The lexicon of love: what cues cause size-assortative courtship by male garter snakes?

Cues that females use to select potential mates have attracted substantial research effort, but the criteria for male mate choice remain very poorly known. Red-sided garter snakes ( Thamnophis sirtalis parietalis) court and mate in large aggregations around overwintering dens in southern Manitoba, Canada. Both courtship and mating are size-assortative: small male snakes court small as well as large females, whereas larger males court only large females. This system provides a unique opportunity to assess the cues that males use in selecting mates, and in particular the mechanisms that generate a size-related shift in mate preference. Experiments in which we manipulated body sizes and scents showed that both vision and scent (sex pheromones) were important. Large males directed intense courtship only when the stimulus provided both visual and chemical (skin lipid) evidence of large body size. Small males were much less discriminating in both respects. Thus, size-assortative mating in this system is generated not by larger males excluding their smaller rivals from the largest females (as has been reported in other reptile species), but by a size-related shift in the visual and pheromonal cues that elicit courtship. Males of some species may thus show complex patterns of mate choice, with the cues that stimulate courtship differing even among males within a single population based on traits such as age or body size.     

Facultative pheromonal mimicry in snakes: “she-males” attract courtship only when it is useful

Males of many animal species mimic females, and thereby deceive rival males. Facultative shifts in posture, color, or movement allow a male using visually-based mimicry to adopt and terminate mimicry rapidly. Pheromonal mimicry is rare in vertebrates perhaps because it is difficult to redeploy pheromones rapidly enough to adjust male tactics to local conditions. In Manitoba garter snakes (Thamnophis sirtalis parietalis), female mimicry benefits males immediately after they have emerged from hibernation. While the snakes are cold and slow, courtship warms them and protects them against predatory crows. This benefit disappears as soon as the snakes are warm. We show that (unlike females) she-male garter snakes attract courting males only when they are cold. Low temperatures may suppress volatility of “less attractive” components of the pheromones (saturated methyl ketones) that she-males use to attract courtship, allowing male snakes to function as transvestites only when this tactic is beneficial.     

Experience with chemotactile cues indicating female feeding history impacts male courtship investment in the wolf spider <Emphasis Type="BoldItalic">Schizocosa ocreata</Emphasis>

Male fitness is often determined by the ability of the male to gain access to multiple mates, although in species that exhibit sexual cannibalism, males might increase their likelihood of being cannibalized with each encounter. This risk should create selection for males who are able to perceive potential risks associated with mating encounters. We studied male Schizocosa ocreata wolf spiders to determine whether they use female chemotactile cues (silk, excreta) as indicators of potential risks and how these cues affected subsequent male courtship behaviors. Female treatments included satiated females vs. starved females, as well as a treatment where females had recently cannibalized a male S. ocreata. We performed experiments to assess (1) if males use female chemotactile cues to determine potential risks associated with differing female feeding treatments and alter courtship investment, and 2) how male experience with female chemotactile cues affected courtship investment in subsequent female encounters. At first encounter, males do not vary courtship investment (number of bouts, duration, and vigor) with different female feeding treatments. However, male behaviors during subsequent encounters with female chemotactile cues varied in complex ways, depending on female feeding treatment and male first encounter experience. These data suggest that male experience impacts perception of female chemical cues and offers the male opportunity to avoid sexual cannibalism in high-risk situations.     

Sexual conflict in the snake den

Red-sided garter snakes (Thamnophis sirtalis parietalis) court and mate in spring, soon after they emerge from large communal overwintering dens in south-central Manitoba. Because of a massive bias in the operational sex ratio, every female attracts intense courtship from dozens to hundreds of males. We suggest that this courtship constitutes significant ”harassment,” because it delays the females’ dispersal from the den and hence increases their vulnerability to predation. Small females may face the greatest costs, because they are less able to escape from amorous males (who court all females, even juvenile animals). Our measurements show that males are stronger and faster than females. Experimental trials confirm that the locomotor ability of females (especially small females) is greatly reduced by the weight of a courting male. Arena trials show that intense courtship stimulates females to attempt to escape. Remarkably, some females that are too small to produce offspring may nonetheless copulate. This precocious sexual receptivity may benefit juvenile females because copulation renders them unattractive to males, and thus allows them to escape more easily from the den. Female ”tactics” to escape male harassment may explain other puzzling aspects of garter snake biology including size-assortative mating, temporal patterns in dispersal from the den, avoidance of communal dens by young-of-the-year snakes, and female mimicry. Hence, sexual conflict may have influenced important features of the mating system and behavioral ecology of these animals. Received: 8 May 2000 / Revised: 28 July 2000 / Accepted: 30 July 2000     

Mating in the red-sided garter snake,Thamnophis sirtalis parietalis: differential effects on male and female sexual behavior

Summary Female red-sided garter snakes, Thamnophis sirtalis parietalis, become unattractive to most males after mating in the field and in the laboratory. Male red-sided garter snakes vary in their latencies to court attractive females following copulation, with courtship resuming in minutes to hours. Unsuccessful males in mating balls disperse from mating pairs, but are not residually inhibited from courting attractive females. These patterns of behavior indicate that males have evolved mechanisms to maximize opportunities for copulation with several females, while females mate only once per season.     

All at sea: aquatic life modifies mate-recognition modalities in sea snakes (Emydocephalus annulatus, Hydrophiidae)

Alternative sensory modalities (e.g. vision, chemoreception) differ in the spatial scale, permanence and reliability of cues they provide to mate-searching males. Males of terrestrial snake species use chemoreception to locate females over large distances, but phylogenetic shifts to aquatic life render such cues unavailable. Do male sea snakes use alternative modalities for identifying potential sexual partners and if so, are the novel systems as effective for mate-finding as the ancestral ones? Observations and experiments show that free-ranging male turtle-headed sea snakes (Emydocephalus annulatus) in shallow-water reef habitats in New Caledonia use visual cues (including size, movement and color pattern) to assess whether snake-shaped objects are potential sexual partners. Skin lipids (pheromones) are important only after the male comes into physical contact with the stimulus. Visual cues provide unreliable information about potential mates, and function over short distances only (generally, <1 m). In consequence, mate-searching male snakes frequently failed to find nearby females, rarely managed to maintain contact with females they did find, and wasted time and energy investigating inappropriate stimuli (e.g. fishes, sea cucumbers, divers). The loss of effective pheromonal mate-location systems means that mate recognition by aquatic snakes functions over smaller distances than in their terrestrial relatives. Phylogenetic transitions among habitat types thus may directly modify central features of the mating system.     

Sexual selection and species recognition in the pygmy swordtail, Xiphophorus pygmaeus: conflicting preferences

Sexual selection and species recognition play important roles in mate choice; however, sexual selection preferences may overlap with traits found in heterospecifics, producing a conflict between sexual selection and species recognition. We examined female preferences in Xiphophorus pygmaeus for male traits that could provide both types of information to determine how females use multiple cues when preferences for these cues would conflict. We also examined X. pygmaeus behavior in the field to determine if females have the opportunity to choose mates. As no male-male competition was observed in the field, and females occasionally chased males from feeding areas, females apparently have the opportunity to exercise mate choice in their natural habitat. In the laboratory, female X. pygmaeus used body size as a sexual selection cue, preferring large heterospecifics (X. cortezi) to small conspecifics. Females also preferred barless X. cortezi over barred X. cortezi when males were size matched. Because X. pygmaeus males do not have bars, this preference suggests that X. pygmaeus females use vertical bars in species recognition, and that large body size and vertical bars are conflicting cues. However, X. pygmaeus females did not have a preference for males of either species when sexual selection and species recognition cues were presented concurrently. This result was surprising, because preferences for species recognition cues are often assumed to be stronger than sexual selection cues. We suggest that females may be using additional species-specific cues in mate choice to prevent hybridization.     

Testosterone treatment suppresses paternal care in superb fairy-wrens, Malurus cyaneus, despite their concurrent investment in courtship

Courtship displays and paternal care in male birds are generally thought to be mutually exclusive, because testosterone, necessary for stimulation of sexual behaviours, suppresses paternal behaviours. Superb fairy-wrens, Malurus cyaneus, are unusual in that males concurrently engage in courtship and paternal care. Fairy-wrens live in stable socially monogamous pairs with 0-4 subordinate male helpers. Both helper and dominant males provide care whenever it is required but continue courtship throughout the period of care as most fertilisations are extra-group and females are multi-brooded. To examine the role of testosterone in this trade-off, we compared testosterone levels in males of different social status, while they had dependent nestlings, and determined the effect of testosterone treatment on provisioning rates of pairs. Testosterone levels were lower in subordinate helpers, although these do not provide more paternal care than dominant males. Conversely, testosterone levels were similar in dominant males with or without helpers, although as the number of helpers increases males invest substantially less in nestling care and more in extra-group courtship. Although testosterone levels are high, irrespective of paternal duties, experimental testosterone treatment of males resulted in a large (65%) reduction in nestling feeding rates. Surprisingly, there was no indication that females compensated for this reduction in provisioning, suggesting that females might assume a constant male contribution to offspring care. We conclude that during nestling provisioning, male fairy-wrens maintain testosterone at an individual level that does not interfere with parental duties, while allowing high investment in extra-group courtship.     

Predation risk affects courtship and attractiveness of competing threespine stickleback males

The effect of predation risk and male-male competition on male courtship behaviour and attractiveness to females was studied in the threespine stickleback (Gasterosteus aculeatus) by presenting dummy or live females to solitary and competing males under different predation risks. In the presence of a predator, males decreased courtship activity. Different courtship components were, however, adjusted to different extents and in opposing directions to predation risk, probably because the single components may have varied in riskiness. The presence of a competing male decreased overall courtship activity, but increased the frequency of zigzags, suggesting zigzagging to be a competitive strategy against other males. In the presence of a predator male courtship activity was not affected by a competitor. Female mate choice correlated with the males' previous frequency of zigzags towards a dummy female. However, when a live female paid attention to a male, the male decreased zigzagging and instead increased leading and fanning behaviours, probably trying to attract the female to the nest to mate. Predation risk affected the attractiveness of males as females reduced their attention to a male when he faced a predator and reduced his courtship activity. As females instead increased their attention to a competing male that had increased his courtship activity, due to decreased competition, males clearly are balancing mating opportunities against predator avoidance. When males vary in their susceptibility to predators, predation risk may thus affect mating success of competing males. Received: 31 January 1997 / Accepted after revision: 15 April 1997     

Evidence for a female sex pheromone mediating male trailing behavior in the red-sided garter snake, Thamnophis sirtalis parietalis

Summary. Male garter snakes locate females during the breeding season utilizing conspecific trailing behavior. It has been hypothesized that the female-derived chemical cue responsible for mediating male reproductive trailing behavior is the sexual attractiveness pheromone, a previously characterized contact pheromone responsible for releasing male courtship behavior. To examine this hypothesis, we tested the response of male red-sided garter snakes, Thamnophis sirtalis parietalis, to pheromone trails produced by males, females and ‘she-males’. She-males are a small subset of males in the natural population that are morphologically and behaviorally similar to other males except that they produce and express the sexual attractiveness pheromone during the breeding season. When tested on a Y-maze, males were found to detect and follow the skin lipid trails of females and she-males, but displayed no behavioral responses to male trails. In addition, males were unable to discriminate between she-male and female trails when given a choice. These results are consistent with the hypothesis that the sexual attractiveness pheromone is the chemical cue primarily utilized by males to mediate reproductive trailing behavior.     

The assessment of female reproductive state during courtship and scramble competition in the fiddler crab, Uca paradussumieri

Male fiddler crabs, Uca paradussumieri, mate underground during a 4- to 7-day period each full and new moon. As soon as the tide recedes, males enter the burrows of females that will ovulate the following day ('pre-ovigerous' females). Males copulate with and guard these females until they ovulate. When interrupted by an intruding male, the first male to reach the female is usually able to defend her and successfully mate with her. In fiddler crabs, females mate multiply and there is last male sperm precedence. Before each semi-lunar mating period, male U. paradussumieri were more likely to court females with whom they would later mate than other nearby females with whom they did not mate. This suggests that males collect information on female reproductive state prior to the females becoming ovigerous. In this species, aggression was common between males that courted the same female. When previously courted females were approached by other males, the initial courter attempted to forcefully disrupt the courtship. This behavior may allow males the exclusive use of information on female reproductive condition. It also suggests a type of scramble competition between males over females. Furthermore, it indicates that males are able to locate receptive females prior to their becoming ovigerous. The shorter guarding period observed in this species, as compared with other fiddler crabs, is caused by females rejecting longer guarding periods. Male ability to assess female reproductive status may therefore be advantageous because it increases male mating success within a scramble type of competitive polygyny.     

Female mate choice determines reproductive isolation between sympatric butterflies

Animal courtship rituals are important for species recognition, and a variety of cues might be utilized to recognize conspecific mates. In this paper, we investigate different species-recognition mechanisms between two sympatric butterfly sister species: the wood white (Leptidea sinapis) and Real’s wood white (Leptidea reali). We show that males of both species frequently court heterospecific females both under laboratory and field conditions. The long-lasting elaborate courtships impose energetic costs, since the second courtship of males that were introduced to two subsequent conspecific females lasted on average only one fourth as long as the first courtship. In this paper, we demonstrate that premating reproductive isolation is dependent on female unwillingness to accept heterospecific mates. We studied female and male courtship behavior, chemical signaling, and the morphology of the sexually dimorphic antennae, one of the few male traits visible for females during courtship. We found no differences in ultraviolet (UV) reflectance and only small differences in longer wavelengths and brightness, significant between-species differences, but strongly overlapping distributions of male L. sinapis and L. reali antennal morphology and chemical signals and minor differences in courtship behavior. The lack of clear-cut between-species differences further explains the lack of male species recognition, and the overall similarity might have caused the long-lasting elaborate courtships, if females need prolonged male courtships to distinguish between con- and heterospecific suitors.     

Why do males tolerate sneakers? Tests with the European bitterling, Rhodeus sericeus

In most species, males attack other males that attempt to gain fertilizations through sneak copulations. Here we report on a system where dominant males show a low level of aggression against sneakers at the initial stages of territory establishment. Females of the European bitterling, Rhodeus sericeus, lay their eggs in living mussels and males fertilize the eggs by releasing sperm over the mussels both before and after egg laying. When we allowed males to court females to a mussel containing no eggs at different male densities - one, two, four, or six males - the dominant male showed a low level of aggression against other males that released sperm. The dominant male became aggressive toward the other males only after eggs had been laid. This unusual pattern could be due to either some benefit of accepting sneakers or a high cost of aggression. We found support for both possibilities. The presence of several males decreased the time until a female spawned, whereas increased aggression by the dominant male against other males during a second female presentation, when the male was more territorial, interrupted courtship and increased the time until spawning. Females appeared to be attracted by both the presence of several males around a mussel and increased courtship under male competition. The bitterling mating system possibly differs from that of other species due to lack of investment in nest building and parental care, and high costs of defending the spawning site against sneakers.     

Variation in male courtship costs in butterflies

A cost of mating is common to both sexes but has predominantly been examined in females. In species where males provide resources to females at copulation, male mating costs are expected to be high as nutrient provisioning enhancing female fecundity is assumed to carry costs. In addition, males frequently court females prior to mating, which is known to carry survival costs to both sexes. However, the magnitude and basis of variation in males’ mating costs remains largely unknown. Here, I examine the effect of nutrient provisioning and courtship on male longevity across full-sib families in the paternally investing green-veined white butterfly, Pieris napi. Copulating males suffered a survival cost as did courting males prevented from copulating, indicating the courtship component of mating is costly. Male P. napi release aphrodisiacs during courtship to promote mating, indicating that these compounds may also be costly to produce. Contrary to expectation, nutrient provisioning was not associated with reduced survival relative to males only allowed to court females, although it is possible that this could be masked by the potentially elevated courtship rates of courting males relative to mating males. Families differed in magnitude of reduced male survivorship, indicating a likely genetic basis to variation in costs of courtship and copulation. Male weight was unrelated to longevity and mating success, whereas longevity strongly influenced male mating success, indicating lifespan is an important male fitness trait in this species.     

Influence of host plants on sexual communication in the herbivorous bug Lygocoris pabulinus

Summary. Host plant volatiles may be involved in the sexual communication of insects in several ways. In the pheromone-producing sex, these volatiles may affect pheromone production or release and, in the receptive sex, plant volatiles may have a synergistic effect on the attraction to sex pheromone. We conducted three types of experiments to determine if and how plant volatiles are involved in the sexual communication of Lygocoris pabulinus (L.) (Heteroptera: Miridae), the females of which attract males. In a one-choice cylinder bioassay, females were offered to males on two different plants, belonging to different plant families, i.e. potato leaves and goosefoot leaves, to determine if specific plant volatiles were involved in the attraction of males towards females. Females on potato leaves were as attractive as females on goosefoot leaves, but significantly more attractive than females without plant material. The latter result suggests an interaction between females and potato leaves. However, in two-choice flying and walking bioassays, using delta traps in a wind tunnel and a vertical Y-track olfactometer, males were attracted to females irrespective of the presence of potato leaves. This difference in result is probably due to the fact that in the latter assays females were confined with pollen as an alternative food source, while females in the one-choice assay had access to water only, so that they may have suffered from malnutrition. Males in the one-choice assay were also attracted to potato leaves from which females had been removed, indicating that attractive components from females are deposited and adsorbed to the substrate. Plants are probably only indirectly involved in sexual communication, their surface merely functioning as a substrate from which pheromone is released. Males may subsequently be attracted to such plants or substrates. Clean plant material was not attractive to L. pabulinus males, hence plant volatiles alone do not seem to be used by these males as possible mate location cues.     

Does mating experience of male house crickets affect their behavior to subsequent females and female choice?

Male mating experience was shown to play an important role in settling conflicts between males; however, little is known about whether and how prior access to females influences male behavior during intersexual interactions and female choice itself. Here, I experimentally test this relationship in the house cricket (Acheta domesticus) by combining one-on-one interaction between the male and female with direct comparison of males by the female, but precluding aggression between males. I found that solitary males were more active during subsequent courtship displays than paired males, suggesting the detrimental effect of mating on courtship performance. At the same time, females spent significantly more time close to solitary males or playbacks of male's natural courtship songs, and responded positively to the condition of males, ignoring body size of males. In contrast, females responded similarly to computer-modified playbacks of courtship songs of solitary and paired males with standardized rate of phrases and amplitudes; however, when females were additionally allowed to contact with anesthetized males they spent more time close to bigger males, irrespective of the acoustic parameters of courtship songs. These results show that although females were able to differentiate between many behavioral and morphological characteristics of males, including voluntary and intrinsic ones, they preferred traits conditional upon the costliness of male's displays. In addition, mating experience appeared to be a crucial factor in the choice of a particular costly mating strategy by males.     

Chemosensory cues allow courting male garter snakes to assess body length and body condition of potential mates

When choosing between two potential mates, a male may benefit by picking a larger (longer and/or more heavy-bodied) female because she is likely to produce more or larger offspring. Males of many species use visual cues to evaluate the sizes of their mates, but in some situations (at night or in a crowded mating swarm), vision may be useless. Potentially, males may be able to use chemical cues that convey information about female body size. We manipulated cues available to free-ranging male garter snakes (Thamnophis sirtalis parietalis) in large courting aggregations near communal dens in Manitoba, Canada. Males not only directed disproportionate courtship to longer and heavier-bodied females, but also courted most vigorously in response to lipids extracted from the skins of such females. Our data show that with a flick of his tongue, a male garter snake can identify not only a female's body length, but also her body condition.     

Predation risk reduces male-male sexual competition in the Trinidadian guppy (Poecilia reticulata)

Because agonistic behaviour can increase an individual's risk of predation, natural selection should favour individuals that modify their behaviour in the face of predation hazard in ways that maximise fitness. We investigated experimentally the effects of an increase in the apparent risk of predation on male-male competition within mixed-sex shoals of the Trinidadian guppy (Poecilia reticulata). We show that males engaged in significantly fewer aggressive interactions with conspecific males in the presence of a fish predator. However, they continued to court and attempt copulations with females at the same rate irrespective of the level of predation risk. In comparison, under predation hazard, female guppies were less responsive sexually and avoided fewer male copulation attempts. Such predator-mediated changes in male-male agonistic interactions and female sexual responsiveness towards males have important implications for the mode and intensity of sexual selection within populations.     

Male preference for colourful females affected by male size in a marine fish

It is becoming increasingly clear that mate preferences are not static, but can vary as a function of ecological conditions and the state of the choosing individual. This applies not only to females, the sex that has usually been the subject in research on mate preferences, but also to males. Under certain conditions, males should be selective in their choice of breeding partner. In the two-spotted goby, Gobiusculus flavescens, a small marine fish, breeding females develop conspicuous yellow-orange bellies, which they actively display to males during courtship. We have recently shown that males prefer more colourful females as mates. In this study, we test if the size of a male affects his preference for colourful females. Using three-compartment mate-choice aquaria, we recorded the interest shown by a male in two females differing in coloration but similar in size. Large and small males were equally eager to court females, but only large males showed a greater interest in the more colourful females. We suggest that small males are unselective because they usually obtain few mating opportunities, as a result of being unsuccessful in mate attraction or male contest competition. This study provides the first demonstration that the size of a male affects his preference for female colour.     

Damselfly females prefer hot males: higher courtship success in males in sunspots

Males of some territorial calopterygid damselflies show an elaborate courtship display that involves high-frequency wing-beats directed toward an incoming female. Although it has been suggested that female mate preference is based on some characteristics of male’s courtship display, it is unclear whether the courtship display varies between males or is influenced by environmental conditions. We combined two recent technologies, thermographic imaging and high-speed digital videography, to show that the wing-beat frequency during courtship (i.e., courtship intensity) in a damselfly, Mnais costalis, is correlated with thorax temperature. Our data indicated that (1) male thorax temperature was associated with solar exposure in his territory, (2) environmentally derived thermal gain enhanced courtship intensity, (3) hotter males were more likely to copulate than others, and (4) female thorax temperature during oviposition within a territory was associated with solar exposure. Males with territories that have longer exposure to sun spots are expected to attain higher thorax temperatures for longer and so are able to successfully court more females. We suggest that females benefit from mating with hot males because they will be on a warmer territory while ovipositing. Hot males might also have greater mate guarding ability, and/or eggs may develop faster in warmer territories.