Discriminating Males and Unpredictable Females: Males Bias Sperm Allocation in Favor of Virgin Females

When both sexes mate with multiple partners, theory predicts that males should adjust their investment in ejaculates in response to the risk and/or intensity of sperm competition. Here, we demonstrate that, in the harlequin beetle riding pseudoscorpion, Cordylochernes scorpioides, males use cues deposited on females by previous males to distinguish between virgin, once‐mated, and multiply‐mated females and adjust sperm allocation accordingly. Sperm number declined in direct proportion to the number of previous males, with virgin females receiving nearly three times more sperm than females exposed to three previous males. Given the lack of first‐male sperm precedence in C. scorpioides, this pattern is not consistent with current sperm competition models and appears best explained by a significant risk of wasting ejaculates on deceitful, mated females. In C. scorpioides, males transfer sperm indirectly to females via a stalked spermatophore deposited on the substrate. Mated females often feign sexual receptivity and cooperate throughout mating, only to reject the sperm packet produced by the male. While indirect sperm transfer facilitates a high level of female deceit and control, females of many species are able to influence the number and fate of sperm transferred during copulation and are likely to conceal their sexual unreceptivity to minimize male retaliation. If males cannot accurately assess female receptivity, increased risk of sperm rejection by mated females could outweigh the risk of sperm competition and favor greater sperm allocation to virgin females.     

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.     

Assessment of Rival Males through the Use of Multiple Sensory Cues in the Fruitfly Drosophila pseudoobscura

Environments vary stochastically, and animals need to behave in ways that best fit the conditions in which they find themselves. The social environment is particularly variable, and responding appropriately to it can be vital for an animal’s success. However, cues of social environment are not always reliable, and animals may need to balance accuracy against the risk of failing to respond if local conditions or interfering signals prevent them detecting a cue. Recent work has shown that many male Drosophila fruit flies respond to the presence of rival males, and that these responses increase their success in acquiring mates and fathering offspring. In Drosophila melanogaster males detect rivals using auditory, tactile and olfactory cues. However, males fail to respond to rivals if any two of these senses are not functioning: a single cue is not enough to produce a response. Here we examined cue use in the detection of rival males in a distantly related Drosophila species, D. pseudoobscura, where auditory, olfactory, tactile and visual cues were manipulated to assess the importance of each sensory cue singly and in combination. In contrast to D. melanogaster, male D. pseudoobscura require intact olfactory and tactile cues to respond to rivals. Visual cues were not important for detecting rival D. pseudoobscura, while results on auditory cues appeared puzzling. This difference in cue use in two species in the same genus suggests that cue use is evolutionarily labile, and may evolve in response to ecological or life history differences between species.     

Aversive Responses of Female Mice to the Odors of Parasitized Males: Neuromodulatory Mechanisms and Implications for Mate Choice

The detection and avoidance of parasitized conspecifics is proposed to have important consequences for the behavior of animals, especially as related to mate choice. A reduction in pain sensitivity (i.e. analgesia) is a major correlate of exposure to real or potential danger and threatening stimuli, facilitating the expression of various active (e.g. fleeing) and passive (e.g. immobilization) defense responses. The present study examined pain sensitivity (latency of a foot-lifting response to 50 ° C thermal surface) of female mice, Mus musculus, that were exposed to the urine and other odor secretions of male mice subclinically infected with the naturally occurring, enteric, sporozoan parasite, Eimeria vermiformis. A 30-min exposure to the odors of a parasitized male induced an analgesia in the female mice that was found to be mediated by the increased activity of endogenous opioid peptide systems. A brief 1-min exposure to the male odors induced a shorter duration and lower amplitude analgesia of a non-opioid (serotonergic) nature. Maximum analgesic responses were induced by the odors of pre-infective [5 days post-infection (PI)] and infective (day 10 PI) males, with significantly lower responses elicited by the odors of post-infective (day 17 PI) male mice. Exposure to the odors of unparasitized males had no significant effects on the pain sensitivity of female mice. These results indicate that female mice can distinguish between the odors of parasitized and non-parasitized male mice, and find the odors of parasitized males threatening and/or stressful. These odor-induced analgesic responses and their neurohormonal correlates may be part of an adaptive preparatory defense mechanism that facilitates the detection and avoidance of parasitized males by female mice and contributes to female mate choice.     

Cross-fostering Does Not Influence the Mate Preferences and Territorial Behaviour of Males in Lake Victoria Cichlids

The ability to recognise conspecifics in contexts of mate choice and territorial defence may have large effects on an individual's fitness. Understanding the development of assortative behaviour may shed light on how species assortative behaviour evolves and how it may influence reproductive isolation. This is the case not only for female mate preferences, but also for male mate preferences and male territorial behaviour. Here we test with a cross-fostering experiment whether early learning influences male mate preferences and male–male aggression biases in two closely related, sympatrically occurring cichlid species Pundamilia pundamilia and Pundamilia nyererei from Lake Victoria. Males that had been fostered, either by a conspecific female or by a heterospecific female, were tested for their aggression bias, as well as for their mate preferences, in two-way choice tests. Males cross-fostered with conspecific and heterospecific foster mothers selectively directed their aggression towards conspecific intruders. The cross-fostering treatment also did not affect male mate preferences. These results are in striking contrast with the finding that females of these species show a sexual preference for males of the foster species.     

Male-specific Iridescent Coloration in the Pipevine Swallowtail (Battus philenor) is Used in Mate Choice by Females but not Sexual Discrimination by Males

We investigated the potential roles in behavioral interactions of sexually dichromatic iridescent blue coloration found on the dorsal hindwing of male Pipevine Swallowtails (Battus philenor). Behavioral experiments in a large enclosure addressed whether male dorsal hindwing coloration mediated sexual recognition by males, female choice of mates, or both. Models presented to males in the enclosure produced responses that show that males discriminate females from other males using chemical but not visual cues. In contrast, ablation of male dorsal iridescence significantly reduced male mating success with virgin females in the enclosure. The results support the hypothesis that male-specific iridescent coloration in this species is a signal that is important for females in assessing either male species identity or quality in intersexual interactions.     

Visual Cues in Mate Recognition by Males of the Damselfly, Coenagrion puella (L.) (Odonata: Coenagrionidae)

Coenagrion puella males search actively for mates and are not aggressive to other males. To study the role of visual cues in male–female discrimination, four types of models were used: (1) bodies of intact insects, (2) models of painted males, (3) models of male–female chimerae, and (4) models of female body parts. Abdomen coloration pattern and presence of wings were the most important cues for sexual recognition by males. Step-by-step elimination of male coloration pattern leads to an increase in the tandem response rate. A female model painted as a male repelled males like the intact male model. The absence of either the head or the thorax slightly decreased the number of tandem responses, but models without both the head and the thorax were not recognized as a mate. Abdomen thickness larger than that of a normal female decreased the attractiveness of the model. Models of the gynochrome female were significantly more attractive than models of the androchrome one. Female models containing male parts were less attractive than models without any structure at this place. Using principal-components analysis, it is shown that models repelling males usually were those containing an intact male abdomen or a female abdomen painted with blue. The results indicate that C. puella males can distinguish males from females visually by morphological structures and coloration pattern.     

Female Mate Choice in a Paternal Brooding Blenny: The Process and Benefits of Mating with Males Tending Young Eggs

Female mate preference for males tending young offspring has been demonstrated in many fishes; however, not much is known about the choice process. Using the barred chin blenny Rhabdoblennius ellipes, a fish with male uniparental care, field experiments were conducted to investigate the female preference for males tending young eggs and then whether females choose the males with young eggs by discriminating young eggs from old eggs in the nests. Males tending young eggs (0‐ to 2‐d old) acquired new eggs nine times more frequently than those tending old eggs (3‐ to 5‐d old) regardless of other traits in males and nests. In the two egg‐switching field experiments (old to young and young to old), contrary to our expectation, male mating success was neither enhanced when given young eggs nor inhibited when given old eggs. These results suggested that females choose males with young eggs not by discriminating the developmental stage of eggs in the nests but by using other choice processes. By choosing males with young eggs, females may benefit from the dilution effects of egg predation and filial cannibalism risks and avoid male parental care failure.     

Male Competition over Access to Females in a Spider with Last-Male Sperm Precedence

Agonistic behaviour between male cellar spiders (Pholcus phalangioides) was investigated to test whether (1) size difference determines which male achieves access to the female, (2) males are able to monopolize access to the female until egg laying and whether (3) female resource value increases before egg laying because of last‐male sperm precedence. We further investigated whether (4) there is variation in time and energy spent on courtship and copulation depending on the degree of sperm competition, i.e. with or without rival present. In three experimental settings we introduced two males of either different or similar sizes, or a single male to a female. The mating units were constantly video‐observed until the females produced their first egg sac. Experience, ownership and female resource value in terms of body size was controlled. Our results show that larger males achieve almost exclusive access to females. Size symmetrical settings resulted in increased fighting activity and duration but dominance did not influence mating success. If copulations were disturbed by the rival male, copulations were terminated earlier in symmetrical settings compared with asymmetrical settings. In 94.8% of trials only one copulation took place, suggesting that the copulating male successfully monopolized access to the female. Males confronted with a rival copulated longer but courted significantly shorter than lone males. Although the last male to copulate sires 88% of the offspring in P. phalangioides, neither fighting nor courtship activity increased before the female laid a batch of eggs. This suggests that males have no indication of the timing of oviposition.     

Spermatophore and Sperm Allocation in Males of the Monandrous Butterfly Pararge aegeria: the Female’s Perspective

In insects, spermatophore production represents a non‐trivial cost to a male. Non‐virgin males have been shown to produce small spermatophores at subsequent matings. Particularly in monandrous species, it may be an issue to receive a sufficiently large spermatophore at the first and typically only mating. Females of the monandrous Speckled wood butterfly Pararge aegeria (L.) produce fewer offspring after mating with a non‐virgin male. After mating, females spend all their active time selecting oviposition sites and typically ignore other males. Here, we show that females did not discriminate between a virgin male and a recently mated male in our laboratory experiments. We demonstrate that the number of eupyrene sperm bundles relative to spermatophore mass differed with subsequent male matings. Males transferred a significantly smaller spermatophore after the first copulation, but the spermatophore mass did not decrease further with subsequent matings. However, the number of eupyrene sperm bundles decreased linearly. Therefore, there was proportionally more eupyrene sperm in the male’s second spermatophore compared with the first and the later spermatophores. Such a pattern has been shown in polyandrous species. Hence, it suggests that differences in sperm allocation strategy between polyandrous and monandrous butterflies may be quantitative rather than qualitative. There was also a tendency for females that had mated with a recently mated male to have higher propensity to remate than did females that had mated with a virgin male. We discuss the results relative to the mating system in P. aegeria, including female remating opportunities in the field and male mate‐locating behaviour.     

Sociality, Mate Choice, and Timing of Mating in American Bison (Bison bison): Effects of Large Males

We studied group size, composition, and mating activities in American bison (Bison bison) during rut on the Delta Junction Bison Range in interior Alaska, USA, in 1996 and 1997. Our purpose was to determine the effects of large males (≥5 yr old) on mating and associated activities. Groups with large males were larger than those containing smaller males. Most groups of bison were mixed‐sex (90%), but large males occurred in only one‐half of all groups. Moreover, females in groups with large males were more likely to copulate than those in groups with smaller males, indicating a female preference for large males. Nevertheless, our results are consistent with large males seeking out adult females for mating rather than vice versa. Mating peaked in mid‐August during both the study years and was highly synchronous. Scent marking was coincident with mating, an outcome consistent with a hypothesis of such behavior triggering ovulation. Scent marking by large male bison occurred in both male–male and male–female contexts, but was associated most often with sexual activities. No differences in group size occurred with changes in weather or among vegetation types occupied by bison. Group size of bison, however, was larger with increasing distance from the forest edge, which likely was a response to predation risk in this predator‐rich environment.     

Paternal Care Decreases Foraging Activity and Body Condition,but Does Not Impose Survival Costs to Caring Males in a Neotropical Arachnid

Exclusive paternal care is the rarest form of parental investment in nature and theory predicts that the maintenance of this behavior depends on the balance between costs and benefits to males. Our goal was to assess costs of paternal care in the harvestman Iporangaia pustulosa, for which the benefits of this behavior in terms of egg survival have already been demonstrated. We evaluated energetic costs and mortality risks associated to paternal egg-guarding in the field. We quantified foraging activity of males and estimated how their body condition is influenced by the duration of the caring period. Additionally, we conducted a one-year capture-mark-recapture study and estimated apparent survival probabilities of caring and non-caring males to assess potential survival costs of paternal care. Our results indicate that caring males forage less frequently than non-caring individuals (males and females) and that their body condition deteriorates over the course of the caring period. Thus, males willing to guard eggs may provide to females a fitness-enhancing gift of cost-free care of their offspring. Caring males, however, did not show lower survival probabilities when compared to both non-caring males and females. Reduction in mortality risks as a result of remaining stationary, combined with the benefits of improving egg survival, may have played an important and previously unsuspected role favoring the evolution of paternal care. Moreover, males exhibiting paternal care could also provide an honest signal of their quality as offspring defenders, and thus female preference for caring males could be responsible for maintaining the trait.     

Ocean Acidification Disrupts Prey Responses to Predator Cues but Not Net Prey Shell Growth in Concholepas concholepas (loco)

Background

Most research on Ocean Acidification (OA) has largely focused on the process of calcification and the physiological trade-offs employed by calcifying organisms to support the building of calcium carbonate structures. However, there is growing evidence that OA can also impact upon other key biological processes such as survival, growth and behaviour. On wave-swept rocky shores the ability of gastropods to self-right after dislodgement, and rapidly return to normal orientation, reduces the risk of predation.

Methodology/Principal Findings

The impacts of OA on this self-righting behaviour and other important parameters such as growth, survival, shell dissolution and shell deposition in Concholepas concholepas (loco) were investigated under contrasting pCO₂ levels. Although no impacts of OA on either growth or net shell calcification were found, the results did show that OA can significantly affect self-righting behaviour during the early ontogeny of this species with significantly faster righting times recorded for individuals of C. concholepas reared under increased average pCO₂ concentrations (± SE) (716±12 and 1036±14 µatm CO₂) compared to those reared at concentrations equivalent to those presently found in the surface ocean (388±8 µatm CO₂). When loco were also exposed to the predatory crab Acanthocyclus hassleri, righting times were again increased by exposure to elevated CO₂, although self-righting times were generally twice as fast as those observed in the absence of the crab.

Conclusions and Significance

These results suggest that self-righting in the early ontogeny of C. concholepas will be positively affected by pCO₂ levels expected by the end of the 21st century and beginning of the next one. However, as the rate of self-righting is an adaptive trait evolved to reduce lethal predatory attacks, our result also suggest that OA may disrupt prey responses to predators in nature.     

Mate Choice and Mating Pattern in a Stream Goby of the Genus Rhinogobius

The mate choice and mating pattern of a benthic goby Rhinogobius sp. CB (cross band type) were investigated in the Kamo River, Shikoku, Japan. During the breeding season, gravid females assumed a nuptial color and either males or females initiated a courtship display. Males preferentially courted a female of similar size to lead her to his nest, whereas females courted more frequently when they encountered a large male. Eggs in any one nest were always at the same developmental stage. Sampling data of nesting males and females indicated that, in more than half the nests, males gathered more than one female before spawning. In some nests with eggs, two or three females had spent ovaries, indicating that the eggs were laid by multiple females within a short span of time. However, a comparison between the total number of eggs which females would spawn in one nest and the number of eggs actually deposited suggested that eggs were contributed by one female in most nests. This low level of polygyny in spite of multiple female availability is attributed to a limited available spawning area of the nest.     

Female Mating History Influences Copulation Behavior but Not Sperm Release in the Orb-Weaving Spider <Emphasis Type="Italic">Tetragnatha versicolor</Emphasis> (Araneae,Tetragnathidae)

We examined the influence of female mating history on copulation behavior and sperm release in the haplogyne spider Tetragnatha versicolor. Despite significant behavioral differences during mating, males released equivalent amounts of sperm to virgin and non-virgin females. When mating with non-virgin females, males showed twice as many pedipalp insertions and half the copulation duration as compared to virgin females; however, males were as likely to mate with non-virgin as virgin females. Even with these overt behavioral differences, males released half of the sperm contained within their pedipalps during mating, regardless of female mating history. With respect to male mating order, first or second, we suggest the numbers of sperm released would lead to an expectation of unbiased paternity. In this species, sperm release is not directly proportional to total copulationduration.     

Males Respond to the Risk of Sperm Competition in the Sexually Cannibalistic Praying Mantis, Mantis religiosa

Although studies on sperm competition examined a wide range of taxa, little is known about the selection pressures on male traits in systems with simultaneous risk of sperm competition and sexual cannibalism. Here, we experimentally studied how the risk of sperm competition affects male copulatory behavior in the sexually cannibalistic praying mantis Mantis religiosa. We recorded the onset and duration of copulations following the introduction of virgin, adult praying mantises into mating arenas with three different sex ratio treatments: polyandrous, monogamous, and polygynous. We did not detect any female phenotypic trait predicting cannibalism. The chance of male survival was related to his condition, with males in better condition being cannibalized significantly less often. In contrast, we did not identify any male trait that would favor some males to obtain copulations. Our results on copulation duration support sperm competition theory in that the copulations in the male‐biased treatment, where the perceived risk of sperm competition was greatest, were significantly longer than those in single‐male treatments. Importantly, males in better condition copulated significantly longer regardless of sex ratio. Overall, our study suggests that males can adjust their copulation behavior in response to the risk of sperm competition even in a system with frequent sexual cannibalism.     

Testes Mass,but Not Sperm Length,Increases with Higher Levels of Polyandry in an Ancient Sex Model

There is strong evidence that polyandrous taxa have evolved relatively larger testes than monogamous relatives. Sperm size may either increase or decrease across species with the risk or intensity of sperm competition. Scorpions represent an ancient direct mode with spermatophore-mediated sperm transfer and are particularly well suited for studies in sperm competition. This work aims to analyze for the first time the variables affecting testes mass, ejaculate volume and sperm length, according with their levels of polyandry, in species belonging to the Neotropical family Bothriuridae. Variables influencing testes mass and sperm length were obtained by model selection analysis using corrected Akaike Information Criterion. Testes mass varied greatly among the seven species analyzed, ranging from 1.6±1.1 mg in Timogenes dorbignyi to 16.3±4.5 mg in Brachistosternus pentheri with an average of 8.4±5.0 mg in all the species. The relationship between testes mass and body mass was not significant. Body allocation in testes mass, taken as Gonadosomatic Index, was high in Bothriurus cordubensis and Brachistosternus ferrugineus and low in Timogenes species. The best-fitting model for testes mass considered only polyandry as predictor with a positive influence. Model selection showed that body mass influenced sperm length negatively but after correcting for body mass, none of the variables analyzed explained sperm length. Both body mass and testes mass influenced spermatophore volume positively. There was a strong phylogenetic effect on the model containing testes mass. As predicted by the sperm competition theory and according to what happens in other arthropods, testes mass increased in species with higher levels of sperm competition, and influenced positively spermatophore volume, but data was not conclusive for sperm length.     

Mate Choice by Non-Virgin Females Contributes to Reproductive Isolation between Populations of the Harlequin Beetle-Riding Pseudoscorpion

Determining whether reproductive isolation evolves through mate choice and/or gametic factors that prevent fertilization or through the post‐zygotic mechanisms of hybrid sterility or inviability is fundamental to understanding speciation. Investigation of the pre‐ and post‐zygotic components of reproductive isolation is facilitated in the pseudoscorpion, Cordylochernes scorpioides, by its indirect method of sperm transfer and viviparous embryonic development. Previous research on this species, in which mate discrimination was assessed in virgin females, suggested that female choice played only a minor role in reproductive isolation between populations from French Guiana and Panamá. Here, in a study of three allopatric populations of C. scorpioides from Panamá, we assessed mating‐stage isolation in both virgin and once‐mated females, and found that female discrimination depends critically on mating status. Virgin females were almost invariably receptive, showing no tendency to discriminate against males from allopatric populations. By contrast, non‐virgin females were significantly more likely to reject foreign males than males from their own population. Male sexual motivation could not account for differences in either female sexual receptivity or male success in sperm transfer. Allopatric and sympatric males did not differ in number of spermatophores deposited as either a female’s first or second mate. Nonetheless, allopatric males achieved significantly lower sperm transfer success not only with choosy, non‐virgin females but also with virgin females. Given the lack of behavioral discrimination by virgin females, female receptivity was not the only factor influencing differences in sperm transfer success. Multivariate analysis of spermatophore morphology suggests that the higher failure rate of matings between allopatric males and virgin females resulted from population differences in sperm packet architecture. Overall, our findings indicate that assessment of discrimination against allopatric males that is limited to virgin females may seriously underestimate the contribution of female mate choice to reproductive isolation between populations.     

Choosing Hunting Sites: Web Site Preferences of the Orb Weaver Spider,Neoscona crucifera,Relative to Light Cues

Field experiments carried out on the nocturnal orb weaver spider, Neoscona crucifera (Aranea: Araneidae), found in deciduous hardwood forests suggest that lighted areas where prey densities are elevated provide cues used by the spiders to rank optimal foraging sites. Specifically, experiments were conducted to test whether spiders exhibited preferences for lighted areas where prey densities are high, maximizing their energy intake per unit of foraging time, and minimizing energy expended on web building. Incandescent light bulbs of 4–60 W were used to influence prey densities, and results indicate that when given a choice of brighter versus darker foraging areas, spiders seek lighted areas where prey densities are high. In addition, results support the hypothesis that the size and time of web construction are drastically reduced in brighter situations.