Maria J. Albo

Nuptial gift-giving behaviour and male mating effort in the Neotropical spider Paratrechalea ornata (Trechaleidae)

The occurrence of nuptial gifts is rare in spiders, being well known only for a single species, Pisaura mirabilis (Pisauridae), whose males offer females a prey wrapped in silk during courtship. Although some males can mate without offering a prey, the gift in this species is thought to represent male mating effort. Male gift offering has been recently described in Paratrechalea ornata , a Neotropical spider belonging to another family, Trechaleidae. We investigated the function of the gift in this species by testing the mating effort hypothesis and two other nonexclusive hypotheses, sexual cannibalism avoidance and paternal investment. Two groups of males were exposed to virgin females: 23 males with no prey (NP group) and 21 males carrying a prey (CP group). Mating success, courtship, copulation and first oviposition were recorded. Males from group CP had better mating success, longer copulations and longer palpal insertions than those from NP. Longer copulations were associated with earlier eggsac construction and oviposition. Some unmated males from NP wrapped prey carrion when they returned to their breeding jars after the trial. Our findings suggest that nuptial gift giving represents male mating effort for P. ornata . Nuptial gifts would allow males to control copulation duration and to accelerate female oviposition, improving sperm supply and paternity, and minimizing possible costs of remating with polyandrous

Worthless donations: male deception and female counter play in a nuptial gift-giving spider

BackgroundIn nuptial gift-giving species, benefits of acquiring a mate may select for male deception by donation of worthless gifts. We investigated the effect of worthless gifts on mating success in the spider Pisaura mirabilis. Males usually offer an insect prey wrapped in silk; however, worthless gifts containing inedible items are reported. We tested male mating success in the following experimental groups: protein enriched fly gift (PG), regular fly gift (FG), worthless gift (WG), or no gift (NG).ResultsMales that offered worthless gifts acquired similar mating success as males offering nutritional gifts, while males with no gift experienced reduced mating success. The results suggest that strong selection on the nuptial gift-giving trait facilitates male deception by donation of worthless gifts. Females terminated matings faster when males offered worthless donations; this demonstrate a cost of deception for the males as shorter matings lead to reduced sperm transfer and thus give the deceiving males a disadvantage in sperm competition.ConclusionWe propose that the gift wrapping trait allows males to exploit female foraging preference by disguising the gift content thus deceiving females into mating without acquiring direct benefits. Female preference for a genuine prey gift combined with control over mating duration, however, counteracts the male deception.

Sperm storage mediated by cryptic female choice for nuptial gifts

Polyandrous females are expected to discriminate among males through postcopulatory cryptic mate choice. Yet, there is surprisingly little unequivocal evidence for female-mediated cryptic sperm choice. In species in which nuptial gifts facilitate mating, females may gain indirect benefits through preferential storage of sperm from gift-giving males if the gift signals male quality. We tested this hypothesis in the spider Pisaura mirabilis by quantifying the number of sperm stored in response to copulation with males with or without a nuptial gift, while experimentally controlling copulation duration. We further assessed the effect of gift presence and copulation duration on egg-hatching success in matings with uninterrupted copulations with gift-giving males. We show that females mated to gift-giving males stored more sperm and experienced 17% higher egg-hatching success, compared with those mated to no-gift males, despite matched copulation durations. Uninterrupted copulations resulted in both increased sperm storage and egg-hatching success. Our study confirms the prediction that the nuptial gift as a male signal is under positive sexual selection by females through cryptic sperm storage. In addition, the gift facilitates longer copulations and increased sperm transfer providing two different types of advantage to gift-giving in males.

Condition dependence of male nuptial gift construction in the spider Pisaura mirabilis (Pisauridae)

Pisaura mirabilis males offer a prey wrapped in silk as a nuptial gift that functions as a male mating effort. If nuptial gift construction is costly, males in poor feeding condition would invest less in this behaviour than males in good condition. We investigated frequencies and characteristics of gift construction in males under different sexual stimuli and different feeding conditions. We analysed gift construction behaviours of 17 males exposed sequentially to three treatments: female silk (S), female silk plus female (SF) and no female cues (control; C). The same individuals were first tested when in good feeding condition (young/satiated) and subsequently in poor feeding condition (old/starved). A separate group in good feeding condition controlling for effects of male age was also tested (old/satiated). Presence of female cues (S and SF) elicited much stronger gift construction response in males compared with the control group. Both groups of satiated males constructed nuptial gifts more frequently than starved males, spending more time on gift construction and using more silk. Our findings show that poor feeding condition affects pre-copulatory gift construction behaviour. Nuptial gift construction may be an honest indicator of male condition and therefore a target of female choice.

Female spiders ignore condition-dependent information from nuptial gift wrapping when choosing mates

In many species, condition-dependent secondary sexual traits are important for female choice. In the spider Pisaura mirabilis, males offer females a nuptial gift (prey wrapped in silk) during courtship. Gift construction may involve high costs for males, and those in low condition invest less time and silk in wrapping the prey. We investigated how male condition and gift wrapping affect male reproductive success and whether females use the wrapped gift as an honest indicator of male condition. We experimentally manipulated male condition (satiated and starved males) and gift wrapping (well- and poorly wrapped gifts) and carried out experiments in a fully factorial design. We found that males in good condition were more successful in obtaining matings and obtained longer copulations than males in poor condition. In contrast, gift wrapping did not affect female mate choice. Only good-condition males obtained offspring. Gift wrapping is an honest indicator of male condition, but in spite of this females did not use this information in mate choice. We argue that because gift wrapping mainly functions to promote male interests, good-condition males would also be better at cheating the female, for example using wrapping to hide a worthless gift. Females should therefore evolve to ignore the wrapping information and instead base their mate choice decision on male traits that unequivocally benefit their own reproductive success. Our results are consistent with this prediction, as females discriminated males based only on their actual feeding condition, and this choice provided them with direct reproductive benefits.

Polyandrous females acquire indirect benefits in a nuptial feeding species

The relative force of direct and indirect selection underlying the evolution of polyandry is contentious. When females acquire direct benefits during mating, indirect benefits are often considered negligible. Although direct benefits are likely to play a prominent role in the evolution of polyandry, post‐mating selection for indirect benefits may subsequently evolve. We examined whether polyandrous females acquire indirect benefits and quantified direct and indirect effects of multiple mating on female fitness in a nuptial gift‐giving spider (Pisaura mirabilis). In this system, the food item donated by males during mating predicts direct benefits of polyandry. We compared fecundity, fertility and survival of singly mated females to that of females mated three times with the same (monogamy) or different (polyandry) males in a two‐factorial design where females were kept under high and low feeding conditions. Greater access to nutrients and sperm had surprisingly little positive effect on fitness, apart from shortening the time until oviposition. In contrast, polyandry increased female reproductive success by increasing the probability of oviposition, and egg hatching success indicating that indirect benefits arise from mating with several different mating partners rather than resources transferred by males. The evolution of polyandry in a male‐resource‐based mating system may result from exploitation of the female foraging motivation and that indirect genetic benefits are subsequently derived resulting from co‐evolutionary post‐mating processes to gain a reproductive advantage or to counter costs of mating. Importantly, indirect benefits may represent an additional explanation for the maintenance of polyandry.

Optimal numbers of matings: the conditional balance between benefits and costs of mating for females of a nuptial gift-giving spider

In species where females gain a nutritious nuptial gift during mating, the balance between benefits and costs of mating may depend on access to food. This means that there is not one optimal number of matings for the female but a range of optimal mating numbers. With increasing food availability, the optimal number of matings for a female should vary from the number necessary only for fertilization of her eggs to the number needed also for producing these eggs. In three experimental series, the average number of matings for females of the nuptial gift‐giving spider Pisaura mirabilis before egg sac construction varied from 2 to 16 with food‐limited females generally accepting more matings than well‐fed females. Minimal level of optimal mating number for females at satiation feeding conditions was predicted to be 2–3; in an experimental test, the median number was 2 (range 0–4). Multiple mating gave benefits in terms of increased fecundity and increased egg hatching success up to the third mating, and it had costs in terms of reduced fecundity, reduced egg hatching success after the third mating, and lower offspring size. The level of polyandry seems to vary with the female optimum, regulated by a satiation‐dependent resistance to mating, potentially leaving satiated females in lifelong virginity.

The shield effect: nuptial gifts protect males against pre-copulatory sexual cannibalism

Several not mutually exclusive functions have been ascribed to nuptial gifts across different taxa. Although the idea that a nuptial prey gift may protect the male from pre-copulatory sexual cannibalism is attractive, it has previously been considered of no importance based on indirect evidence and rejected by experimental tests. We reinvestigated whether nuptial gifts may function as a shield against female attacks during mating encounters in the spider Pisaura mirabilis and whether female hunger influences the likelihood of cannibalistic attacks. The results showed that pre-copulatory sexual cannibalism was enhanced when males courted without a gift and this was independent of female hunger. We propose that the nuptial gift trait has evolved partly as a counteradaptation to female aggression in this spider species.

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.

Evolution of worthless gifts is favoured by male condition and prey access in spiders

Males from gift-giving species attempt to obtain food to offer to females. Therefore, food access may affect both their body condition and their reproductive success. In some species, males reduce the costs associated with giving gifts by reusing gifts, or by offering inedible items. Males from the spider Paratrechalea ornata (Trechaleidae) offer fresh prey or ‘genuine gifts’ to females, but also offer prey leftovers or ‘worthless gifts’. We examined gift weight and content, and their relation to male condition in the field. We also investigated how gift content, male condition and female reproductive status (virgin/mated) affect male mating success. In the field, most gifts were worthless; genuine gifts were heavier than worthless ones; and gift weights (both genuine and worthless gifts combined) were positively correlated with male condition. In the laboratory, males in good condition had higher mating success than males in poor condition. Males offering gifts (genuine or worthless) to virgin females enjoyed similar mating success and duration; neither differed significantly when compared to males without gift. In contrast, mated females behaved differently. Males without gifts were consistently rejected by mated females, while those that offered worthless gifts achieved matings. The interplay between male condition, prey access, female mating history and female preferences for gifts can favour the evolution of worthless gifts under certain conditions. Females do not penalize males with non-nutritive items by not mating or by reducing mating duration, but penalties may be potentially exerted via postcopulatory process.