Copulatory behavior in a pholcid spider: males use specialized genitalic movements for sperm removal and copulatory courtship

Sexual selection may operate on pre-copulatory, copulatory, and post-copulatory traits. An example of a copulatory target of sexual selection is the genitalic movements a male performs during copulation. These movements may function either to prevent sperm competition or to influence a female’s fertilization decision. Here we investigated how copulation duration, pedipalp movements, and abdominal movements that males of the pholcid spider Holocnemus pluchei produce during copulation influence sperm removal and/or patterns of successful sperm transfer. We compared mating events with virgin and mated females for differences in copulatory and post-copulatory behavior. We expected longer copulation duration, longer pedipalp movement duration, and more complex and frequent pedipalp and abdominal movements when males mated with mated females compared to virgin females. Except for abdominal movements, our results corroborated these predictions. Furthermore, when we investigated mating events with mated females, we observed sperm mass ejection from the female gonopore and physical removal of sperm by males’ procursi. Females with interrupted second mating events showed a significant reduction of stored sperm masses compared to females with completed mating events. We suggest that males use alternating pedipalp movements to remove most of the rival sperm stored by mated females prior to sperm transfer. Copulation duration and pedipalp movements can be further used to transfer sperm and/or as a form of genitalic copulatory courtship.     

Territorial meadow pipit males (<Emphasis Type="Italic">Anthus pratensis</Emphasis>; Passeriformes) become more aggressive in female presence

Although mate guarding as prevention of extra-pair copulation is common among birds, evidence for aggressive behaviour involving physical contact related to mate guarding in passerines is scarce and cases of the presence of one partner directly influencing the aggressiveness of the other are lacking. We investigated the intra-specific territorial behaviour of male meadow pipits (Anthus pratensis; Passeriformes: Motacillidae) at the beginning of the breeding season by placing a pipit model accompanied by an intra-specific song playback in the territory of socially paired males and compared the responses of males whose mates were physically present during trials with those whose females were out of sight. The level of aggression of males was significantly higher in the presence of the female; half of the males in this group physically attacked the model (the most intense and risky aggressive behaviour). Physical attacks did not occur among males whose female was absent during the trial; response to the playback by most of these males was only weak. This pattern may be related to the prevention of extra-pair copulation; if the risks involved in the conflict are outweighed by potential loss of paternity, such aggressive mate guarding may pay off. The apparently overlooked effect on the territorial behaviour of a partner’s passive physical presence during conflict should be further evaluated because it may be important for the design and interpretation of results of behavioural experiments.     

Sexual behavior,cannibalism, and mating plugs as sticky traps in the orb weaver spider <Emphasis Type="BoldItalic">Leucauge argyra</Emphasis> (Tetragnathidae)

Unpublished field observations in Leucauge argyra, a tropical orb weaver spider, suggest the occurrence of conspicuous mating plugs that could reduce or prevent remating attempts. Otherwise, the sexual behavior of this species remains unknown. The aims of this study were to describe the courtship behavior and copulation in L. argyra and investigate mating plug formation in this species. Fourteen virgin females and 12 plugged females were exposed to up to three males and checked for mating plug formation. Of the 12 virgins that copulated, nine produced plugs (five immediately after copulation), and the five plugged females that copulated produced another mating plug immediately after copulation. We did not detect the transfer of any male substance during copulation but observed a whitish liquid emerging from female genital ducts. Plug formation was positively associated with male twanging during courtship. One virgin and four plugged females cannibalized males. In seven trials with virgins and in three trials with plugged females, the male’s palp adhered to a substance that emerged from female genital ducts and spread on her genital plate. The male had to struggle energetically to free his glued palp; two of these males were cannibalized while trying to release their palps. Females seem to determine copulation duration by altering the timing of mating plug formation and through sexual cannibalism. This is the first case reported of a mating plug as a sticky trap for males.     

Male wing color properties predict the size of nuptial gifts given during mating in the Pipevine Swallowtail butterfly (Battus philenor)

In many animals, males bear bright ornamental color patches that may signal both the direct and indirect benefits that a female might accrue from mating with him. Here we test whether male coloration in the Pipevine Swallowtail butterfly, Battus philenor, predicts two potential direct benefits for females: brief copulation duration and the quantity of materials the male passes to the female during mating. In this species, males have a bright iridescent blue field on the dorsal hindwing surface, while females have little or no dorsal iridescence. Females preferentially mate with males who display a bright and highly chromatic blue field on their dorsal hindwing. In this study, we show that the chroma of the blue field on the male dorsal hindwing and male body size (forewing length) significantly predict the mass of material or spermatophore that a male forms within the female’s copulatory sac during mating. We also found that spermatophore mass correlated negatively with copulation duration, but that color variables did not significantly predict this potential direct benefit. These results suggest that females may enhance the material benefits they receive during mating by mating with males based on the coloration of their dorsal hindwing.     

The reproductive choices of eavesdropping female black-capped chickadees,<Emphasis Type="Italic"> Poecile atricapillus</Emphasis>

In animals where males engage in signalling interactions, females might evaluate male–male contests to inform their reproductive choices. We used interactive playback to engage territorial male black-capped chickadees (Poecile atricapillus) of known dominance status in countersinging contests with an aggressive or submissive opponent. Previous analysis of these data showed that high-ranking males who received aggressive playback were more likely to be cuckolded. Here we describe the particular reproductive decisions of females whose partners received aggressive versus submissive playback. The proportion of extra-pair young per brood was higher for females paired to high-ranking males that received aggressive playback compared to submissive playback, and similar to levels in broods of females paired to low-ranking males. We found no strong predictors of whether high-ranking subjects lost paternity following aggressive playback. Females usually preferred extra-pair sires with high dominance status. When females had extra-pair fertilizations with low-ranking males, females chose males who had received submissive playback. We conclude that females mated to aggressive-playback, high-ranking males pursued mixed mating strategies similar to those of females mated to low-ranking males. Our results support the idea that male performance in song contests may influence multiple aspects of female reproductive choices.     

Females prefer carotenoid colored males as mates in the pentamorphic livebearing fish,<Emphasis Type="Italic"> Poecilia parae</Emphasis>

The first results of female preference and chosen male mating success in a new model organism, the pentamorphic livebearing fish, Poecilia parae, are presented. Poecilia parae is a relative of the guppy, P. reticulata, and is assumed to have similar reproductive behavior. We tested the hypothesis that P. parae females, like female guppies, prefer caretenoid colored males as mates. Here we show that the time a female spent with males was significantly greater for carotenoid coloration in red and yellow melanzona, but time with these two morphs did not differ. The preferred red and yellow males mated significantly more often with their choosing females than did the non-preferred blue and parae males. The few blue melanzona and parae males that mated did so without performing courtship displays. Some females mated with all phenotypes including immaculata males during open group trials. Female P. parae clearly preferred males with carotenoid coloration, thereby corroborating the hypothesis. Alternative male mating tactics by blue melanzona, parae, and immaculata morphs and promiscuous mating by females also resembled features of reproductive behaviors exhibited by guppies.     

Female feeding regime and polyandry in the nuptially feeding nursery web spider, Pisaura mirabilis

We examined the influence of female feeding regime on polyandry in the nuptially feeding nursery web spider (Pisaura mirabilis). In this species, the nuptial gift, a dead prey item wrapped in the male’s silk, is physically separate from the ejaculate. We manipulated female feeding regime (starved or fed) and the presence or absence of a gift with three successive males to test direct-benefits hypotheses (nuptial gift or sperm supply) for the expression of polyandry. The presence of a gift was necessary for copulation, as no male without a gift successfully copulated. Female mating behavior most strongly supports polyandry due to the accumulation of gifted food items (“nuptial gift” direct-benefits hypothesis). Starved females that were presented with a gift accepted significantly more gifts and inseminations than fed females. Most starved females (74%) copulated two or more times, as opposed to only 3% of the fed females. Nearly all of the females that accepted a gift subsequently copulated. The nuptial gift item seems to function as male mating effort and females appear to receive multiple matings as part of a feeding strategy.     

Dynamics of sperm transfer in the ant Leptothorax gredleri

Mating tactics differ remarkably between and within species of social Hymenoptera (bees, wasps, ants) concerning, e.g., mating frequencies, sperm competition, and the degree of male sperm limitation. Although social Hymenoptera might, therefore, potentially be ideal model systems for testing sexual selection theory, the dynamics of mating and sperm transfer have rarely been studied in species other than social bees, and basic information needed to draw conclusions about possible sperm competition and female choice is lacking. We investigated sperm transfer in the ant Leptothorax gredleri, a species in which female sexuals attract males by “female calling.” The analysis of 38 female sexuals fixed immediately or up to 7 days after copulation with a single male each revealed that the sperm is transferred into the female bursa copulatrix embedded in a gelatinous mass, presumably a spermatophore. Sperm cells rapidly start to migrate from the tip of the spermatophore towards the spermatheca, but transfer is drastically slowed down by an extreme constriction of the spermathecal duct, through which sperm cells have to pass virtually one by one. This results in the spermatheca being filled only between one and several hours after mating. During this time, the posterior part of the spermatophore seals the junction between bursa copulatrix and spermathecal duct and prevents sperm loss. The prolonged duration of sperm transfer might allow female sexuals to chose between ejaculates and explain previously reported patterns of single paternity of the offspring of multiply mated queens. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Eunuchs as better fighters?

Male–male competition for females can significantly affect a male’s reproductive success and hence his fitness. Game theory predicts that an individual should avoid fighting when its future reproductive potential is high, but should fight forcefully when its future reproductive potential is insignificant. When mates are scarce, extreme competition and fatal fighting is expected. We recently showed that Nephilengys malabarensis eunuchs, i.e. sterile spider males that lost their genitals during copulation, become more aggressive during male–male contests. Here, we add crucial comparative data by exploring eunuch fighting behaviour in Nephilengys livida from Madagascar, specifically by testing the ‘better fighter hypotheses’ in a laboratory setting. Similar to N. malabarensis, N. livida copulations resulted in total male castration with the severed palp plugging the female genitals in 70.83% cases, which mostly (63.63%) prevented subsequent copulations. Unexpectedly, however, N. livida eunuchs exhibited lower aggressiveness than virgin males. We interpret these results in the light of different mating biology between the so far studied species known for the eunuch phenomenon, which might reflect differing plug effectiveness due to variation in genital anatomy in N. livida, N. malabarensis and Herennia multipuncta. However, detected differences in aggressive behaviour of N. livida versus N. malabarensis eunuchs might also be explained by the species’ ecology, with lower population densities resulting in a relaxed male–male competition making excessive aggression and mate guarding redundant. This study thus questions the generality of overt aggressiveness in mated males with no reproductive value, and highlights the importance of understanding the natural history of species in the question.     

The effect of vegetation density on male mate guarding and extra-territorial forays in the yellow-breasted chat (<Emphasis Type="Italic">Icteria virens</Emphasis>)

Extra-pair paternity is widely documented in birds, but the behaviors that lead to extra-pair copulations (EPCs) have been less well studied, particularly in territorial songbirds. We studied the behaviors associated with extra-territorial forays (ETFs) and male mate guarding in a socially monogamous, but genetically promiscuous, neotropical migrant passerine, the yellow-breasted chat (Icteria virens). Focal observations and radiotelemetry revealed that both males and females engaged in ETFs. 65% of the females in our study engaged in at least one foray onto a neighboring territory. 50% of males also were observed engaging in ETFs, but males were much more conspicuous during these intrusions compared to females. Females preferred to remain close to the ground in areas where vegetation was the densest. Female behavior was difficult to observe during ETFs but females sometimes interacted with neighboring extra-pair males. Males attempted to guard their mates by remaining close to them and following them during extra-territorial intrusions. We observed instances in which a male attacked his mate and appeared to herd her back to his territory. However a males ability to maintain close proximity to his mate was significantly and negatively correlated with vegetation density. Our results suggest that the behaviors which lead to extra-pair encounters are influenced by the behavior of all participants and are modified by the characteristics of the habitat.     

Carotenoid-based plumage coloration predicts resistance to a novel parasite in the house finch

The Hamilton-Zuk hypothesis proposes that the bright colours displayed by many species of birds serve as signals of individual resistance to parasites. Despite the popularity of this hypothesis, only one previous study has tested whether plumage coloration predicts how individuals respond to a disease challenge. We inoculated 24 male house finches (Carpodacus mexicanus) of variable plumage hue with a novel bacterial pathogen, Mycoplasma gallicepticum (MG). We found no relationship between plumage hue and time to first symptoms following inoculation, but we found a significant negative relationship between plumage hue and clearance of disease: males with redder plumage cleared MG infection significantly better than did males with yellower plumage. The hue of carotenoid-based plumage coloration has been shown to be a primary criterion in female mate choice in the house finch. These observations suggest that one benefit to females for choosing redder males is obtaining mates with better resistance to parasites.     

Odor familiarity and female preferences for males in a threatened primate,the pygmy loris<Emphasis Type="Italic"> Nycticebus pygmaeus</Emphasis>: applications for genetic management of small populations

Here we use sexual selection theory to develop a logistically simple, yet effective, method for the manipulation of female reproductive behavior for conservation goals. Mate choice leading to nonrandom mating patterns can exacerbate the loss of genetic diversity in small populations. On theoretical grounds, females should choose high-quality mates. A prediction stemming from chemical communication theory is that competitive males will be better able to saturate an area with scent marks. If this is true, females should mate preferentially with males whose odors they encounter most frequently. We tested this hypothesis with the pygmy loris, Nycticebus pygmaeus, a threatened and poorly studied nocturnal prosimian. For several weeks females were exposed repeatedly to the urine from a particular male, and were then allowed to choose between a male whose odors were familiar and one whose odors were novel. Females showed an unusually strong preference for the familiar-odor male, as indicated by several behavioral measures of mate preference. Conservation managers can use this method as a tool to obtain reproductive pairings that will maximize genetic compatibility and diversity. For example, unsuccessful males may be given the opportunity to reproduce. In captive populations, studbook managers often select pairs in order to optimize outbreeding, but these selected pairings may not coincide with the preferences of the individual animals involved. Although several authors have made theoretical arguments for manipulating mate choice for conservation, this is a novel test of a proximate mechanism that can be manipulated, cultivating applications rather than mere implications.     

Alternative mating behaviors of the queen polymorphic ant <Emphasis Type="Italic">Temnothorax longispinosus</Emphasis>

Mating behaviors of ants fall into two categories: female calling, in which a female alate releases pheromones that attract males, and male swarming, in which large male aggregations attract females. Female calling is common in species with queens that return to their natal nest to found colonies dependently after mating, while male swarming is common in species with queens that disperse to found independently. In some species that display both founding strategies, a queen-size polymorphism has evolved in which dependent-founding queens are smaller than independent-founding queens. Dependent founding is likely difficult if gynes (virgin queens) are mating in distant swarms. Therefore, a queen may adopt one or the other mating strategy based on its size and founding behavior. We investigated mating behaviors in the queen-polymorphic ant, Temnothorax longispinosus. Observations in laboratory mating arenas indicated that small gynes exhibited significantly lower flight activity than large gynes. Both forms mated in male swarms, and neither form exhibited female calling. The reduced flight activity of the small morph may facilitate returning to the natal nest after mating, provided the mating swarm is located nearby. Therefore, alternative colony-founding behaviors may be possible without the evolution of female-calling behavior; however, the reduced flight activity of small morphs may require that mating swarms are not distant from the natal nest.     

Mate guarding and territorial aggression vary with breeding synchrony in golden whistlers (<Emphasis Type="Italic">Pachycephala pectoralis</Emphasis>)

Male paternity assurance behaviour during the female fertile period has been widely documented amongst birds. In contrast, how sex-specific behavioural strategies vary with local breeding synchrony levels remains largely unknown. This is important because, in many species, intra-population patterns of extra-pair fertilisation rates, and hence cuckoldry risk, are known to vary with the number of simultaneously fertile females. Each sex may therefore differ in how they behave towards male conspecifics during different degrees of breeding synchrony. Here I provide evidence of such sex-specific differences in the golden whistler (Pachycephala pectoralis), a species in which within-pair paternity assurance is negatively associated with breeding synchrony. Via simulated territorial intrusions using decoy males, I show that males, but not females, increase levels of aggression to male intruders during periods of low synchrony, possibly because cuckoldry risk is greatest during this period. In addition, males appear to invest more effort into mate guarding after, but not before, territorial intrusions during this period. These inter-sexual differences may reflect conflicts in interest between the sexes, with females consistently showing interest in males during the fertile period regardless of synchrony levels and males investing more resources into expelling intruders when the risk of paternity loss is greatest. This study thus provides evidence that males may be able to detect variation in breeding synchrony and cuckoldry risk and adjust their paternity assurance behaviour accordingly.     

Where to find a mate? Resource-based sexual communication of webbing clothes moth

Mate location in moths typically entails long-range attraction of males to female-produced pheromone. Here, we show that male and female webbing clothes moths, Tineola bisselliella, seek larval habitats (dry carrion, animal lairs, etc) to encounter mates. With males seeking, and arriving at, larval habitat earlier at night than females, male-produced pheromonal and sonic signals enhance the habitat's attractiveness to females. This resource-based mating strategy of T. bisselliella differs from that known for most other moths. It may have evolved in response to larval habitats that are patchy and temporary, but that disseminate attractive semiochemicals so abundantly that T. bisselliella encounter them more readily than their own pheromones.     

Monogamy in a new species of wild guinea pigs (Galea sp.)

A new species of wild guinea pigs from Bolivia was recently discovered: Galea sp. So far no data are available concerning its social and mating systems. We therefore investigated behavioural compatibility, sexual dimorphism, paternity in a male-competing situation, testicular and epididymal size, and sperm morphology and motility. The results showed a complete intrasexual and moderate intersexual behavioural incompatibility between unfamiliar animals, a reversed sexual dimorphism with females larger than males, and litters always fathered by single males. Furthermore, both the reproductive organ weights and the percentage of motile sperm and sperm with intact acrosomes were significantly lower compared with the promiscuous congeneric Galea musteloides. In summary, these data strongly suggest a monogamous social and mating system for the recently discovered Galea sp.     

Mating behaviour in a slave-making ant, Rossomyrmex minuchae (Hymenoptera, Formicidae)

The mating behaviour of the ant Rossomyrmex minuchae, a rare, protected slave-making species in Spain, seems to be significantly affected by its particular life history and patchy habitat. The mating behaviour of the entire genus Rossomyrmex is virtually unknown. We present here the results of a 3-year study of mating behaviour in R. minuchae.Behavioural observations and limited nest excavations revealed that R. minuchae does not produce sexuals every year, the number of sexuals is low, and the sex ratio tends to be female biased. Females typically exhibit two distinct activity periods. The first, the mating period, takes place in early afternoon: the ants call near the natal nest, mate and then return to their nest. The second, the dispersal period takes place in late afternoon: the mated females exit their nest and fly in search of a new, non-parasitized Proformica longiseta host nest. Males are highly active during the mating period, but will remain inactive in the dispersal period even if experimentally presented with virgin females. It appears that females are monogamous, while males are polygamous. When males are late arriving at the female calling site, the females will frequently congregate presumably calling in chorus.The low reproductive efficiency exhibited by R. minuchae, coupled with the postulated low genetic variation in the population, as sisters may mate with the same male, could result in a low survival rate and risk of eventual extinction. The observed decrease in nest density we observed during the 2004 season may be indicative of such a process.     

Silk wrapping of nuptial gifts as visual signal for female attraction in a crepuscular spider

An extensive diversity of nuptial gifts is known in invertebrates, but prey wrapped in silk is a unique type of gift present in few insects and spiders. Females from spider species prefer males offering a gift accepting more and longer matings than when males offered no gift. Silk wrapping of the gift is not essential to obtain a mating, but appears to increase the chance of a mating evidencing a particularly intriguing function of this trait. Consequently, as other secondary sexual traits, silk wrapping may be an important trait under sexual selection, if it is used by females as a signal providing information on male quality. We aimed to understand whether the white color of wrapped gifts is used as visual signal during courtship in the spider Paratrechalea ornata. We studied if a patch of white paint on the males’ chelicerae is attractive to females by exposing females to males: with their chelicerae painted white; without paint; and with the sternum painted white (paint control). Females contacted males with white chelicerae more often and those males obtained higher mating success than other males. Thereafter, we explored whether silk wrapping is a condition-dependent trait and drives female visual attraction. We exposed good and poor condition males, carrying a prey, to the female silk. Males in poor condition added less silk to the prey than males in good condition, indicating that gift wrapping is an indicator of male quality and may be used by females to acquire information of the potential mate.     

Male antenna morphology and its effect on scramble competition in false garden mantids

Well-developed antennae are crucial for many insects, but especially for scramble competitors, who race to find their mates using female sex cues. In these systems, the ability of males to locate females quickly is thought to be under strong selection. A rarely tested assumption is that males with more sensory structures are able to locate females faster. In the present study, we used the false garden mantid Pseudomantis albofimbriata to investigate male antennal morphology and its effect on male efficiency in finding a mate. We used scanning electron microscopy to describe the major sensilla types and their arrangement along the length of male antennae. We also conducted field enclosure trials relating male antennal morphology to scramble competition in this system. We identified six different types of antennal sensilla (cheatic, trichoid, basiconic, grooved peg, ceolocapitular and campaniform) on male P. albofimbriata antennae. As expected, males who had more trichoid sensilla located females quicker than did males with fewer sensilla. Results of the current study suggest that antenna morphology plays a significant role in mate location and hence scramble competition in the P. albofimbriata mating system.     

Skin lipids of the striped plateau lizard (<Emphasis Type="Italic">Sceloporus virgatus</Emphasis>) correlate with female receptivity and reproductive quality alongside visual ornaments

Sex pheromones can perform a variety of functions ranging from revealing the location of suitable mates to being honest signals of mate quality, and they are used in the mate selection process by many species of reptile. In this study, we determined whether the skin lipids of female striped plateau lizards (Sceloporus virgatus) can predict the reproductive quality of females, thereby having the potential to serve as pheromones. Using gas chromatography/mass spectrometry, we identified 17 compounds present in skin lipids of female lizards. Using principal component analysis to compare the skin lipid profile of receptive and non-receptive females, we determined that an uncharacterized compound may allow for chemical identification of receptive mates. We also compared extracted principal components to measures of female fitness and reproductive qualities and found that the level of two 18 carbon fatty acids present in a female’s skin lipids may indicate her clutch size. Finally, we compared the information content of the skin lipids to that of female-specific color ornaments to assess whether chemical and visual cues transmit different information or not. We found that the chroma of a female’s orange throat patch is also related to her clutch size, suggesting that chemical signals may reinforce the information communicated by visual ornamentation in this species which would support the “backup signals” hypothesis for multiple signals.