth and filters to experimentally manipulate light spectrum, mimicking conditions found naturally: early morning/late afternoon light (SC treatment), midday forest shade (F89 filter treatment) and midday woodland shade (F55 filter treatment). Females were more responsive to male courtship and males were less likely to attempt sneak copulations under F55 light than the other two treatments. By contrast, male display rate was not influenced by treatment. Females tended to prefer the same males under SC and F55 light, but attractiveness in these treatments was unrelated to attractiveness under F89 light. There were similarities among treatments in the traits that females preferred: females preferred males with larger areas of orange in all three treatments. There were, however, also some differences, including preference for larger males under F89 light and for smaller males under the other treatments. Overall, the influence of ambient light spectrum on the relative importance of mate choice and male sneak copulation may have important implications for the mode and strength of sexual selection in different environments. The findings on attractiveness and preference functions, however, suggest that light spectrum only weakly affects the direction of sexual selection by female choice.

INTERACTIONS AMONG MECHANISMS OF SEXUAL SELECTION ON MALE BODY SIZE AND HEAD SHAPE IN A SEXUALLY DIMORPHIC FLY

Darwin envisaged male-male and male-female interactions as mutually supporting mechanisms of sexual selection, in which the best armed males were also the most attractive to females. Although this belief continues to predominate today, it has been challenged by sexual conflict theory, which suggests that divergence in the interests of males and females may result in conflicting sexual selection. This raises the empirical question of how multiple mechanisms of sexual selection interact to shape targeted traits. We investigated sexual selection on male morphology in the sexually dimorphic fly Prochyliza xanthostoma, using indices of male performance in male-male and male-female interactions in laboratory arenas to calculate gradients of direct, linear selection on male body size and an index of head elongation. In male-male combat, the first interaction with a new opponent selected for large body size but reduced head elongation, whereas multiple interactions with the same opponent favored large body size only. In male-female interactions, females preferred males with relatively elongated heads, but male performance of the precopulatory leap favored large body size and, possibly, reduced head elongation. In addition, the amount of sperm transferred (much of which is ingested by females) was an increasing function of both body size and head elongation. Thus, whereas both male-male and male-female interactions favored large male body size, male head shape appeared to be subject to conflicting sexual selection. We argue that conflicting sexual selection may be a common result of divergence in the interests of the sexes.

Interaction between natural and sexual selection during the evolution of mate recognition.

The interaction between natural and sexual selection is central to many theories of how mate choice and reproductive isolation evolve, but their joint effect on the evolution of mate recognition has not, to my knowledge, been investigated in an evolutionary experiment. Natural and sexual selection were manipulated in interspecific hybrid populations of Drosophila to determine their effects on the evolution of a mate recognition system comprised of cuticular hydrocarbons (CHCs). The effect of natural selection in isolation indicated that CHCs were costly for males and females to produce. The effect of sexual selection in isolation indicated that females preferred males with a particular CHC composition. However, the interaction between natural and sexual selection had a greater effect on the evolution of the mate recognition system than either process in isolation. When natural and sexual selection were permitted to operate in combination, male CHCs became exaggerated to a greater extent than in the presence of sexual selection alone, and female CHCs evolved against the direction of natural selection. This experiment demonstrated that the interaction between natural and sexual selection is critical in determining the direction and magnitude of the evolutionary response of the mate recognition system.

Does paternity or paternal investment determine the level of paternal care and does female choice explain egg stealing in the fifteen-spined stickleback?

An earlier field study on the fifteen-spined stickleback (Spinachia spinachia) showed that frequent male--male interactions result in high frequencies of sneaking and egg stealing. Moreover, sneaking behavior was performed not only by males adopting alternative mating strategies, but also by males with their own nests. The advantage of sneaking is easily understood, but it is more difficult to explain the evolutionary benefit of stealing eggs from other males. I investigated whether males suffering from sneaking adjust their paternal effort in relation to their degree of paternity. I also examined whether females prefer males that have more eggs in their nests, as this could explain egg stealing. There was no relationship between the degree of paternity and fanning activity, hatching success, or nest defense. However, the older the eggs become, the more the males increase their attack rate toward potential egg predators (goldsinny wrasse and shore crabs). Thus, males adjusted their level of defense to the amount of energy and time already invested in the clutch. Females did not prefer males with more eggs in their nests. On the contrary, females preferred males with reduced clutches over males with enlarged clutches. Therefore, female choice is unlikely to be a driving force behind egg stealing in this species. Copyright 2002.

Experimental manipulation of male eggspots demonstrates female preference for one large spot in Pseudotvopheus lombavdoi

Females of the Lake Malawi cichlid Pseudotropheus lombardoi preferred males with one eggspot, the natural number, on their anal fin compared to males with two eggspots which had been artificially manipulated in number. Furthermore by manipulating the size of the eggspot. it was found that females preferred males with one large eggspot to males with one small eggspot. These results indicate that female preferences are responsible for the single eggspot in P. lombardoi and that this may be linked to species recognition as females of closely related species appear to exhibit different preferences for male eggspots.