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Empty nuptial gifts: a further step in the evolution of deception in spiders?
Abstract
In the spider families Trechaleidae and Pisauridae, males offer nuptial gifts to females during courtship. Nutritive gifts contain recently caught prey wrapped in silk, while worthless gifts contain prey leftovers or plant parts. The presence of wrapped gifts is known in three out of 16 genera (Paratrechalea Carico, 2005, Trechalea Thorell, 1869 and Trechaleoides Carico, 2005) in Trechaleidae, suggesting that this sexual trait is of widespread occurrence in the family. Here, we report the presence of wrapped nuptial gifts in the genus Paradossenus F.O. Pickard-Cambridge, 1903. Males of P. longipes (Taczanowski, 1874) produce prey-gifts following the same sequence of behavioral units as described for other species of the family. More surprisingly, these males may also produce empty gifts consisting of a silken structure lacking contents. This is the first record of empty nuptial gifts in spiders. This novel male tactic may have evolved from worthless gifts as a further step in the evolution of deception in gift-giving spiders.
... Other gifts are exogenous and allow males to modify them and deceive the females, creating scope for sexual conflict (Preston-Mafham, 1999;LeBas & Hockham, 2005;Albo et al., 2014aAlbo et al., , 2014b. This seems to be the case in spiders, where males offer females either nutritive gifts (i.e., prey) (Bristowe, 1958;Costa-Schmidt et al., 2008;Trillo & Albo, 2019;Rengifo-Gutiérrez et al., 2021), worthless gifts (i.e., prey leftovers) gathered from the surroundings (Albo et al., 2011(Albo et al., , 2014a, or even empty silk gifts (Martínez-Villar et al., 2020). Female spiders benefit from receiving nutritive gifts as they acquire food that increases their fecundity and survival (Toft & Albo, 2015;Pandulli-Alonso et al., 2017). ...
... The genus includes only two known species, T. keyserlingi and T. biocellata (Carico, 2005), and belongs to the family Trechaleidae. This family consists of 131 species from 17 genera of which 7 have been reported to have males producing silk-wrapped nuptial gifts: Paratrechalea (Costa-Schmidt et al., 2008), Trechalea (Da Silva & Lise, 2009;Lapinski & Tschapka, 2009;Da Silva & Lapinski, 2012), Trechaleoides (Trillo & Albo, 2019), Paradossenus (Martínez-Villar et al., 2020), Enna (Rengifo-Gutiérrez et al., 2021), Dossenus (A. Santos personal communication) and Hesydrus (D. Poy, personal communication). ...
... We hypothesize that the absence of male use of a nuptial gift in T. biocellata is an example of an evolutionary loss of a sexual trait. Nuptial gifts in the form of silk-wrapped food items are widespread in the spider family Trechaleidae, occurring in almost half of the genera (Costa-Schmidt et al., 2008;Da Silva & Lise, 2009;Lapinski & Tschapka, 2009;Da Silva & Lapinski, 2012;Trillo & Albo, 2019;Martínez-Villar et al., 2020;Rengifo-Gutiérrez et al., 2021;A. Santos and D. Poy, personal communication). ...
Evolutionary loss of sexual traits may occur if the forces that maintain those traits weaken or disappear. Females may evolve resistance or a change in preference if the male sexual trait decreases their fitness (e.g., coercive or deceptive traits). In nuptial gift-giving spiders, males offer a food gift wrapped in silk during courtship, taking advantage of female foraging motivation. Males may also produce worthless gifts, which could select for female emancipation from deception and subsequent loss of gift function. This might be the case in the two known species of the spider genus Trechaleoides (Trechaleidae). Here, we examined the females’ preference for nuptial gifts, and gift function as male mating effort and/or male protection in both species. Trechaleoides keyserlingi males offering gifts acquired significantly fewer matings than males without gifts and thus, we verified no female preference for the gift. In T. biocellata males never produced a gift, although they experienced a high risk of pre-copulatory cannibalism. To assess whether T. biocellata females possess a pre-existing sensory bias for nuptial gifts, they were presented with heterospecific T. keyserlingi males with and without gifts. No female preference was detected, and the gift did not protect males from sexual cannibalism. If silk-wrapped nuptial gifts are ancestral in the spider family Trechaleidae, a basal loss of female preference for the gift in the genus Trechaleoides could be hypothesized. This may subsequently have changed the gift’s sexual function in T. keyserlingi and led to the complete loss of the gift-giving behaviour in T. biocellata.
... Under these circumstances, the information carried by potential signals could meet the requirements stated by Lewis et al.'s (2014) definition of nuptial gifts, that is, gifts that are (1) provided by a donor to a recipient during courtship or copulation and (2) effective at improving the donor's fitness. Despite the original definition focusing on the material nature of gifts, usually food items, examples of inedible gifts can be found in both arthropods (LeBas & Hockham, 2005;Martínez Villar et al., 2020, 2021 and birds (Pizzari, 2003;Stokes, 1971). In addition, the value of edible gifts in terms of energy intake is still debated (Morehouse et al., 2020, p. 42). ...
... For instance, males can benefit from modifying their investment in the gift and reduce costs associated with its maintenance according to their own attributes in relation to the environment, as suggested for other sexual traits (Piersma and Drent 2003;Cornwallis and Uller 2010). Traces of evolutionary changes in the content of nuptial gifts from genuine nutritive (fresh prey) to deceptive gifts, such as worthless (prey leftovers) and even empty silk packages, have been observed in some genera of the spider family Trechaleidae (Costa-Schmidt et al. 2008;Albo et al. 2009;Da Silva and Lise 2009;Lapinski and Tschapka 2009;Da Silva and Lapinski 2012;Trillo and Albo 2019;Martínez-Villar et al. 2020;Rengifo-Gutiérrez et al. in press). The diversity of gift types may result in the co-occurrence of different male mating tactics in the population (Endler 1995;Gross 1996;Brockmann 2001;Engqvist and Taborsky 2015) and is evidence of a change in the function of the sexual trait as a source of nutrients. ...
Male sensory exploitation of female gustatory pre-existing bias has been proposed for the origin of nuptial gifts in insects and spiders. This sexual trait may have been beneficial to both sexes, giving mating and survival advantages to males and providing nutritional resources for females. However, the evolution of deceptive worthless gifts is against females’ interests and may trigger a co-evolutionary change in females’ preferences. We evaluated females’ preferences for nuptial gifts and the adaptive function of the gift in the spider Trechaleoides keyserlingi. The genus belongs to the understudied Neotropical family Trechaleidae in which nuptial gifts are widespread. The family is composed of only two species, and the gift seems to be absent in the sister species, creating a relevant scenario for understanding co-evolutionary processes. In the laboratory, we found that although males invested more in nuptial gifts when encountering mated females compared to unmated, they had similar mating access and duration than males lacking a gift. We also found an absence of female choice between males offering nutritive and worthless gifts. Few females were aggressive and cannibalized males, and we did not find evidence that the gift protected males from cannibalism. In the field, 50% of the gifts were worthless items. This is congruent with the laboratory findings where males offering worthless gifts seem to better attract females, which we discuss in the context of exploitation of female gustatory bias. We therefore propose that females may have evolved indifference for the gift and that gift-giving in this species represents a currently non-functional remnant of a behaviour.
Significance statement
Nutritive nuptial gifts can exploit female gustatory preferences, with mutual benefits for both sexes: males can increase mating success and survival, while females increase their fecundity. But males can offer worthless gifts leading females to suboptimal matings, and in turn females can evolve indifference for the trait. The spider genus Trechaleoides is ideal to examine this process because gift-giving behaviour is present in one species and absent in the other. We examined females’ preferences for nuptial gifts and its function for males in the gift-giving species T. keyserlingi. We found that males invest in a gift but gain no reproductive advantage, as females were equally likely to mate with them regardless of whether they offered a gift or whether the gift was nutritive or worthless. We propose that females may have changed their preferences and that the gift is a remnant non-functional trait.
The spider family Trechaleidae includes 17 genera and 131 species distributed throughout the Neotropical region. Most of them are semiaquatic spiders living adjacent to streams and rivers. Very few species of the family have been studied for their natural history or behavior; however four genera (ParatrechaleaCarico, 2005, Trechalea Thorell, 1869, Paradossenus F. O. Pickard-Cambridge, 1903 and TrechaleoidesCarico, 2005) are already known to have males that offer wrapped nuptial gifts to females. Here we describe a new species from the genus Enna O. Pickard-Cambridge, 1897, namely E. gloriae sp. nov. from Quindío, Colombia. We additionally report the presence of males of this species offering nuptial gifts to females during courtship, being the first record of this sexual trait for the genus.
Background
Polyandry is commonly maintained by direct benefits in gift-giving species, so females may remate as an adaptive foraging strategy. However, the assumption of a direct benefit fades in mating systems where male gift-giving behaviour has evolved from offering nutritive to worthless (non-nutritive) items. In the spider Paratrechalea ornata, 70% of gifts in nature are worthless. We therefore predicted female receptivity to be independent of hunger in this species. We exposed poorly-fed and well-fed females to multiple males offering nutritive gifts and well-fed females to males offering worthless gifts.
Results
Though the treatments strongly affected fecundity, females of all groups had similar number of matings. This confirms that female receptivity is independent of their nutritional state, i.e. polyandry does not prevail as a foraging strategy.
Conclusions
In the spider Pisaura mirabilis, in which the majority (62%) of gifts in nature are nutritive, female receptivity depends on hunger. We therefore propose that the dependence of female receptivity on hunger state may have evolved in species with predominantly nutritive gifts but is absent in species with predominantly worthless gifts.
Electronic supplementary material
The online version of this article (doi:10.1186/s12862-017-0953-8) contains supplementary material, which is available to authorized users.
Nuptial gifts are an intriguing male sexually selected trait that has evolved in a wide range of forms among different animals. Wrapped prey gifts have been intensively studied in two spiders: Paratrechalea ornata (Trechaleidae), a neotropical species, and Pisaura mirabilis (Pisauridae), a Palearctic species. Interestingly, these species experience differences in their ecology but show remarkable similarities in sexual behavior, suggesting convergent evolution of the male trait. The origin of nuptial gifts probably was derived from a fecundity advantage to females and a mating advantage to males. However, the benefits to each sex might be sensitive to fluctuations in food availability, leading to antagonistic co-evolution. When food is scarce, males may deceive females by providing worthless gifts and females may counter this exploitation by limiting sperm transfer. We review studies on the function and evolution of nuptial gifts, particularly comparing the neotropical with the Palearctic species, and discuss evolutionary implications of nuptial gifts for males and females.
Animal nuptial gifts display multitudinous forms, and such gifts are especially interesting because they sit at the intersection of sexual selection, foraging ecology, and life-history evolution. However, even though such gifts are likely to play key roles in sexual selection and conflict, remarkably little is known about the selective agents responsible for their origin and maintenance.In this chapter, we propose a classification scheme based on (1) how gifts are produced (endogenous vs. exogenous) and also (2) how they are absorbed by the recipient (oral, genital, or transdermal). This classification provides a conceptual framework that should prove useful for formulating and testing predictions about how different gift types affect fitness of both males and females. Moving beyond earlier work that had coerced potential benefits to gift-giving males into the falsely dichotomous categories of parental investment versus mating effort, we illustrate how nuptial gifts might enhance male fitness across multiple selection episodes that occur before, during, and after mating. Finally, we highlight a few studies that have used comparative phylogenetic methods to see how nuptial gifts and other life-history traits may have changed over evolutionary time. One such study analyzed the evolutionary trajectories of spermatophore gifts within firefly beetles (Coleoptera: Lampyridae), revealing that male gifts have undergone correlated evolution with female flight ability. Thus, this study supports the idea that shifts in female resource allocation may potentially drive male investment in nuptial gifts.Looking forward, phylogenetic analyses across different taxonomic groups will be needed to provide insight into the evolutionary origin and maintenance of nuptial gifts. By including relevant ecological and life-history traits associated with resource allocation, such studies will undoubtedly expand our understanding of nuptial gift evolution.
Uniquely positioned at the intersection of sexual selection, nutritional ecology and life-history theory, nuptial gifts are widespread and diverse. Despite extensive empirical study, we still have only a rudimentary understanding of gift evolution because we lack a unified conceptual framework for considering these traits. In this opinion piece, we tackle several issues that we believe have substantively hindered progress in this area. Here, we: (i) present a comprehensive definition and classification scheme for nuptial gifts (including those transferred by simultaneous hermaphrodites), (ii) outline evolutionary predictions for different gift types, and (iii) highlight some research directions to help facilitate progress in this field.
Nuptial gift offering is a courtship trait found among several insect orders and some spider families. Recent studies indicate that this gift-giving behavior in spiders represents the male mating effort acting on female receptivity through a mechanism of foraging motivation. However, little attention has been given to the sensory channels that are influencing female acceptance. To understand the role of these sensory channels in female perception of a nuptial gift, we focused on the nuptial gift of the neotropical spider Paratrechalea ornata (Araneae, Trechaleidae). The nuptial gift of this species is composed of a prey item wrapped in silk, and previous works suggest that visual and/or chemical cues may be involved in inducing female grasping behavior. We isolated sensory channels using mimetic nuptial gifts (artificial items) or by manipulating real nuptial gifts. Isolated visual signals were not responsible for female acceptance, whereas chemical signals found within the nuptial gift silk layer induced female acceptance. Our findings clearly indicate that a chemical signal located in the silk of the nuptial gift is the main attractant channel, and we formulated 2 hypotheses to explain the mechanisms of action in the female sensory system. We also discuss the consequences of such signaling over female acceptance.
Courtship displays of empidine dance flies (Diptera: Empididae), which include transfers of nuptial gifts during mating, are reviewed in light of sexual selection theory. Sex-role reversed courtship behavior, involving female swarming and male choice, appears to be correlated with certain female secondary sexual characters that are widespread throughout the Empidinae. The tendency to shift mate choice from females to males, and the apparent development of autogeny in many empidine species, are both hypothesized to have resulted from males monopolizing the proteinaceous food source of non-hunting females, through transfers of nuptial gifts of prey. The autogenous condition appears to have led to the ritualized presentation of various types of inedible nuptial gifts by males of several species, possibly including the development of secreted nuptial gifts, or balloons, as displays of male fitness.
By wrapping prey and offering it as a nuptial gift, males can obtain mating and/or parental benefits despite some costs. Males of the Neotropical semiaquatic spider Paratrechalea ornata (Trechaleidae) offer females a nuptial gift consisting of a prey item wrapped in silk. What stimulus inhibits males from feeding and elicits gift construction? We hypothesized that signals associated with female silk threads could affect decision-making by males. We investigated three groups of males carrying a captured prey under different experimental treatments. In the treatment S, males were exposed to an arena with female silk; in SF, males were exposed to both silk and a female confined in a cell, and in the control group, males were exposed to a clean arena. Gift construction was observed only in the S and SF groups, with a similar occurrence rate. After touching females (SF group), males did not change their pattern of gift construction. Gift construction occurrence increased with male and female age. The results lead us to assume that the existence of chemical cues associated with female silk elicits male searching behaviour and gift construction, allowing males to decide between eating or wrapping prey according to the possibility of a sexual encounter. Anticipating gift construction, males are ready to mate, diminishing the risks of predation, female desertion or male–male scramble competition. The effect of age on behavioural variation and the rate of construction is discussed.
Adaptive female choice is thought to have led to the evolution of nutritionally valuable nuptial gifts in many insect species.
However, in several dance fly species, males offer and females accept “empty gifts” with no nutritional value. In the species
studied here, Empis snoddyi Steyskal, males produce empty balloons comprised of hundreds of silk bubbles and form mating swarms that females approach
to investigate males. Males within the swarm engage in agonistic interactions. The empty balloon has been hypothesized to
be an indicator of male condition such that males with larger balloons are predicted to have higher mating success and be
more successful in male-male interactions than males with smaller balloons. We examined the role of male body size and balloon
size in the context of intersexual and intrasexual selection. We found that neither male body size nor balloon size affected
the outcome of pairwise male-male interactions. Using multiple-regression techniques, we found significant linear selection
for increasing male body size and decreasing balloon size associated with mating success, a surprising result given a positive
relationship between male body size and balloon size. A visualization of selection showed the highest peak of male mating
success for larger males with intermediate-size balloons. These results can be explained by a trade-off between long-range
attraction of females using large balloons and close-range attraction of females via improved flying efficiency associated
with smaller balloons. Both male body size and balloon size are important components in determining male mating success; however,
the empty balloon does not appear to play a typical role as a sexually selected ornament.
In 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).
Males 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.
We 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.
The first record of a nuptial gift in Trechalea amazonica F.O.P.-Cambridge, 1903, is herein presented. The observations were made in the Oriximiná, Pará, northern Brazil. Two males were found on tree trunks near the water, each holding in the chelicerae a small prey wrapped in silk. This is the second confirmed observa - tion of the nuptial gift behavior in the family Trechaleidae, first in the genus Trechalea Thorell, 1869, and later in Paratrechalea Carico, 2005 from southern Brazil. This new observation could be used in phylogenetic and evolutionary studies for this poorly studied spider family.
Edible and seminal gifts that male arthropods transfer to their mates range from important material donations to items that provide little direct benefit. Recent reviews and research have emphasized the negative effect of gifts on female fitness, suggesting that male donations reduce the female's remating rate below her optimum or even that nuptial feeding is a net detriment to her fitness. However, comparative, experimental, and natural history evidence reveal that most edible gifts of prey or glandular products provide direct benefits to females. Gifts clearly supply nutrients when females compete for them or increase mating rates when food from other sources is limited. I point out the difficulties in determining that female remating rates are suboptimal and suggest several alternative hypotheses for the apparently low female mating rates in some gift-giving species. With regard to seminal contributions (absorbed from the ejaculate), I discuss how to separate hormonal (potentially manipulative) and material-benefit effects of male secretions on females.
Male delivering of a prey packed in silk as a nuptial gift is rare in spiders and restricted until now to Pisauridae. Here, we describe this behavioral pattern found in two Trechaleidae species, Paratrechalea azul Carico 2005, and Paratrechalea ornata (Mello-Leitão 1943), mainly based on field observations. We observed the following steps of sexual behavior: sperm induction, nuptial gift construction, mate searching, pre-copulatory courtship, copulation, and copulatory ending. In this group, a nuptial gift consists of a prey wrapped in silk, which appears as a white rounded shape. The male carries his nuptial gift in his chelicerae while searching for a female. When he finds a female, he shows a stereotyped courting behavior consisting of a hyperflexed posture that is also assumed by the receptive female while they face each other. The copulatory position and pattern is similar to that found in other Lycosoidea: the male mounts the female and makes a total of four palpal insertions while alternating sides. However, after each palpal insertion the male dismounts and returns to a frontal position while biting the gift. Copulatory courtship is evidenced by palpal and leg movements. The copulation ends by female initiative and she almost always retains the nuptial gift. No case of pre-copulatory or post-copulatory cannibalism has been recorded. Descriptions of nuptial gift construction by males and copulation in these species, as well as hypotheses about the origin of nuptial gift construction among spiders, are presented. These descriptions are the first records of such nuptial gift offering for Neotropical spiders and for non-Pisauridae species as well.
In some spiders, nuptial gifts consist of prey or inedible items wrapped in silk by males and offered to females during courtship. Such gifts occur in the Neotropical family Trechaleidae, of which most species are semi-aquatic, associated with watercourses in riparian habitats. Here, we describe the sexual behaviour of the South American species Trechaleoides keyserlingi and report the presence of nuptial gift-giving behaviour for the first time in the genus.
Nuptial feeding encompasses any form of nutrient transfer from the male to the female during or directly after courtship and/or copulation. In insects, nuptial gifts may take the form of food captured or collected by the male, parts, or even the whole of the male's body, or glandular products of the male such as salivary secretions, external glandular secretions, the spermatophore and substances in the ejaculate. Over the past decade, there has been considerable debate over the current function of nuptial feeding in insects. This debate has centred on the issue of whether nuptial gifts function as paternal investment (i.e. function to increase the fitness and/or number of the gift-giving male's own offspring) or as mating effort (i.e. function to attract females, facilitate coupling, and/or to maximize ejaculate transfer), although the two hypotheses are not mutually exclusive. In the present article, evidence for the potential of nuptial gifts to function as either paternal investment, mating effort, or both is reviewed for each form of nuptial feeding in each insect taxon for which sufficient data are available. Empirical evidence suggests that many diverse forms of nuptial feeding in different insect taxa function, at least in part, as mating effort. For example, nuptial prey and salivary masses in the Mecoptera, regurgitated food in Drosophila (Diptera), hind-wing feeding in Cyphoderris (Orthoptera) and the secretion of the male's cephalic gland in Neopyrochroa (Coleoptera) and Zorotypus (Zoraptera) appear to function to entice females to copulate and/or to facilitate coupling. Nuptial prey and salivary masses in the Mecoptera also appear to function to maximize ejaculate transfer (which is also a form of mating effort), as do nuptial prey in Empis (Diptera), external glandular secretions in Oecanthus and Allonemobius (Orthoptera) and the spermatophylax in gryllids and tettigoniids (Orthoptera). Large spermatophores in, for example, the Lepidoptera and Coleoptera, also appear to be maintained by selection on the male to maximize ejaculate transfer and thereby counter the effects of sperm competition. In contrast to the large amount of evidence in support of the mating effort hypothesis, there is a relative lack of good evidence to support the paternal investment hypothesis. Certain studies have demonstrated an increase in the weight and/or number of eggs laid as a result of the receipt of larger gifts, or a greater number of gifts, in tettigoniids, gryllids, acridids, mantids, bruchid beetles, drosophilids and lepidopterans. However, virtually all of these studies (with the possible exception of studies of the spermatophylax in tettigoniids) have failed to control adequately for hormonal substances in the ejaculate that are known to affect female reproductive output. Furthermore, in at least four tettigoniids (but not in the case of two species), three lepidopterans, a drosophilid and probably also bruchid beetles and bittacids, evidence suggests that the male has a low probability of fertilising the eggs that stand to benefit from his nuptial gift nutrients. Therefore, the hypothesis that paternal investment might account for the function of nuptial gifts in general is not supported.
The genus Trechalea Thorell, 1869 was revised by Carico (1993), who redescribed the eight species known at that time and described two new species, Trechalea boliviensis Carico, 1993 and Trechalea lomalinda Carico, 1993, which were recently transferred to Syntrechalea F.O. Pickard-Cambridge, 1902 by Silva et al. (2012). Presently, the genus comprises eight species, distributed from Southern Arizona, USA to Northern Argentina (Platnick 2012). Other taxonomic papers on Trechalea were made by Carico (2008b), who described male of T. trinidadensis Carico, 1993, and Carico & Silva (2010) who described a new species, T. rothi Carico & Silva, 2010, from Colombia. Both species were synonymized by Silva & Lise (2010) with T. amazonica F.O. Pickard-Cambridge, 1903.
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 life-long virginity.This article is protected by copyright. All rights reserved.
Summary After a short review of the literature, beginning with the discovery of the nuptial gift of the nursery-web spider Pisaura mirabilis (Clerck, 1757) in 1884 by Van Hasselt, the courtship, mating, agonistic behaviour, and peaceful coexistence of a female with two males in a planted terrarium are described (Table 1). Details of the normal mating process with a wrapped fly of different sizes are given (Figs. 3–10). Copulations occurred during both day and night. Eyesight seems to be of little importance for recognition of sexes and the gift, apart from perceiving movements. Mating variations using a freshly caught unwrapped fly (Lucilia) (Figs. 11–12), a small fly (one Drosophila), a wrapped substitute (heather blossom, Fig. 13) and even without any gift (Figs. 14–15, 23) are shown (Table 4). Males can even perform successfully with females with prey or egg sacs and on nursery webs. Agonistic behaviour, gift robbery, disturbance of mating by a rival, a threesome with one female and two males, but also peaceful male-male encounters are described and illustrated (Figs. 16–23, Table 3). Intersexual aggression and sexual cannibalism are demonstrated and discussed. The so-called “feigning death” of males (Fig. 8) is considered as an evolutionarily stable trick of the male to maintain contact with the female within the dense layer of the herbaceous stratum if she suddenly runs away after a disturbance, or simply for recovering the gift. This behaviour also occurs when two males share one gift (Fig. 22) and try to copulate with each other (Fig. 19). The benefits and disadvantages of the different kinds of gifts, evolution of the gift, its functions and the degree of cannibalism are discussed. Comparisons with the mating behaviour of related Pisauridae and Trechaleidae species using gifts and silk in courtship are made, and suggestions for further research are given.
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.
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.
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 females.
Adult males of the hunting spider Pisaura mirabilis wrap up prey with silk and pass these nuptial gifts to females prior to copulation. The females digest the nuptial gifts, including the silk, during mating. Laboratory experiments were carried out to determine the amount of silk males of P. mirabilis invest in nuptial gifts, and its possible role in sexual reproduction. The amount of silk was always small, indicating that the silk of the nuptial gift has little nutritional value for females. Males that had more time to wrap up the prey produced a larger amount of silk. Starved males required more time than satiated males to produce a given amount of silk. A larger male body size had a positive effect on the amount of silk. In general, the size of the prey used for nuptial gifts had no influence on the amount of silk. However, due to handling problem, smaller males produced no silk for very large flies. Females took more time to digest a nuptial gift with a larger amount of silk than a nuptial gift with a smaller amount of silk. A possible interpretation of the adaptive significance of wrapping is that males use silk to prolong the copulation time during mating.
The nuptial prey gift in the spider Pisaura mirabilis has been suggested to function as a male protection against sexual canni- balism during courtship and mating. This hypothesis together with two alternatives—male mating effort and paternal investment hypotheses—were tested in a laboratory experiment with sexually inexperienced males and females. One group of males offered no gift to the female while three groups of males offered small, medium, or large sized gifts, respectively. No male was canni- balized among 82 trials. Aggression was observed only in encounters where a gift was presented. Males without a gift courted females, and 40% of these males managed to copulate, compared to 90% of males offering a gift. The copulation duration was positively correlated with gift size. In general, the female terminated the copulation and ran away with the gift. The proportion of eggs fertilized increased with copulation time. Presence or size of the nuptial gift did not affect female fecundity or spiderling size significantly. The results refute the hypotheses of sexual cannibalism and paternal investment. The nuptial gift represents a male mating effort; it entices the female to copulate, facilitates coupling during copulation, and by prolonging copulation it may increase the amount of sperm transferred. I conclude that the nuptial prey gift in Pisaura mirabilis is maintained by sexual selection. Key words: female choice, mating effort, natural selection, nuptial gift, paternal investment, Pisaura mirabilis, sexual cannibalism, sexual selection, spider. (Behav Ecol 12:691-697 (2001))
Two new genera in the spider family Trechaleidae, Trechaleoides and Paratrechalea, are described. The females of the two known species of Trechaleoides, T. keyserlingi (F.O.P.-Cambridge) (type species) and T. biocellata (Mello-Leitão) are redescribed and their respective males are described for the first time; both are transferred from Trechalea. Two additional previously described species, also both transferred from Trechalea, are herein placed in the genus Paratrechalea are redescribed from their types, i.e., the female of P. ornata (Mello-Leitão) (type species) and male of P. wygodzinskyi (Soares & Camargo). The male of P. ornata is described for the first time. Four new species of Paratrechalea, P. longigaster, P. galianoae, and P. azul from females, and P. saopaulo from males and females are described. The immature specimen historically regarded as the holotype of Trechalea longitarsis (C.L. Koch) and regarded as a mistaken identity, is an unidentified species of Trechaleoides. The female holotype of Trechalea limai Mello-Leitão is confirmed to be lost but is considered to be a member of the genus Paratrechalea based on a study of the original description.
The Neotropical spider genus Paradossenus is revised and currently comprises a total of 14 species. P. andinus (Simon 1898), P. protentus (Karsch 1879) and P. venezuelanus (Simon 1898) are new junior synonyms of P. longipes (Taczanowski 1874), the type species of the genus. Five known species, P. longipes, P. caricoi Sierwald 1993, P. pulcher Sierwald 1993, P. corumba Brescovit & Raizer 2000, and P. minimus (Mello-Leitão 1940), are redescribed and illustrated. New species: P. isthmus, P. benicito, P. amazonensis, P. acanthocymbium, P. tocantins and P. pozo are described from both male and female. The new species P. sabana is described only from the male while P. junin is described only from the female. The subfamily Trechaleinae is erected, diagnosed, and an illustrated key to all the included genera is presented.
Nuptial feeding encompasses any form of nutrient transfer from
the male to the female during or directly after
courtship and/or copulation. In insects, nuptial gifts may take the
form of food captured or collected by the
male, parts, or even the whole of the male's body, or glandular
products of the male such as salivary
secretions, external glandular secretions, the spermatophore and
substances in the ejaculate. Over the past
decade, there has been considerable debate over the current function
of nuptial feeding in insects. This
debate has centred on the issue of whether nuptial gifts function as
paternal investment (i.e. function to
increase the fitness and/or number of the gift-giving male's
own offspring) or as mating effort (i.e. function
to attract females, facilitate coupling, and/or to maximize
ejaculate transfer), although the two hypotheses
are not mutually exclusive. In the present article, evidence for the
potential of nuptial gifts to function as
either paternal investment, mating effort, or both is reviewed for
each form of nuptial feeding in each insect
taxon for which sufficient data are available. Empirical evidence suggests
that many diverse forms of nuptial
feeding in different insect taxa function, at least in part, as
mating effort. For example, nuptial prey and
salivary masses in the Mecoptera, regurgitated food in Drosophila
(Diptera),
hind-wing feeding in Cyphoderris
(Orthoptera) and the secretion of the male's cephalic gland in
Neopyrochroa (Coleoptera) and Zorotypus
(Zoraptera) appear to function to entice females to copulate and/or
to
facilitate coupling. Nuptial prey and
salivary masses in the Mecoptera also appear to function to maximize
ejaculate transfer (which is also a form
of mating effort), as do nuptial prey in Empis (Diptera),
external glandular secretions in Oecanthus and
Allonemobius (Orthoptera) and the spermatophylax in gryllids and
tettigoniids (Orthoptera). Large
spermatophores in, for example, the Lepidoptera and Coleoptera, also
appear to be maintained by selection
on the male to maximize ejaculate transfer and thereby counter the effects
of sperm competition. In contrast
to the large amount of evidence in support of the mating effort hypothesis,
there is a relative lack of good
evidence to support the paternal investment hypothesis. Certain studies
have demonstrated an increase in
the weight and/or number of eggs laid as a result of the receipt of
larger gifts, or a greater number of gifts,
in tettigoniids, gryllids, acridids, mantids, bruchid beetles, drosophilids
and lepidopterans. However,
virtually all of these studies (with the possible exception of studies
of the spermatophylax in tettigoniids) have
failed to control adequately for hormonal substances in the ejaculate
that are known to affect female
reproductive output. Furthermore, in at least four tettigoniids (but
not in the case of two species), three
lepidopterans, a drosophilid and probably also bruchid beetles and
bittacids, evidence suggests that the male
has a low probability of fertilising the eggs that stand to benefit
from his nuptial gift nutrients. Therefore,
the hypothesis that paternal investment might account for the function
of nuptial gifts in general is not supported.
Males of the spider Pisaura mirabilis present a nuptial prey gift to the female during courtship as a mating effort. The gift is usually round and wrapped in white silk. It was suggested that the wrapped gift functions as a sensory trap by mimicking the female’s eggsac implying that males exploit the female maternal care instinct and not her foraging motivation in a sexual context. The shape of the gift (round) and appearance (white) should then increase female acceptance of males. We tested these predictions experimentally and found that neither gift shape (round or oblong) nor silk wrapping (wrapped or unwrapped) facilitated female acceptance, in contrast unwrapped gifts were accepted faster than wrapped ones. Instead, we found that silk wrapping benefited the males because it significantly decreased the risk of females stealing the gift without copulation and consequently directly increased male mating success. Large oblong gifts were difficult for males to handle during copulation, resulting in shorter copulations for oblong vs. round gifts. Thus, round gifts were not preferred by the females but were beneficial to the males. Our results indicate two adaptive benefits to males of wrapping the nuptial gift: to reduce the risk of losing the gift to females without copulation, and make it possible to reshape an oblong prey into a round gift that facilitates the male’s access to the female’s genitalia. Our results suggest that the male gift wrapping trait may be selected though sexual conflict over remating rate.
Selección sexual y citogenética en arañas donadoras de regalos nupciales
- M J Albo
Albo, M.J. 2009. Selección sexual y citogenética en arañas donadoras
de regalos nupciales (Trechaleidae y Pisauridae). Master Thesis,
PEDECIBA. Montevideo, Uruguay.
The World of Spiders
- W S Bristowe
Bristowe W.S. 1958. The World of Spiders. Collins, London.
World Spider Catalog version 16
- World Spider Catalog
World Spider Catalog. 2019: World Spider Catalog version 16. Bern:
Natural History Museum, online at http://wsc.nmbe.ch
Emerging issues in the evolution of animal nuptial gifts.
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