Sneak Copulation Research Articles

Video evidence of mountings by female‐plumaged birds of paradise (Aves: Paradisaeidae) in the wild: Is there evidence of alternative mating tactics?

AbstractThe bewildering courtship phenotypes of male birds of paradise (Paradisaedae) represent a classic example of sexual selection through mate choice. While the majority of sexual selection studies have focused on either mate choice or intrasexual competition, males across a variety of taxa adopt alternative mating tactics as additional means of obtaining fertilization when they are otherwise unable to. For example, across various polygynous birds, subordinate males engage in sneak copulations, which may offset the fitness costs of prolonged subordinate periods. Despite exhibiting strong mating skews and male delayed plumage maturation, reports of sneak copulation in the birds of paradise are exceedingly rare. After reviewing an extensive video collection of courtship interactions, we found examples of mountings by female‐plumaged birds in three birds of paradise species: the Western parotia Parotia sefilata, Carola's parotia Parotia carolae, and the magnificent bird of paradise Cicinnurus magnificus. While homosexual mountings by females have been documented previously in Lawes' parotia P. lawesii, adult males in the magnificent bird of paradise violently attacked intruding female‐plumaged birds attempting to mount receivers, suggesting that they may be immature males engaging in alternative mating tactics. Overall, the rare video footage described here is suggestive of two fascinating, yet unexplored phenomena in polygynous birds: alternative mating tactics and female homosexual behaviour.

Male guppies compensate for lost time when mating in turbid water

Turbidity (a measure of the cloudiness of water) decreases the visual range of organisms, altering interactions within and between species. For species that visually assess mates, turbidity may affect mating interactions and mate choice. A central question, then, is to what degree organisms plastically adjust mating behaviors to cope with visually altered environments. Here, we investigate the effect of turbidity on the mating behavior of guppies (Poecilia reticulata) in Trinidad, where some streams are increasingly turbid due to upstream rock quarrying. We collected fish from two highly turbid streams (with upstream rock quarries) and two pristine streams (no upstream quarries) in the same drainages. We then observed male mating behaviors with females from the same populations in both turbid and clear assays, recording displays and sneak copulation attempts. Males from turbid streams showed greater individual consistency in mating behaviors. But regardless of provenance, male guppies spent less time associating with females in turbid water overall. When males and females did interact, however, males greatly increased the rate of all mating behaviors in turbid as compared to clear water. Thus, even when lacking a long-term evolutionary history with high turbidity, guppies compensate for lost time when mating in a visually altered environment. Given the global nature of increases in turbidity, understanding behavioral responses to this aquatic anthropogenic change is critical. Here, we investigate the degree to which Trinidadian guppy males in affected areas are able to plastically compensate in turbid water by adjusting mating behaviors. We also test the degree to which previous chronic exposure to turbidity alters this plasticity. In contrast to predictions, we did not find population differences in plasticity; across all populations, however, we found significant plasticity in the guppy mating system in response to anthropogenically increased turbidity. While males spent less time associating with females in turbid water overall, males increased mating effort during periods of association, compensating for lost time in turbid water. We discuss this plasticity and the implications for guppy sexual selection and secondary sexual characteristics such as coloration.

Female social response to male sexual harassment in poeciliid fish: a comparison of six species.

Sexual harassment is common among poeciliid fish. In some fishes, males show a high frequency of sneak copulation; such sexual activity is costly to the females in terms of foraging efficiency. In mosquitofish (Gambusia holbrooki), when males are present, the distance between females tends to decrease, and this behavior has been interpreted as an adaptive strategy to dilute the costs of male sexual activity. In this study, the tendency to reduce distance in the presence of a male has been investigated in females of six poeciliid species (Girardinus metallicus, Girardinus falcatus, G. holbrooki, Poecilia reticulata, Xiphophorus hellerii, and Xiphophorus mayae) that exhibit different male mating strategies and different levels of sexual activity. Results revealed large interspecific differences in the pattern of female aggregation. Females of species with a high frequency of sneak copulations tended to reduce their social distance in the presence of a male. By contrast, species that rely mainly on courtship showed little or no variation in social distance. The proportion of sneak copulations predicts the degree of variation in female social response, but the amount of total sexual activity does not, suggesting that the change in females' social distance when a male is present may indeed serve to reduce the costs of male sexual harassment.

Male Mating Posture and Courtship Coloration of the Temperate Marine Tubesnout,Aulorhynchus flavidus(Gill)

Species that engage in sexual reproduction often exhibit dynamic physical features and behavioral actions that serve to signal conspecifics. Body posture, vocalizations or the incorporation of bright coloration are typically used to establish dominance (Wiley 1973, Warner 1975, Clarke and Faulkes 1997, Peterson and Jacobs 2002) alert conspecifics of nearby threats or foraging opportunities (Godin and Morgan 1985, Beauchamp and Heeb 2001, Le Roux et al. 2009, Townsend et al. 2011) and for breeding purposes (Wiley 1973, Hagen et al. 1980, Christy 1983, Gibson 1989, DeMartini and Sikkel 2006). In many species females select a male based on their behavioral display of some desirable trait or their ability to express dominance or competitive superiority over other potential mates (DeMartini and Sikkel 2006). Such criteria are often not mutually exclusive in that particular features or actions may act to deter competitor males while simultaneously attracting females (Hagen et al. 1980, Cairns 1982). Understanding such physical characteristics or behavioral signals improves our knowledge of reproductive systems within and among taxonomic groups. Reproductive strategies have been well documented in the marine realm, including monogamous pairs (Whiteman and Cote 2004), large broadcast breeding aggregations (Coleman et al. 1996, Colin 1996, Carolsfeld et al. 1997), sneak copulation (Pilastro and Bisazza 1999, Hurtado-Gonzales and Uy 2010) and nesting species (Limbaugh 1964, Wiley 1973). Limbaugh (1962) previously described the nesting habitat for the temperate marine tubesnout, Aulorhynchus flavidus (Gill), but male mating behavior has not been characterized. A proposed description of male mating behavior is reported here from observations of A. flavidus on display at the Aquarium of the Pacific (AOP) in Long Beach, California during early May, 2013. Male A. flavidus pelvic fins are red in color (Fig. 1A) and are thought to remain that way year round (Love 2011). The heads of males are also dark blue to black with a prominent iridescent blue patch on their snout (Fig. 1B). Iridescent blue spots/coloration have also been observed along the full body length of males (Love 2011) while females are a drab brownish color throughout (Fig. 2). Although typically found at depths of 20 m, and as deep as 37 m (Love 2011), the preferred nesting habitat of A. flavidus is the upper blades of the macrophyte Macrocystis pyrifera. While bright coloration is common to tropical waters, it is disfavored in temperate marine habitats due to low light penetration at depth. The conspicuous coloration of males may be apparent only when actively breeding in the upper water column where red light is still present. It appears the pelvic fins are often folded up against the body (Fig. 1B) and covered partially by the pectoral fins when they are not actively displaying them. The anterior underside of male threespine stickleback (Gasterosteus aculeatus), another gasteriform species, are also red (Hagen et al. 1980) and both species breed in shallower water than they are typically found (,20– 30 m depth). Similarities in external morphology despite differences in breeding habits Bull. Southern California Acad. Sci. 113(3), 2014, pp. 176–179 E Southern California Academy of Sciences, 2014

Individual Variation in Male Size and Behavioral Repertoire in the Sailfin Molly Poecilia latipinna

AbstractVariation among individuals in the expression of behaviors and associations of behaviors in different contexts can lead to the maintenance of behavioral polymorphisms. Individual variation in morphology is often associated with behavioral polymorphism, yet the degree to which morphology predicts behavioral phenotype is not well understood. We measured individual variation in size and behaviors in the sailfin molly, Poecilia latipinna, by comparing the behavior of individual males of different sizes across four different contexts (mating, exploratory tendency, sociability, and predator inspection). We also investigated the degree to which male size, a fixed genetic trait, influenced the expression of each behavior and associations between behaviors. We found that male mollies show strong associations between certain behaviors and only some of these are predicted by male size. For example, size has a strong influence on the courtship‐boldness axis with larger males showing higher rates of courtship displays and being bolder in predator inspection. A positive association was found between exploratory tendency, sociability, and gonopodial thrusting rates, yet the expression of these behaviors was independent of male size. Thus, sailfin mollies, like many fish species, show associations of behaviors that contribute to differences among males in personality type. The fixed genetic effect of male size at maturity influences courtship and boldness, but individual variation in exploratory tendency, sociability, and sneak copulation attempts through gonopodial thrusts is independent of male size. Such variation among males in behavioral associations within and between different contexts may slow the rate at which populations of P. latipinna can diverge in individual behaviors.

Comparison of Mating Behavior and Offspring Production Success of the Guppy, Poecilia reticulata, Stocked Under Different Operational Sex Ratios

Experiments were conducted to record mating behavior (Experiment 1) and offspring production (Experiment 2) in the guppy, Poecilia reticulata, stocked under different operational sex ratios. Male and female guppies were stocked in aquaria (Experiment 1) and in concrete tanks (Experiment 2) at sex ratios (male:female) of 2:1 (Treatment 1), 1:1 (Treatment 2), and 1:2 (Treatment 3). Courtship displays were significantly less in Treatment 3 (P < 0.05). Sneak copulation was highest in Treatment 1 (P < 0.05). Time spent by the focal female on feeding was highest in Treatment 3 and lowest in Treatment 1 (P < 0.05). Offspring production per female, initial weight of offspring, and growth values recorded for the adult female fish were highest in Treatment 3 (P < 0.05). Weight and survival rate of offspring produced from each experiment was highest in Treatment 3 (P < 0.05). Treatment 3 appeared to be the most viable in terms of both quality and quantity of offspring produced. The results indicate a female biased sex ratio (adult male:female, 1:2) to be more effective than a male biased or an evenly matched sex ratio for enhanced offspring production in the guppy.

Intrasexual competition facilitates the evolution of alternative mating strategies in a colour polymorphic fish

BackgroundIntense competition for access to females can lead to males exploiting different components of sexual selection, and result in the evolution of alternative mating strategies (AMSs). Males of Poecilia parae, a colour polymorphic fish, exhibit five distinct phenotypes: drab-coloured (immaculata), striped (parae), structural-coloured (blue) and carotenoid-based red and yellow morphs. Previous work indicates that immaculata males employ a sneaker strategy, whereas the red and yellow morphs exploit female preferences for carotenoid-based colours. Mating strategies favouring the maintenance of the other morphs remain to be determined. Here, we report the role of agonistic male-male interactions in influencing female mating preferences and male mating success, and in facilitating the evolution of AMSs.ResultsOur study reveals variation in aggressiveness among P. parae morphs during indirect and direct interactions with sexually receptive females. Two morphs, parae and yellow, use aggression to enhance their mating success (i.e., number of copulations) by 1) directly monopolizing access to females, and 2) modifying female preferences after winning agonistic encounters. Conversely, we found that the success of the drab-coloured immaculata morph, which specializes in a sneak copulation strategy, relies in its ability to circumvent both male aggression and female choice when facing all but yellow males.ConclusionsStrong directional selection is expected to deplete genetic variation, yet many species show striking genetically-based polymorphisms. Most studies evoke frequency dependent selection to explain the persistence of such variation. Consistent with a growing body of evidence, our findings suggest that a complex form of balancing selection may alternatively explain the evolution and maintenance of AMSs in a colour polymorphic fish. In particular, this study demonstrates that intrasexual competition results in phenotypically distinct males exhibiting clear differences in their levels of aggression to exclude potential sexual rivals. By being dominant, the more aggressive males are able to circumvent female mating preferences for attractive males, whereas another male type incorporates subordinate behaviours that allow them to circumvent male aggression and female mating preferences. Together, these and previous results indicate that exploiting different aspects of social interactions may allow males to evolve distinct mating strategies and thus the long term maintenance of polymorphisms within populations.

THE EFFECTS OF GENOTYPE, AGE, AND SOCIAL ENVIRONMENT ON MALE ORNAMENTATION, MATING BEHAVIOR, AND ATTRACTIVENESS

The traits thought to advertise genetic quality are often highly susceptible to environmental variation and prone to change with age. These factors may either undermine or reinforce the potential for advertisement traits to signal quality depending on the magnitude of age-dependent expression, environmental variation, and genotype-age and genotype-environment interaction. Measurements of the magnitude of these effects are thus a necessary step toward assessing the implications of age dependence and environmental variability for the evolution of signals of quality. We conducted a longitudinal study of male guppies (Poecilia reticulata) from 22 full-sibling families. Each fish was assigned at maturity to one of three treatments in order to manipulate his allocation of resources to reproduction: a control in which the male was kept alone, a courtship-only treatment in which he could see and court a female across a clear partition, and a mating treatment in which he interacted freely with a female. We measured each male's size, ornamental color patterns, courtship, attractiveness to females, and mating success at three ages. Size was influenced by treatment and age-treatment interactions, indicating that courtship and mating may impose costs on growth. Tail size and color patterns were influenced by age but not by treatment, suggesting fixed age-dependent trajectories in these advertisement traits. By contrast, display rate and attempted sneak copulation rate differed among treatments but not among ages, suggesting greater plasticity of these behavioral traits. As a result of the different patterns of variation in ornamentation and behavior, male attractiveness and mating success responded to male age, treatment, and the interaction between age and treatment. Neither age nor treatment obscured the presence of genetic variation, and the genetic relationship between male ornamentation and attractiveness remained the same among treatments. Our findings suggest that neither age-dependent variation nor environmentally induced variation in reproductive effort is likely to undermine the reliability of male signaling.

THE EFFECTS OF GENOTYPE, AGE, AND SOCIAL ENVIRONMENT ON MALE ORNAMENTATION, MATING BEHAVIOR, AND ATTRACTIVENESS

The traits thought to advertise genetic quality are often highly susceptible to environmental variation and prone to change with age. These factors may either undermine or reinforce the potential for advertisement traits to signal quality depending on the magnitude of age-dependent expression, environmental variation, and genotype-age and genotype-environment interaction. Measurements of the magnitude of these effects are thus a necessary step toward assessing the implications of age dependence and environmental variability for the evolution of signals of quality. We conducted a longitudinal study of male guppies (Poecilia reticulata) from 22 full-sibling families. Each fish was assigned at maturity to one of three treatments in order to manipulate his allocation of resources to reproduction: a control in which the male was kept alone, a courtship-only treatment in which he could see and court a female across a clear partition, and a mating treatment in which he interacted freely with a female. We measured each male's size, ornamental color patterns, courtship, attractiveness to females, and mating success at three ages. Size was influenced by treatment and age-treatment interactions, indicating that courtship and mating may impose costs on growth. Tail size and color patterns were influenced by age but not by treatment, suggesting fixed age-dependent trajectories in these advertisement traits. By contrast, display rate and attempted sneak copulation rate differed among treatments but not among ages, suggesting greater plasticity of these behavioral traits. As a result of the different patterns of variation in ornamentation and behavior, male attractiveness and mating success responded to male age, treatment, and the interaction between age and treatment. Neither age nor treatment obscured the presence of genetic variation, and the genetic relationship between male ornamentation and attractiveness remained the same among treatments. Our findings suggest that neither age-dependent variation nor environmentally induced variation in reproductive effort is likely to undermine the reliability of male signaling.

Absence of female conspecifics induces homosexual behaviour in male guppies

Social environment can have dramatic effects on the expression of species-typical sexual behaviour. Using guppies, Poecilia reticulata, we asked how an all-male social environment affects male sexual behaviour. Males were assigned to either single-sex or mixed-sex groups. After 15 weeks, their sexual behaviour was assayed in the presence of three novel individuals of each sex. Males from single-sex groups performed higher rates of sexual displays and sneak copulation attempts towards stimulus males than did males from mixed-sex groups. Males from mixed-sex groups directed the majority of their sexual behaviour towards females using typical heterosexual behaviour. The social environment for each subject was then reversed for 2 weeks, after which subjects in both treatments showed a stronger tendency to display or sneak towards males. These findings reveal that homosexual behaviour is not readily extinguished when females become accessible and that it can be induced even after the ontogeny of heterosexual behaviour. While guppies may rarely occur in all-male groups in nature, these findings highlight the capacity for social environment to shape mating behaviour, which is particularly relevant for captive populations used in behavioural studies or conservation breeding programmes.

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.

Insemination efficiency of two alternative male mating tactics in the guppyPoecilia reticulata

In this study we compared the insemination efficiency of two alternative mating tactics (courtship and sneak mating) in the guppy Poecilia reticulata by quantifying the number of sperm delivered during a copulation. During a single copulation, guppies delivered between zero and 92% of the sperm available, as determined by mechanically stripping the male's sperm reserve at rest. The absolute number of sperm delivered after courtship was three times larger than that delivered through sneak mating; nonetheless, the variance was large with both tactics and the two distributions largely overlapped. The number of sperm available at rest increased with male size. With both tactics, the number of sperm delivered was positively correlated with the sperm available. Contrary to courtship copulations, in sneak copulations there was no correlation between the number of sperm delivered and male size. However, once the data were standardized for sperm reserve, small males delivered a larger proportion of their available sperm during sneak copulation. The rate of sexual acts (sigmoid and thrust rate) before copulation was not correlated with the number of sperm available. After the occurrence of a copulation in both the courtship and sneak copulation groups, the sexual activity of the male decreased in proportion to the amount of sperm he previously inseminated.

Intersexual and intrasexual selection, sneak copulation and male ornamentation in guppies (Poecilia reticulata)

To test the relative importance of female choice, sneak copulation and male dominance as determinants of male mating success in a feral guppy population, we conducted a paired-male mating experiment using the colour patterns of male progeny to score paternity. Sneak copulation and male-male aggression had no noticeable effect on male mating success. Mating success was strongly related to the frequency of female behavioural responses to both displaying and non-displaying males. Relative area of orange colouration and complexity of male colour patterns were positively related to mating success. This substantiates the observed behavioural preference for orange, and strengthens claims that female choice is integral to male mating success. Males in trials in which both females failed to produce offspring showed lower levels of black pigmentation, suggesting a threshold mating preference for this ornament despite it not being correlated with variation in male mating success or attractiveness measures. The implications of these findings for the evolution of multiple secondary sex traits in male guppies are discussed.

Predation, light intensity and courtship behaviour in Poecilia reticulata (Pisces: Poeciliidae)

The colour patterns of guppies, Poecilia reticulata, represent a balance between selection for crypsis (by predators) and selection for conspicuousness (by females). To a predator or mate, the conspicuousness of a colour pattern depends on environmental light conditions at the time of viewing. In this study light intensity and predation had significant effects on male courtship behaviour in guppies. Males courted less and used visually conspicuous behavioural elements less often in the presence of predators or under high light levels. Maximum risk due to predation naturally occurs at the highest light intensities, so either light intensity or the presence of a predator can be used as a cue for predator avoidance. Guppies minimized predator risk during courtship by shifting visually conspicuous displays to times of day when visual predation is minimal, and using the visually less conspicuous sneak copulation strategy when predation risk is greatest. Because ambient light conditions vary with time of day, the same colour patterns are seen under different visual conditions by predators and mates. Such context-dependent conspicuousness reduces the need for an evolutionary compromise between colour patterns that reduce the risk of visual predation and those that increase visibility to females.