Mutual Mate Assessment in Wolf Spiders: Differences in the Cues Used by Males and Females

When males engage in conspicuous courtship displays, it seems obvious that females would use characteristics of that display in mating decisions. However, males must also have a way to identify and evaluate females prior to engaging in what might be a costly mating ritual. Although it was known that female wolf spiders of the species Pardosa milvina (Araneae; Lycosidae) attract males using volatile chemical cues, the nature of the cues used by males and females in mate selection had not been investigated. Specifically we determined whether males could detect the mating status of the female and if chemotactile cues from the female played a role in that process. In addition, we quantified conspicuous aspects of the male courtship (leg raises and body shakes) to determine if courtship intensity was related to female choice. Although repeated mating occurred in our studies, males were more likely to court and mate with virgin females. Males used substrate‐borne cues deposited by females to discriminate between mated and virgin females. Females used the conspicuous behaviors of males during courtship, body shakes and leg raises, in mate selection. Thus males and females use different kinds of information and different sensory modalities to assess the suitability of a potential mate.     

Sensory Aspects of Trail-Following Behaviors in the Asian Longhorned Beetle, <Emphasis Type="Italic">Anoplophora glabripennis</Emphasis>

Anoplophora glabripennis has a complex suite of mate-finding behaviors, the functions of which are not entirely understood. These behaviors are elicited by a number of factors, including visual and chemical cues. Chemical cues include a male-produced volatile semiochemical acting as a long-range sex pheromone, a female-produced cuticular hydrocarbon blend serving as a sex-identification contact pheromone, and a recently identified female-produced trail sex pheromone that is followed by mate-seeking males. However, the sensory appendages and sensilla on these appendages used to detect the trail sex pheromone are unknown. We evaluated the ability of virgin male A. glabripennis to follow a sex pheromone trail after removal of the terminal four antennal segments and/or the maxillary and labial palps using a two-choice behavioral bioassay. We also tested the ability of males to follow the trail sex pheromone using volatile pheromone cues only, without physical contact with the pheromone. Results indicate that the palps are primarily responsible for sensing the pheromone, with males lacking palps unable to respond behaviorally to the trail sex pheromone. Under the conditions of this study, males could not follow the sex pheromone trail without direct contact, suggesting that olfaction may not be involved in detection of this pheromone. However, we did not determine to what degree the trail pheromone chemicals can volatilize under our experimental conditions. This work is important in elucidating the behaviors and sensory structures involved in mate-finding by this species on host trees, and these studies may help determine whether the trail sex pheromone has applications for monitoring and management.     

Silk‐ and volatile‐based male mate choice in the genital plug‐producing spider

Female mating history can have a strong effect on male fertilization success. Although males often prefer to mate with virgin females, they often also engage with mated females. As the intensity of sperm competition can differ among mated females, males are expected to evolve means to identify their status. In spiders, males often use female silk to gather information about female quality. Males of many spider species deposit mating plugs into female genitalia to hinder further copulations. We tested whether males of the foliage‐dwelling, plug‐producing spider Philodromus cespitum, which is an important natural enemy of pests, discriminate between females of different mating status and whether they can determine the extent of genital plugging in mated females solely on the basis of cues gained from deposited female silk. We presented males with draglines of females that varied in either mating status (virgin vs. mated), the extent of plugging (small vs. big plug), or the age of the plug (fresh vs. old plug) and examined their mate preferences. Additionally, we tested whether males were attracted to volatile cues produced by female bodies. Our experiments revealed that males preferred draglines of virgin females to those of mated females, and mated females with small plugs to those with large plugs. They were also attracted to female volatile cues. This study suggests that males are able to extract fine‐scale information on mating status from female draglines.     

Tracking of Female Conspecific Odor Trails by Male Broad-headed Skinks (Eumeces laticeps)

The ability of the broad-headed skink (Eumeces laticeps) to follow conspecific odor trails on paper substrates was investigated in y-maze experiments. Adult males enter the trail-containing arm at much greater than chance frequency when the odor source is female. The data support the hypothesis that males can follow odor trails of females. The often-repeated direct contact with the trail made by tongue-flicking as the lizard passed through the maze provided evidence that males could follow the scent. There was no evidence that males followed male odors or that females followed trails laid by either sex. It is suggested that the major selective force leading to evolution by males of the ability to trail females was an increase in reproductive success accruing to males able to locate females and guard them during a temporally limited period of sexual receptivity.     

Species-Specificity of Chemical Signals: Silk Source Affects Discrimination in a Wolf Spider (Araneae: Lycosidae)

Female spiders deposit chemical cues that elicit male courtship behavior with silk. These cues are often assumed to be species-specific although male spiders may court in response to chemical cues of closely-related species. We used behavioral assays to test the extent of species discrimination of female chemical cues by male Schizocosa ocreata, a wolf spider (Lycosidae). Discrimination, expressed as relative courtship intensity of males, varied significantly with phylogenetic distance. Males did not discriminate between female cues of conspecifics and a sibling species, S. rovneri. Courtship response was intermediate for another species within the ocreata clade and not different from control for spiders outside the clade. These findings support the sibling species status of S. ocreata and S. rovneri, and also suggest the composition of female chemical signals is conserved across closely related wolf spider species.     

同种雄性竞争对手的存在对星豹蛛雄蛛求偶和交配行为的影响

越来越多的研究发现,雄性产生精子(精液)也需付出代价。雄性除了依据配偶质量和竞争对手的竞争强度适应性调整生殖投入外,雄性在求偶和交配行为上也相应产生适应性反应,求偶和交配行为具有可塑性。目前雄性求偶和交配行为可塑性研究主要集中于雌性多次交配的类群中,在雌性单次交配的类群中研究甚少。以雌蛛一生只交配一次而雄蛛可多次交配的星豹蛛为研究对象,比较:(1)前一雄性拖丝上信息物质对后续雄蛛求偶和交配行为的影响,(2)雌雄不同性比对雄蛛求偶和交配行为的影响。研究结果表明,星豹蛛前一雄蛛拖丝上的信息物质对后续雄蛛求偶潜伏期、求偶持续时间和交配持续时间都没有显著影响,但前一雄蛛拖丝上的信息物质对后续雄蛛求偶强度有显著抑制作用。同时,性比对星豹蛛雄蛛求偶和交配行为都没有显著影响。可见,星豹蛛雄蛛对同种雄性拖丝上的化学信息可产生求偶行为的适应性调整,而对性比不产生适应性反应。     

Disruption of the chemical communication of the European agrobiont ground‐dwelling spider Pardosa agrestis by pesticides

Lycosid spiders are among the most abundant and diverse insectivores occurring in all agroecosystems. Certain pest management practices, such as the application of pesticides, can disrupt their role in insect pest control. Therefore, understanding the effects of pesticides, including sublethal effects, is essential for the assessment of chemical effects on beneficial arthropods. We investigated the sexual chemical communication of the beneficial agrobiont spider Pardosa agrestis and its disruption by two widely used pesticides, the glyphosate‐based herbicide Roundup and the pyrethroïd‐based insecticide Nurelle D. A two‐choice olfactometer and Y‐maze were used to study the effectiveness of female airborne and dragline pheromone cues and the disruptive effect of the pesticides. Males of P. agrestis did not locate females via airborne cues, but were very receptive to female dragline silk and male dragline silk. When both female dragline silk and male dragline silk were provided at the same time, the males preferred female silk. Pesticide treatments significantly affected the male ability to follow female cues deposited on dragline silk. The 3‐h residues of both Roundup and Nurelle D significantly disrupted the male ability to follow female cues deposited on dragline silk. Treatment by 48‐h residues significantly disrupted the male ability only in the case of Nurelle D. Our results demonstrate that pesticides reduce the ability of male spiders to search for a mate due to the disruption of the male's ability to detect the silk cues of the female.     

Changes in male sexual responses from silk cues of females at different reproductive states in the wolf spider Schizocosa malitiosa

Male wolf spiders are capable of recognising sexual signals associated with female silk threads. In the wolf spider Schizocosa malitiosa variations in female receptivity have been studied, but changes in female silk attractiveness remain unknown. We analysed the sexual responses of adult males (leg shaking, papal drumming and searching) exposed to silk cues from subadult, virgin and mated females of different ages, and females that were or were not carrying an egg-sac. Penultimate and recently moulted adult females elicited low levels of male sexual behaviour, while those of virgin females (21–40 days old) were the most attractive. Silk threads slowly became less attractive after mating. Cues from females carrying an egg-sac as well as females in the inter egg-sac period were fairly attractive. The low attractiveness of recently moulted females disagrees with their high sexual receptivity. In contrast, females continued to elicit strong male responses during a 10-day period after mating, despite the fact that they immediately become sexually reluctant, suggesting strong selection for male searching ability. Low attractiveness during the egg-carrying period could reflect the fact that females do not require any further sperm. Concordances and discordances between attractiveness and sexual receptivity suggest that they respond to different physiological mechanisms.     

Mate Finding Via a Trail Sex Pheromone by <Emphasis Type="Italic">Aphytis melinus</Emphasis> DeBach (Hymenoptera: Aphelinidae) Males

Finding mates is frequently problematic for parasitoid wasps. In some parasitoid species, males rely on volatile, airborne sex pheromones for locating mates, while in others they rely on contact, trail sex pheromones. This study sought to shed light on the mate finding mechanism of males of Aphytis melinus. Specifically, the goal was to determine whether A. melinus males use airborne or contact pheromones, or both, for locating mates. The study showed that A. melinus males rely on a contact, trail sex pheromone for locating mates: A. melinus males responded to substrate-borne cues left by virgin females, while they did not respond to airborne cues from virgin females. Specifically, males more frequently encountered virgin females when the females walked across an arena to a fixed encounter point compared to when they were manually placed at the encounter point, and spent greater than expected time on surfaces previously visited by virgin females compared to control surfaces not visited by females. In contrast, males did not respond to airborne cues from virgin females in an airflow olfactometer nor to traps baited with virgin females in the field, and spent similar lengths of time on surfaces visited by newly-mated or 24-h mated females versus control surfaces not visited by females. The main effect of the trail sex pheromone on the behavior of A. melinus males was to direct their search and, so, increase the likelihood of encountering mates. This effect apparently is not preceded by longer-range attraction of males via an airborne female sex pheromone. Overall, the results of this study support a hypothesis in which A. melinus males searching on substrates on which females may be present rely exclusively on a trail sex pheromone to locate mates.     

Sexual Differences in the Behavior of the Harvestman Leiobunum vittatum (Opiliones, Sclerosomatidae) Towards Conspecific Cues

Preliminary observations of the harvestman Leiobunum vittatum found that individuals rub their bodies against the substrate, presenting the possibility of chemical marking. To determine whether or not L. vittatum individuals can detect substrate-borne chemical cues, we compared responses of L. vittatum males and females to substrate-borne male and female cues. We found that individuals of L. vittatum do respond to conspecific cues and that their responses are sex-specific. In response to substrate-borne conspecific cues, male L. vittatum spent more time, engaged in more scraping with their sensory legs I, and engaged in pedipalpal tapping more often in the presence versus absence of conspecific cues (male and female equally). Furthermore, in the presence of conspecific cues, males engaged in two behaviors never observed in females—(a) “fast approach” and (b) “jerking”, the latter of which was never observed in the presence of cricket cues. In contrast to males, females did not spend more time on conspecific cues, but did spend more time tapping their pedipalps in the presence of male vs female cues, suggesting an ability to distinguish between them. A final experiment explored the possibility that females could discriminate among males of varying histories of agonistic interactions based upon their chemical cues. We found no support for this hypothesis. Our results demonstrate that L. vitattum do respond to conspecific cues, and introduce the possibility that intraspecific communication may be mediated in part by chemical cues.     

The predatory mite <Emphasis Type="Italic">Neoseiulus womersleyi</Emphasis> (Acari: Phytoseiidae) follows extracts of trails left by the two-spotted spider mite <Emphasis Type="Italic">Tetranychus urticae</Emphasis> (Acari: Tetranychidae)

As it walks, the two-spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae) spins a trail of silk threads, that is followed by the predatory mite, Neoseiulus womersleyi Schicha (Acari: Phytoseiidae). Starved adult female N. womersleyi followed T. urticae trails laid down by five T. urticae females but did not follow a trail of one T. urticae female, suggesting that the amount of spun threads and their chemical components should correlate positively with the number of T. urticae individuals. To examine whether chemical components of T. urticae trails are responsible for the predatory mite’s trail following, we collected separate T. urticae threads from the exuviae and eggs, and then washed the threads with methanol to separate chemical components from physical attributes of the threads. Female N. womersleyi did not follow T. urticae trails that had been washed with methanol but contained physical residues, but they did follow the direction to which the methanol extracts of the T. urticae trails was applied. These results suggest that the predatory mite follows chemical, not physical, attributes of T. urticae trails.     

Male competition reverses female preference for male chemical cues

Females must choose among potential mates with different phenotypes in a variety of social contexts. Many male traits are inherent and unchanging, but others are labile to social context. Competition, for example, can cause physiological changes that reflect recent wins and losses that fluctuate throughout time. We may expect females to respond differently to males depending on the outcome of their most recent fight. In Bolitotherus cornutus (forked fungus beetles), males compete for access to females, but copulation requires female cooperation. In this study, we use behavioral trials to determine whether females use chemical cues to differentiate between males and whether the outcome of recent male competition alters female preference. We measured female association time with chemical cues of two size‐matched males both before and after male–male competition. Females in our study preferred to associate with future losers before males interacted, but changed their preference for realized winners following male competitive interactions. Our study provides the first evidence of change in female preference based solely on the outcome of male–male competition.     

Female mating status affects male mating tactic expression in the wolf spider Rabidosa punctulata

Males and females have conflicting interests on the frequency and outcomes of mating interactions. Males maximize their fitness by mating with as many females as possible, whereas choosy females often reduce receptivity following copulation. Alternative male mating tactics can be adaptive in their expression to a variety of mating contexts, including interactions with a relatively unreceptive mated female. Male Rabidosa punctulata wolf spiders can adopt distinctive mating tactics when interacting with a female, a complex courtship display, and/or a more coercive direct mount tactic that often involves grappling with females for copulation. In this study, we set up female mating treatments with initial trials and then paired mated and unmated females with males to observe both female remating frequencies and the male mating tactics used during the interactions. Males adopted different mating tactics depending on the mating status of the female they were paired with. Males were more likely to adopt a direct mount tactic with already-mated females and courtship with unmated females. Already-mated females were considerably less receptive to males during experimental trials, although they did remate 34% of the time, the majority of which were with males using a direct mount tactic. Whereas males adjusting to these contextual cues were able to gain more copulations, the observation of multiple mating in female R. punctulata introduces the potential for sperm competition. We discuss this sexual conflict in terms of the fitness consequences of these mating outcomes for both males and females.     

Preference for Chemical Cues Associated with Recent Prey in the Wolf Spider Hogna helluo (Araneae: Lycosidae)

In the wolf spider, Hogna helluo , we tested the response to insect and spider prey chemical cues and whether they show a preference for cues associated with prey consumed most recently. Thirty adult female H. helluo were maintained on a diet of either females of a smaller co-occurring wolf spider ( Pardosa milvina ) or domestic crickets ( Acheta domesticus ). A single P. milvina or cricket nymph was maintained on filter paper for 24 h, after which the papers from both prey sources were simultaneously presented to individual H. helluo from each diet treatment group. H. helluo locomotor behavior on each treatment and initial substrate preference was recorded (n = 15/treatment). H. helluo fed crickets showed significantly longer residence time and decreased mobility on filter paper previously occupied by a cricket; spiders fed P. milvina showed longer residence times and decreased mobility on filter paper previously occupied by P. milvina . H. helluo fed P. milvina exhibited an initial preference for substrates previously occupied by P. milvina but H. helluo fed crickets did not show a corresponding initial preference for crickets. Results suggest that H. helluo can detect distant cues associated with P. milvina but not crickets before contacting the substrate and that H. helluo respond to chemical cues from prey and show a preference for those cues associated with their most recent prey.     

Sex differences in dogfish behaviour: alternative activity patterns and habitat choice

Guppies are highly sexually dimorphic and females have been shown to mate preferentially with males with various visible traits. Guppies, however, have been shown to respond behaviourally to odour cues from conspecifics. Using a specially designed olfactory choice tank, we tested whether females (1) could detect other guppies on the basis of their olfactory cues alone, (2) preferred to associate with males or with females and (3) could distinguish between different males. Female guppies were found to associate preferentially with other guppies when given a choice between water containing cues from another fish and water containing no cues. When females were presented with olfactory cues from a male or a female, they preferred the female initially but most then reversed their decision and swam to the male. Females associated preferentially with certain males based upon olfactory cues alone. Males, however, preferred on the basis of olfactory cues were the least preferred for visual cues.     

Female preferences based on olfactory cues in the guppy (Poecilia reticulata)

Guppies are highly sexually dimorphic and females have been shown to mate preferentially with males with various visible traits. Guppies, however, have been shown to respond behaviourally to odour cues from conspecifics. Using a specially designed olfactory choice tank, we tested whether females (1) could detect other guppies on the basis of their olfactory cues alone, (2) preferred to associate with males or with females and (3) could distinguish between different males. Female guppies were found to associate preferentially with other guppies when given a choice between water containing cues from another fish and water containing no cues. When females were presented with olfactory cues from a male or a female, they preferred the female initially but most then reversed their decision and swam to the male. Females associated preferentially with certain males based upon olfactory cues alone. Males, however, preferred on the basis of olfactory cues were the least preferred for visual cues.     

Sex‐Specific Response of Pardosa milvina (Araneae: Lycosidae) to Experience with a Chemotactile Predation Cue

Predators frequently leave behind chemical information (i.e., semiochemicals such as pheromones or kairomones) that can be detected by their prey and used to avoid areas where predators are likely present. Prey that have interacted indirectly with predators via chemical information thus may gain insight into their risk of being consumed that naïve individuals lack. Pardosa milvina (Araneae: Lycosidae) is a chemosensitive wolf spider that shows adaptive responses to chemotactile cues deposited by the larger wolf spider Tigrosa helluo. We raised offspring from P. milvina to examine the effect of experience with a predation cue on activity, foraging, and antipredator behavior. Spiders differed in activity and foraging behavior across ontogeny and between sexes, but there was no effect of experience with a predation cue. However, a sex‐specific effect of experience was found in antipredator behavior. Male spiders, but not females, used experience with a predator cue to increase their survival in the presence of a live predator. Specifically, naïve males were attacked sooner than experienced males, indicating that prior exposure to predator cues can modify Pardosa antipredator behavior. Intersexual differences in how spiders respond to experience with a predation cue likely reflect the risk of predation faced by males and females in nature.     

The effects of sex on chemosensory communication in a terrestrial salamander (Plethodon shermani)

Although much evidence reveals sexually dimorphic processing of chemosensory cues by the brain, potential sex differences at more peripheral levels of chemoreception are understudied. In plethodontid salamanders, the volume of the vomeronasal organ (VNO) is almost twice as large in males as compared to females, both in absolute and relative size. To determine whether the structural sexual dimorphism in VNO volume is associated with sex differences in other peripheral aspects of chemosensation, we measured sex differences in chemo-investigation and in responsiveness of the VNO to chemosensory cues. Males and females differed in traits influencing stimulus access to VNO chemosensory neurons. Males chemo-investigated (“nose tapped”) neutral substrates and substrates moistened with female body rinses more than did females. Compared to females, males had larger narial structures (cirri) associated with the transfer of substrate-borne chemical cues to the lumen of the VNO. These sex differences in chemo-investigation and narial morphology likely represent important mechanisms for regulating sex differences in chemical communication. In contrast, males and females did not differ in responsiveness of VNO chemosensory neurons to male mental gland extract or female skin secretions. This important result indicates that although males have a substantially larger VNO compared to females, the male VNO was not more responsive to every chemosensory cue that is detected by the VNO. Future studies will determine whether the male VNO is specialized to detect a subset of chemosensory cues, such as female body rinses or female scent marks.     

Absence of social facilitation of courtship in the wolf spider, Schizocosa ocreata (Hentz) (Araneae: Lycosidae)

Males of many animal species are reproductively limited by the difficulty and time costs of finding mates. Males of such species should be selected to take advantage of any cues that might reveal the location of prospective mates. Cues to female location are not restricted to those produced by females, but might also include the highly apparent courtship displays of males that have already found a female. By “eavesdropping” on these courting rivals, initiating sexual displays when courting rivals are detected (i.e., social facilitation of displays); males might effectively exploit the mate-searching efforts of their rivals. We tested the possibility that male Schizocosa ocreata wolf spiders exhibit social facilitation of courtship behaviors using a combination of live behavioral trials and video playback with single stimulus presentations. When exposed to visual cues from another male, male S. ocreata can discern the presence of another individual whether that individual is courting or not. However, we found no evidence of social facilitation of courtship or chemoexploratory behaviors in response to seismic or visual cues presented in isolation or combined. While complex, multimodal, male courtship signals are important in mate choice by female S. ocreata, males do not appear to use these cues to socially facilitate their own courtship.     

Seismic Signaling is Crucial for Female Mate Choice in a Multimodal Signaling Wolf Spider

Complex courtship signals can be dissected into distinct components that can either function independently or via interactions with one another. Male Rabidosa rabida wolf spiders use courtship displays that couple a seismic signal with the waving of an ornamented foreleg. While previous studies suggest that female R. rabida exhibit mate choice and that both the seismic and visual modalities are important in mating interactions, it remains unclear how variation in each component influences female mating decisions. To investigate this, we ran two separate experiments in which we manipulated (1) male diets, to induce variation in the seismic courtship signal, and (2) male foreleg color, to artificially induce variation in visual foreleg ornamentation. To determine the influence of variation in each component independently, females were paired with males in environments that allowed the detection of only the manipulated signal component (e.g. seismic signal only and visual signal only). Variability in the seismic signal alone influenced female mate choice, but variability in visual ornamentation alone did not. In a third experiment, we manipulated foreleg color and allowed it to interact with the seismic signal to determine whether inter‐signal interactions influence female mating decisions. When females were able to detect both signal components, variation in visual ornamentation did influence mate choice – females preferred ornamented males. Together, these results suggest that the seismic signal of male R. rabida is integral for female mate choice and that the components of the courtship display interact to influence female mating decisions.