Mate Choice Tests Research Articles

Evaluating mate choice in the zebra finch

Finding reliable ways of assessing female mate choice is an essential prerequisite to understanding variation in female preferences and its impact on sexual selection. The zebra finch, Taeniopgyia guttata , is a classic avian model species for investigating mate choice and sexual selection, but to date virtually all work has been carried out using domesticated birds, and there are inconsistencies in the findings between studies. We tested three different methods for measuring female preferences in this species using both wild and domesticated birds. The first method was a traditional two-way mate choice chamber, where we measured the time spent with each male. The second method was a no-choice chamber where a single male and female were placed in the same cage for 5 min, such that the pair could physically interact, and the female's sexual response was recorded. The third method was an aviary set-up, comprising eight birds (four males and four females), and we recorded the number of pair-bonding behaviours observed over a 24-h period. In the aviary, we found that birds formed pair bonds almost exclusively with their own type (wild males paired with wild females, and domestic males paired with domestic females). In the two-way choice chamber, this assortative mating preference was only shown by domestic females, and in the no-choice test, only wild females showed this assortative mating preference. We discuss the possible reasons for these differences between mate choice tests and make recommendations for future studies on mate choice.

Living with the Past: Nutritional Stress in Juvenile Males Has Immediate Effects on their Plumage Ornaments and on Adult Attractiveness in Zebra Finches

The environmental conditions individuals experience during early development are well known to have fundamental effects on a variety of fitness-relevant traits. Although it is evident that the earliest developmental stages have large effects on fitness, other developmental stages, such as the period when secondary sexual characters develop, might also exert a profound effect on fitness components. Here we show experimentally in male zebra finches, Taeniopygia guttata, that nutritional conditions during this later period have immediate effects on male plumage ornaments and on their attractiveness as adults. Males that had received high quality food during the second month of life, a period when secondary sexual characteristics develop, were significantly more attractive as adults in mate choice tests than siblings supplied with standard food during this period. Preferred males that had experienced better nutritional conditions had larger orange cheek patches when nutritional treatments ended than did unpreferred males. Sexual plumage ornaments of young males thus are honest indicators of nutritional conditions during this period. The mate choice tests with adult birds indicate that nutritional conditions during the period of song learning, brain and gonad development, and moult into adult plumage have persisting effects on male attractiveness. This suggests that the developmental period following nutritional dependence from the parents is just as important in affecting adult attractiveness as are much earlier developmental periods. These findings thus contribute to understanding the origin and consequences of environmentally determined fitness components.

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.

Seasonal change in female choice for male size in the two-spotted goby

Mate choice may vary according to various factors, such as mate availability and variation in mate quality. We tested seasonal changes in female choice regarding male size in a marine fish, the two-spotted goby, Gobiusculus flavescens. In this species, males occupy nests in which females lay their eggs and males thereafter provide exclusive parental care of the eggs until hatching. Females are predicted to prefer large males if, for example, they are better at competing for and defending nests. In this species, the opportunity for females to be selective should decline over the breeding season as the availability of males decreases. We therefore predicted a reduction in female choosiness with season. We conducted mate choice tests, during the early (May) and later (June) part of the breeding season, in which females were allowed to choose between males differing in body length. Females chose large males early in the season, but became unselective with respect to male size later on. This change in mate choice may be caused by a reduction in overall choosiness as a result of the decline in male availability with season. Alternatively, the change could be caused by a switch in choice cues used by females if factors other than male size become more important for female reproductive success later in the breeding season. Further studies are needed to test between these alternative explanations.

Sexual selection for male parental care in the sand goby, Pomatoschistus minutus

Male parental care is typically thought to come at a cost to mate attraction and future mating success. However, it has also been hypothesized that paternal care may be under sexual, as well as natural, selection, such that good fathers actually attract more mates. Here we show experimentally that in the sand goby, Pomatoschistus minutus, females prefer to mate with males that provide higher levels of parental care. We manipulated male behavior using (1) different nest sizes and (2) an application of low-O2 water in the nests, and found that females consistently preferred males with elevated levels of care in dichotomous mate choice tests. This complements our earlier study in which we showed that males increase the amount and quality of care they provide in the presence of females. Our results demonstrate that male care may have evolved as a result of sexual selection rather than natural selection alone, and furthermore, that male care may not necessarily be in conflict with mate attraction.

NO REPRODUCTIVE ISOLATION BETWEEN FRESHWATER PULMONATE SNAILS PHYSA VIRGATA AND P. ACUTA

Abstract Mate choice tests provided no evidence of prezygotic reproductive isolation between a population of Physa virgata (Gould, 1855) collected from its type locality in the Gila River of Arizona and Physa acuta (Draparnaud, 1805) from a control site in Charleston, South Carolina. Reared in a no-choice experimental design, 10 outcross Arizona × South Carolina pairs initiated reproduction at approximately the same age as Arizona × Arizona controls, and earlier than South Carolina × South Carolina controls. Parents in the outcross experiment did not differ significantly from either control in their median weekly fecundity across 10 weeks of observation, yielding an F1 generation with significantly improved viability. We detected no evidence of reduction in F1 fertility. Thus, P. virgata, the most widespread freshwater gastropod of the American Southwest, should be considered a junior synonym of the cosmopolitan P. acuta.

Assortative Mating in Drosophila Adapted to a Microsite Ecological Gradient

Elucidating the causes of population divergence, and ultimately speciation, is a central objective of evolutionary biology. A number of previous studies of Drosophila populations from the Nahal Oren canyon (Mt Carmel, Israel) revealed significant interslope differences for a complex of fitness and behavioral traits. Peculiarities in courtship song patterns and nonrandom mating were observed, despite a small interslope distance. Single and multiple mate choice tests with D. melanogaster from the opposite slopes displayed highly significant assortative mating, with preference for sexual partners from the same slope. Here we report the results on mate choice in the sibling species D. melanogaster and D. simulans inhabiting Nahal Oren canyon. Significant assortative mating was found in both species. Genetic heterogeneity in mate choice was found among the isofemale lines of D. melanogaster. Samples of isofemale lines established from females collected in spring and fall seasons show the same mating patterns.

Female preference for symmetry in computer-animated three-spined sticklebacks, Gasterosteus aculeatus

Fluctuating asymmetries are subtle random deviations from perfect symmetry in bilateral traits caused by the inability of individuals to buffer their development against the disruptive effects of genetic and environmental stresses. The degree of asymmetry of secondary sexual characters is supposed to convey information about a male's phenotypic and/or genetic quality, and females may thus be expected to use bilateral symmetry as a cue in mate choice. We independently and simultaneously manipulated the length and the relative symmetry of the pelvic spines of computer-animated three-spined sticklebacks, Gasterosteus aculeatus. In all mate choice tests involving two male models differing in spine symmetry, females preferred the symmetric model, irrespective of spine length, though only significantly so when both male models had short spines. Females did not significantly discriminate between male models differing in spine length alone. The preference for symmetry was stronger the higher the females' physical condition. Our study demonstrates that female sticklebacks master the perceptual abilities required to discriminate between potential mates basing exclusively on small length differences between paired structures, and provides experimental evidence that spine symmetry is subject to sexual selection through female choice in this species.

POPULATION GENETICS OF ACCESSORY GLAND PROTEINS AND SEXUAL BEHAVIOR IN DROSOPHILA MELANOGASTER POPULATIONS FROM EVOLUTION CANYON

Evolution Canyon in Lower Nahal Oren, Mount Carmel, Israel has been identified as a location promoting sympatric speciation. Several previous studies on Drosophila melanogaster populations from the two disparate slopes of the canyon suggest that these two populations are experiencing incipient speciation. However, recent microsatellite data did not reveal the expected level of population differentiation. Given the importance of this system for studying speciation, we set out to test two predictions of the incipient speciation hypothesis—genetic differentiation and sexual isolation. We sequenced six different Acp genes from isofemale lines from the south-facing slope (11 lines) and north-facing slope (nine lines) of Evolution Canyon. We found no evidence of genetic differentiation between the two slopes (FST = −0.03). We also conducted mate choice tests, using intraslope F1 hybrids between different isofemale lines. There was no significant departure from random mating in mixtures of flies from the two slopes. Our results provide further indication that it is unlikely these two populations are experiencing incipient speciation. We discuss our results in light of the discrepancies that have been published on this enigmatic D. melanogaster system from Evolution Canyon.

Host-associated differences in emergence pattern, reproductive behavior and life history of Asteralobia sasakii (Monzen) (Diptera: Cecidomyiidae) between populations on Ilex crenata and I. integra (Aquifoliaceae)

We assessed potential adult longevity and male choice for a mate in two populations of Asteralobia sasakii associated with Ilex crenata and I. integra to test the hypothesis that interbreeding between these populations is prevented by the difference in emergence timing in the field. A previous study showed that the last day of adult emergence on I. integra and the first day of adult emergence on I. crenata were separated by six to 11 days. When adults were maintained in the laboratory with restricted flying, mating and oviposition, adults from both populations survived for four to five days, suggesting that the period when adults were active did not overlap between the two populations in the field. The mate choice test showed that males clearly approached females of the same host origin. These results suggest that the two populations have little chance of interbreeding even when they occur sympatrically. Other life history parameters such as the number of eggs in the ovary, daily emergence pattern, sex ratio and the duration of copulation also varied between the two populations. Our overall results strongly suggest that the two populations on different host plants can be referred to as distinct species.

The period gene and allochronic reproductive isolation in Bactrocera cucurbitae.

Clock genes that pleiotropically control circadian rhythm and the time of mating may cause allochronic reproductive isolation in the melon fly Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae). Flies with a shorter circadian period (ca. 22 h of locomotor activity rhythm) mated 5 h earlier in the day than those with a longer circadian period (ca. 30 h). Mate-choice tests demonstrated significant pre-mating isolation between populations with short and long circadian periods. Pre-mating isolation did not occur when the mating time was synchronized between the two populations by photoperiodic controls, indicating that reproductive isolation is due to variations in the time of mating and not any unidentified ethological difference between the two populations. We cloned the period (per) gene of B. cucurbitae that is homologous to the per gene in Drosophila. The relative level of per mRNA in the melon fly exhibited a robust daily fluctuation under light : dark conditions. The fluctuation of per expression under dark : dark conditions is closely correlated to the locomotor rhythm in B. cucurbitae. These results suggest that clock genes can cause reproductive isolation via the pleiotropic effect as a change of mating time.

Pleiotropic effect, clock genes, and reproductive isolation

AbstractThe mechanism by which a clock gene pleiotropically controlling life history and behavioral traits causes reproductive isolation is explained using a model species, the melon fly, Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae). Melon flies mate once a day, at dusk. The population selected for life history traits exhibits correlated responses in the time of mating during the day. For example, the fly populations selected for faster (slower) development have an earlier (later) time of mating. A circadian rhythm controls the time of mating. The circadian periods in constant darkness were about 22 h in lines selected for a short developmental period and about 31 h in lines selected for a long developmental period. The data on crosses between the selected lines indicated that the developmental period is controlled by a polygene, whereas the circadian period may be controlled by a single clock gene. These results suggest a clock gene pleiotropically controls developmental and circadian periods in the melon fly. Reproductive isolation may often evolve as an indirect (pleiotropic) consequence of adaptation to different environments or habitats. For example, niches that are temporally or seasonally offset can select organisms with different developmental characteristics. These developmental differences can inadvertently cause reproductive isolation by a variety of means including shifts in mating activity patterns. The difference in time of mating between populations selected for developmental period translated into significant prezygotic isolation, as measured by mate choice tests. If the mating time between populations differed more than 1 h, the isolation index was significantly higher than zero. These findings indicate that premating isolation can be established by a pleiotropic effect of a clock gene. There are many examples in which the difference in timing of reproduction prevents gene flow between populations, such as the egg spawning time in marine organisms, the flowering time in angiosperms, and the time of mating in insects. In such organisms, if genetic correlations between circadian rhythm and reproductive traits exist, multifarious divergent selection for life history traits would often accelerate the evolution of reproductive isolation through clock genes. Natural populations may diverge in reproduction time through drift, direct natural selection for time of reproduction, or as a by‐product effect of genetic correlations. In any case, clock genes are keys in reproductive isolation.

A test of speciation via sexual selection on female preferences

Sexual selection for divergent female preferences has been proposed to stimulate speciation. We tested this basic model by selecting for divergence in the courtship repertoire of the house fly Musca domestica L. Specifically, we subjected replicate strains to artificial selection for differentiation along the first two principal components of the phenotypic intercorrelation structure of five courtship traits. Highly significant differentiation in courtship repertoire resulted, and the magnitude of the selection response was highest along the first principal component (representing the ‘size’, or general intensity, of courtship). Videotaped matings of the crosses between divergent lines (i.e. males of one strain mating with females from a different line) showed that the selection responses in the intensities of male performances were due to shifts in female preferences. In particular, the males were able to accommodate the demands of ‘foreign’ females (as well as their own) in the no-choice situation (i.e. only one male and one female per mating chamber). In contrast to this plasticity of the males, the females were consistent in their differential resistance responses, regardless of the type of male involved in the courtship. Multiple-choice mate choice tests revealed significant reproductive isolation among some lines, although the effect was asymmetrical. The patterns of nonrandom mating were largely due to females from more genetically healthy lines (i.e. with overall high mating propensity) discriminating against males from populations with more inbreeding depression. We suggest that the inability to achieve true (symmetrical) reproductive isolation could have been due to low evolutionary potential in the ‘shape’ of courtship, as defined by the second principal component. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.

Sexual Imprinting on a Novel Adornment Influences Mate Preferences in the Javanese MannikinLonchura leucogastroides

We investigated whether sexual imprinting on an artificial novel adornment in the Javanese MannikinLonchura leucogastroides, a monomorphic estrildid finch, can occur and might provide a mechanism for the evolution of novel traits. We introduced a red feather on the forehead as a novel adornment. Young were raised by parents which were both adorned, which were both unadorned, or only one of which was adorned with the red feather. We tested the female and male offspring of those parents in mate choice tests with an adorned and unadorned conspecific of the opposite sex. Males raised by an adorned mother or adorned parents preferred adorned females significantly more often than males raised by unadorned parents. We conclude that males were sexually imprinted on the red feather. Females raised by an adorned mother or raised by adorned parents significantly preferred adorned males, whereas females raised by unadorned parents showed no preference for adorned males. Thus, females also became imprinted on the red feather. Males might learn the novel adornment in combination with the parent's sex or learn just the most conspicuous sex, whereas females showed a preference for the adornment independent of which sex bore the feather. Our study shows that sexual imprinting might be an effective mechanism for the evolution of a novel trait and that males and females might become imprinted on a novel trait in different ways.

MATING SUCCESS AND MALE COURTSHIP BEHAVIORS IN THREE POPULATIONS OF THE THREESPINE STICKLEBACK

Abstract Genetic and morphological studies indicated the existence of two phylogenetically distinct groups in the threespine stickleback, Gasterosteus aculeatus, around Japan. These two morphotypes were named as the Pacific Ocean group and the Japan Sea group, respectively. In the Pacific Ocean group, there are anadromous populations and populations that reside permanently in freshwater. This study presented the results of mate choice tests among three allopatric populations of Japanese threespine sticklebacks and we found significant evidence of assortative mating. A total of 226 mate choice test was carried out in 1995 and 1996. Ten courtship behaviors were collected and comparisons were made among three intrapopulational pairings. It was concluded that the Pacific Ocean group and the Japan Sea group have distinct behavioral characteristics. We also found effects of male size and female size on the probability of mating success between populations.

SEXUAL IMPRINTING SUPPORTS THE EVOLUTION OF NOVEL MALE TRAITS BY TRANSFERENCE OF A PREFERENCE FOR THE COLOUR RED

We investigated if sexual imprinting on birds with a red artificial trait can influence female preference for mates bearing other novel, i.e. not-imprinted traits in male Javanese mannikins (Lonchura leucogastroides). We tested two groups of females in mate choice tests. One group of females was sexually imprinted on parent birds adorned with a red feather on the forehead. The other group was raised by normal unadorned birds and was assumed to be sexually imprinted on the normal unadorned phenotype. Females could choose between unadorned and adorned males in simultaneous double choice tests. The adorned males were ornamented with three different kinds of artificial ornament, which differed from the learned red feather on the forehead in a specific manner. The novel traits were a blue feather which differed from the familiar red feather in colour only, red stripes at the tail which had the same colour as the red feather but differed in shape and position at the body, and blue stripes at the tail (same colour as the blue forehead feather), which were different from the red feather in all three qualities. Females which were sexually imprinted on the red feather showed a similar strong preference for the red stripes at the tail as for the learned red feather. These same females showed no preference for males bearing a blue feather on the forehead or for males bearing blue stripes at the tail. This shows that sexual imprinting on a red trait leads to a preference only for another novel red trait due to transference of a preference for the colour red. The control females which were raised by unadorned birds responded on average indifferently to males bearing any of the artificial traits, i.e. some females rejected adorned males, some females preferred adorned males. To latter females it seems that a novel male ornament is somewhat attractive independent of any previous learning. Sexual imprinting on the red feather can influence female mate preferences for mates bearing other novel artificial traits due to transference of a preference for the colour red. Transference of colour preference makes it possible to react to a stimulus that differs from the imprinting stimulus in size, shape or position and therefore might play an important role in the evolution of conspicuous male traits.

Cross-mating tests and the species status of Trissolcus basalis reared from the eggs of different heteropteran species.

Laboratory choice and no-choice cross-mating tests were conducted to establish whether Trissolcus basalis individuals from green vegetable bug, Nezara viridula, and nine other host species sharemating characteristics and belong to the same species. In no-choice cross-mating tests, all individuals in self- and out-crosses mated within 10 minutes. Although all females mated, they were not all inseminated successfully. However, a similar proportion of females was inseminated across all self- and out-crosses in each set of cross-mating tests. Mate-choice tests indicated that males and females selected mates at random. Overall, the results indicate that T. basalis individuals from the ten host species represent a single genetical species.

Female zebra finches prefer symmetrically banded males, but only during interactive mate choice tests

We used a four-arm choice chamber to investigate whether the symmetry of artificial traits (leg bands) influenced how attractive male zebra finches,Taeniopygia guttata, were to females, and whether a female’s preference was influenced by the opportunity to interact with males during choice tests. Females (N=10) were tested separately and moved freely between the chamber’s arms, each of which contained a male wearing bands (two per leg) in symmetric, asymmetric or cross-asymmetric configurations. In three of the six tests experienced by each female, one-way glass (mounted diagonally within each arm) prevented males from seeing the female or their own reflection. During the other three tests, transparent glass was used, so males could see and react to the female. A male’s band combination had a significant influence on the amount of time that females spent with him, but only during transparent-glass tests, where symmetric males were preferred. The results of our transparent-glass tests were similar to those reported by Swaddle & Cuthill (1994,Nature,367, 165–166), in a study where females selected between males that were interacting with their own mirror images (reflected by one-way glass). We discuss why females display the same apparent preference when tested with males engaged in intra- (Swaddle & Cuthill’s study) versus intersexual activities (our study). Since females in our study displayed a preference only when males could interact with them, caution may be required when extrapolating the results of static choice tests (e.g. involving models, one-way glass or video images) to situations where the participants can interact.

GENETIC CORRELATIONS BETWEEN LIFE-HISTORY AND BEHAVIORAL TRAITS CAN CAUSE REPRODUCTIVE ISOLATION.

Reproductive isolation may often evolve as an indirect (pleiotropic) consequence of populations adapting to different environments or habitats. For example, niches that are temporally or seasonally offset can select for organisms with different developmental characteristics. These developmental differences can inadvertently cause reproductive isolation by a variety of means including shifts in mating activity patterns. Here, we show a genetic correlation between a life-history trait (developmental period) and a behavioral trait (time of mating) that causes significant premating isolation in the melon fly, Bactrocera cucurbitae (Diptera: Tephritidae). Fly lines selected for short and long developmental periods differ in their preferred times of mating during the evening. This difference translates into significant prezygotic isolation, as measured by mate choice tests. If the time of mating between two populations differed more than one hour, the isolation index was significantly higher than zero. These indicate that premating isolation can be established if the developmental period is divergently selected for. If such genetic correlations are ubiquitous in many organisms, multifarious divergent selection for life-history traits would often accelerate the evolution of reproductive isolation. We speculate that reproductive isolation may have been evolved via genetic correlations among time-related traits, for example, developmental period and time of mating, as in other organisms.

Sexes of a monomorphic species differ in preference for mates with a novel trait

We investigated the different roles of the sexes in the origination of novel traits in the sexually monomorphic Javanese mannikin Lonchura leucogastroides. We introduced a red feather as an evolutionarily novel trait in both sexes and tested their preferences for prospective mates with this trait. Males rejected females bearing the red feather and preferred to court unadorned females. In contrast, females partly preferred adorned males. Specifically, previously unattractive males gained in attractiveness and could increase their reproductive success when bearing the ornament, whereas previously attractive males lost in attractiveness, but this did not affect their reproductive success. We introduced two other novel traits in males and investigated the females’ response to these in mate choice tests. Each of the three new traits interacted with the natural attractiveness of males. The more attractive a male was before ornamentation, the more it lost in attractiveness after ornamentation and vice versa. Thus, the position of the trait did not affect the interaction. Because males rejected adorned females and females partly preferred adorned males, novel traits might evolve by intersexual selection in males rather than in females. This can lead to a sexual dimorphism with conspicuous traits in males. Our study reveals a new insight into the mechanism of the evolution from monomorphism to dimorphism with ornamental traits in males.