Anita Aisenberg

Daring females, devoted males, and reversed sexual size dimorphism in the sand-dwelling spider Allocosa brasiliensis (Araneae, Lycosidae)

Sexual selection theory predicts that a higher investment in offspring will turn females into the selective sex, while males will compete for accessing and courting them. However, there are exceptions to the rule. When males present a high reproductive investment, sex roles can reverse from typical patterns, turning males into the choosy sex, while females locate males and initiate courtship. In many spiders, males are smaller than females, wandering in search of sedentary females and maximizing the number of copulations. In the present study, we present findings on the sand-dwelling wolf spider, Allocosa brasiliensis, evidencing a reversal in typical courtship roles reported for the first time in spiders. Males were bigger than females. Females located males and initiated courtship. Copulation always occurred in male burrows and took place mainly in long burrows. Males donated their burrows to the females after copulation, closing the entrance before leaving with female cooperation from inside. Males would provide females with a secure place for ovipositing, being exposed to predation and diminishing their future mating possibilities until constructing a new burrow. The cost of vacating the burrow and losing the refuge in an unpredictable habitat, such as sand dunes, would explain the courtship roles reversal in this spider species. Results turn A. brasiliensis as a promising model for discussing the determinants of sex roles and the pressures that drive their evolution and maintenance.

Reversed cannibalism, foraging, and surface activities of Allocosa alticeps and Allocosa brasiliensis: two wolf spiders from coastal sand dunes

Abstract Environments where prey availability is scarce or highly variable have been reported as potential settings for the occurrence of paternal investment and sex-role reversal (choosy males and competitive, courting females). Allocosa brasiliensis (Petrunkevitch 1910) and Allocosa alticeps (Mello-Leitão 1944) are two sand-dwelling wolf spiders that construct burrows along the Uruguayan coastline. Both species present a reversal in typical sex roles and size dimorphism. In the present study, we investigated foraging behavior and population density of both species by performing monthly samplings at the field during one year. Both Allocosa are general and highly opportunistic predators, varying their diet according to prey availability. The three most represented common prey belonged to Araneae, Diptera, and Hymenoptera (Formicidae). There were high levels of cannibalism in A. brasiliensis and, furthermore, males were observed frequently preying on conspecific adult females. Our discussion of the results based on hypotheses about food limitation and sex-role reversal contributes to our understanding of Allocosa species and establishes them as models for future evolutionary, behavioral, and ecological studies.

Sexual behavior, cannibalism, and mating plugs as sticky traps in the orb weaver spider Leucauge argyra (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.

Sexual dimorphism in chelicerae, forelegs and palpal traits in two burrowing wolf spiders (Araneae: Lycosidae) with sex-role reversal

Allocosa alticeps and Allocosa brasiliensis are two sex-role-reversed spiders. Females locate males and initiate courtship. Copulation occurs inside male burrows and after copulation the males deliver their burrows to the females. We explored the occurrence of differences in morphological traits related to sex roles in both Allocosa species and compared the results with two non-burrowing wolf spiders with typical sex roles. We measured the length of the forelegs tibia-patella and the chelicerae. Scanning electron micrographs of palpal tarsus distal sections were taken. Males showed higher values than females in all the traits considered. Adult and penultimate males lacked true claws compared with juveniles and females, but showed modified spines. The palpal organ was more proximal to the tibia compared with the non-burrowing lycosids considered in this study. Spines and palpal organ location could be associated with more effective digging. We discuss how natural and sexual selection could interact on morphology in this scenario.

Behavioural evidence of male volatile pheromones in the sex-role reversed wolf spiders Allocosa brasiliensis and Allocosa alticeps.

The use of chemical signals in a sexual context is widespread in the animal kingdom. Most studies in spiders report the use of female pheromones that attract potential sexual partners. Allocosa brasiliensis and Allocosa alticeps are two burrowing wolf spiders that show sex-role reversal. Females locate male burrows and initiate courtship before males perform any detectable visual or vibratory signal. So, females of these species would be detecting chemical or mechanical cues left by males. Our objective was to explore the potential for male pheromones to play a role in mate detection in A. brasiliensis and A. alticeps. We designed two experiments. In Experiment 1, we tested the occurrence of male contact pheromones by evaluating female courtship when exposed to empty burrows constructed by males or females (control). In Experiment 2, we tested the existence of male volatile pheromones by evaluating female behaviour when exposed to artificial burrows connected to tubes containing males, females or empty tubes (control). Our results suggest the occurrence of male volatile pheromones that trigger female courtship in both Allocosa species. The sex-role reversal postulated for these wolf spiders could be driving the consequent reversal in typical pheromone-emitter and detector roles expected for spiders.

Spatial distribution, burrow depth and temperature: implications for the sexual strategies in two Allocosa wolf spiders

Allocosa brasiliensis and Allocosa alticeps are two burrowing wolf spiders that inhabit Uruguayan sandy coasts. Male efficient digging is necessary because copulation and oviposition occur inside their burrows. We examined burrow distribution, density and temperature variation according to burrow depth. Adult burrows were more frequent at the slope of sand-dunes in A. alticeps and at the base in A. brasiliensis. The base provides better digging conditions, whereas A. alticeps adults could prefer the slope to avoid intra-guild predation. Temperature buffering increased with depth, providing thermal stability in such a harsh environment as coastal dunes.

Cryptic Female Choice in Arthropods

Dipteran females have many opportunities to influence the reproductive success of their mates. After each mating, females may influence their mates’ postcopulatory reproductive success by choosing whether and where to store sperm, whether and when to remate and lay eggs, and how much to invest in eggs fertilized by different males. Female neural, endocrine, and muscular mechanisms are necessary for these processes to occur. We review physiological experiments that have borne this out. Further evidence from many Diptera shows that seminal fluid proteins (Sfps) also influence female post-copulatory processes including ones that affect sperm use. The most comprehensive evidence comes from Drosophila melanogaster, whose seminal proteome is well characterized. In this species, studies of sequence variation, including in natural populations, and of gene-specific knockdown in the laboratory, have identified male and female genes whose actions influence and/or correlate with post-copulatory processes in the female. Furthermore, co-evolution between Sfps and female reproductive proteins suggests their involvement in common functional pathways. We review the evidence for the interaction of Sfp-mediated effects and cryptic female choice (CFC), with a focus on D. melanogaster and evidence from other Diptera as available. L.K. Sirot (*) Department of Biology, College of Wooster, Wooster, OH 44691, USA e-mail: Lsirot@wooster.edu M.F. Wolfner Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY 14853, USA e-mail: mariana.wolfner@cornell.edu 352 L.K. Sirot and M.F. Wolfner Finally, we conclude by assessing what is known and as yet unknown about the interface between CFC and Sfps and by suggesting avenues for further research in this fascinating area.

Spermatozoa and spermiogenesis of the wolf spider Schizocosa malitiosa (Lycosidae, Araneae) and its functional and phylogenetic implications

The wolf spider Schizocosa malitiosa is a well-known model system for studies on sexual selection in spiders. Despite this, little is known about the morphology of the reproductive system and spermatozoa in this species. In the present study, we investigate the male genital system and sperm cells of S. malitiosa using electron microscopy and provide a computer-based 3D reconstruction of the spermatozoa for the first time for arthropods. In general, the male genital system consists of two long, tube-like testes that lead into convoluted deferent ducts. The ejaculatory duct is enlarged and contains a large quantity of sperm and secretion. As revealed by transmission electron microscopy, only one type of secretion droplet is present in the seminal fluid. The spermatozoa of S. malitiosa resemble an organization known for members of the RTA clade, i.e., with an arrow-shaped acrosomal vacuole partly sunk into the nucleus and a chambered centriolar adjunct (a newly introduced character). This organization provides further support for these characters as potential synapomorphies for the RTA clade. By the end of the spermiogenesis, the nucleus and axoneme coils within the cell and a multi-layered secretion sheath are formed representing cleistospermia. The function of the thick secretion sheath is still unknown, but might be correlated either with the residency time in the female (insemination until oviposition) since female S. malitiosa do not lay eggs before the fourth month after copulation or with the receptivity-inhibiting substances suggested for this species.

Timing of female sexual unreceptivity and male adjustment of copulatory behaviour under competition risk in the wolf spider Schizocosa malitiosa

Males can change their copulatory or sperm transfer patterns in response to sperm competition risk. Schizocosa malitiosa performs long copulations, which include two consecutive patterns (Patterns 1 and 2). Virgin females are very sexually receptive, but mated females diminish their receptiveness. Female unreceptivity has been attributed to the action of receptivity-inhibiting substances, mainly transferred during Pattern 1. We tested: (1) if females who mated only with Pattern 1 were immediately unreceptive; (2) male and female behaviours when the copulating couple was exposed to another male. For (1), we interrupted mating when Pattern 1 finished and immediately exposed the female to a second male. For (2), we introduced a second male when the couple was starting (Ei) or finishing copulation (Li). Females were unreceptive immediately after finishing Pattern 1. Males from Ei and Li dismounted and approached the second males. Ei males diminished the frequencies of insertion after perceiving the presence of a second male and dismounted less frequently when copulating with heavy females. The study provides insights about the timing of sexual unreceptivity in S. malitiosa under possibilities of sperm competition, discussing male adjustment of copulatory behaviour in the presence of rival males.

Characterisation of burrow architecture under natural conditions in the sand-dwelling wolf spider Allocosa brasiliensis

Abstract Allocosa brasiliensis (Petrunkevitch, 1910) is a wolf spider that constructs silk-lined burrows along the coastal sand dunes of Argentina, Brazil and Uruguay. This species shows a reversal in typical sex roles and sexual size dimorphism expected for spiders. Females are the smaller and mobile sex, which initiates courtship at the male burrow entrance. Mating occurs in the male burrow, and when it ends, the male leaves and the female stays inside. Females prefer to mate with those males showing longest burrows, so burrow dimensions would be under strong sexual selection pressures. Previous studies in the laboratory indicated that male burrows are longer than those of virgin females, which were described as simple silk capsules. Preliminary observations suggested that juvenile burrows presented differences from those of adults; however, detailed observations of A. brasilienisis burrow characteristics at the field were lacking. The aim of this study was to characterise the burrows of adults and juveniles of A. brasiliensis under natural conditions. We recorded the dimensions of burrows inhabited by males, females and juveniles (n = 30 for each category) and created beeswax moulds that reflected burrow shape. Juveniles inhabited tubular burrows with two branches and two openings; on the contrary, adults were found in tubular burrows with a single entry. Males and females inhabited burrows of similar length and width, but those of juveniles were shorter and narrower. We discuss the results and their possible functional explanations according to the selective pressures expected for each developmental stage and sex.