Paratrechalea Ornata Research Articles

Variability in Precipitation Weakens Sexual Selection for Nuptial Gifts in Spiders.

AbstractEnvironmental conditions (i.e., climatic variation) can strongly influence the cost and benefits of reproductive traits. Yet there is still no consensus on whether changing environmental conditions strengthen or relax sexual selection. Evidence from the literature suggests that highly variable environments can limit mate choice and investment in sexual traits, hence relaxing sexual selection pressures. Here, we tested this hypothesis using the nuptial gift-giving spider Paratrechalea ornata, in which males can either wrap nutritive (fresh prey) or worthless (prey leftovers) items in silk. We examined changes in males' sexual trait and female choice among six populations living under different climatic conditions. We found that large variation in precipitation limits female choice, potentially favoring the spread of deceptive worthless gifts. In populations under highly variable conditions and with the highest frequencies of worthless gifts (70%), males offering such gifts acquire longer mating durations than those offering nutritive gifts. In contrast, in populations with less variable conditions and the lowest frequencies of worthless gift (36%), females shortened mating duration to males offering worthless gifts. Our findings are consistent with the prediction that highly variable environmental conditions relax sexual selection.

Stressful environments favor deceptive alternative mating tactics to become dominant

BackgroundDeceptive alternative mating tactics are commonly maintained at low frequencies within populations because males using them are less competitive and acquire lower fitness than those using dominant tactics. However, the successful invasion of a male deceptive tactic is plausible if deception carries no fitness cost to females. Among populations of the gift-giving spider Paratrechalea ornata, males very often offer females a deceptive worthless gift, rather than a nutritive gift. We tested the degree to which deceptive worthless gifts can occur in natural populations living under divergent environmental conditions (moderate and stressful). We examined the plasticity of morphological and behavioral traits and analyzed the fitness of females in relation to the gift type, also examining the paternity acquired by males offering either gift type.ResultsWe demonstrated that worthless gifts can become dominant under highly stressful environmental conditions (84–100%). Individuals in such environment reach smaller sizes than those in moderate conditions. We suggest that the size reduction probably favors low metabolic demands in both sexes and may reduce the costs associated with receiving deceptive worthless gifts for females. In contrast, males living under moderate conditions varied the use of the deceptive tactic (0–95%), and worthless gifts negatively influenced female fecundity. Furthermore, male size, rather than gift content, positively impacted paternity success in the moderate but not in the stressful environment.ConclusionsOverall, this is the first empirical evidence that a reversible deceptive tactic can become dominant when the environment becomes harsh and mate choice becomes limited.

Beyond the prey: male spiders highly invest in silk when producing worthless gifts.

In the spider Paratrechalea ornata, males have two gift-giving mating tactics, offering either a nutritive (prey) or a worthless (prey leftovers) silk wrapped gift to females. Both gift types confer similar mating success and duration and afford males a higher success rate than when they offer no gift. If this lack of difference in the reproductive benefits is true, we would expect all males to offer a gift but some males to offer a worthless gift even if prey are available. To test this, we allowed 18 males to court multiple females over five consecutive trials. In each trial, a male was able to produce a nutritive gift (a live housefly) or a worthless gift (mealworm exuviae). We found that, in line with our predictions, 20% of the males produced worthless gifts even when they had the opportunity to produce a nutritive one. However, rather than worthless gifts being a cheap tactic, they were related to a higher investment in silk wrapping. This latter result was replicated for worthless gifts produced in both the presence and absence of a live prey item. We propose that variation in gift-giving tactics likely evolved initially as a conditional strategy related to prey availability and male condition in P. ornata. Selection may then have favoured silk wrapping as a trait involved in female attraction, leading worthless gift-giving to invade.

The handsome liar: Male spiders offering worthless gifts can benefit increasing mating duration

AbstractFemales of nuptial gift‐giving species are known to mate with several males, so that they secure multiple ejaculates and food via nuptial gifts. However, gifts may decrease females’ reproductive success, for instance, if they received non‐nutritive gifts (worthless). The gift‐giving mating system of the spider Paratrechalea ornata creates a scenario in which females may receive either a nutritive prey or a worthless inedible item wrapped in silk. The worthless gift tactic is expected to be less successful as females should prefer to mate and to mate for longer with males offering nutritive gifts. However, at the moment, the scarce information suggests that both mating tactics may have similar reproductive success. By exposing females to a double mating experimental design, we examined whether mating access and duration correlate with the gift type (nutritive‐worthless), mating order (first‐second), and male size, and additionally explored possible effects on female fitness (e.g., fecundity). We found that the females accepted to mate with courting males independently of gift type, mating order, or size. But, mating duration was positively correlated with male size, and longer when males offered worthless gifts. Furthermore, females’ fecundity increased with mating duration and female size. This demonstrated that males offering worthless gifts might enhance their reproductive success by transferring more sperm than those offering nutritive gifts. Thus, either due to female choice or male effort, male size might be a more relevant feature for reproductive success than gift type, which can explain the high frequencies of worthless gifts in the field.

Differential allocation in a gift-giving spider: males adjust their reproductive investment in response to female condition

BackgroundWhen males are selective, they can either reject low-quality females or adjust their reproductive investment in response to traits that indicate female quality (e.g., body size or condition). According to the differential allocation hypothesis, males increase their reproductive investment when paired with high-quality females (positive differential allocation) or increase their reproductive investment when paired with low-quality females (negative differential allocation). This hypothesis has been proposed for monogamous species with biparental care, and most empirical studies focus on birds. Here we used the polygamous spider Paratrechalea ornata, in which males offer prey wrapped in silk as nuptial gifts, to test whether males adjust their reproductive investment in gift size, pre-copulatory and copulatory courtship, and sperm transfer in response to female body condition.ResultsMales exposed to females in good body condition added more flies to the gift, stimulated these females longer with abdominal touches during pre-copulatory courtship, and had longer pedipalp insertions than males exposed to females in poor body condition. Female condition affected neither silk investment in nuptial gift wrapping nor the quantity of sperm transferred by males. Finally, females in good body condition oviposited faster after copulation and laid more eggs than females in poor body condition.ConclusionsWe provide experimental evidence that males of a gift-giving spider exhibit positive differential allocation in three key aspects of their reproductive investment: the size of the nutritious gift, duration of pre-copulatory courtship, and duration of pedipalp insertions, which is regarded as a form of copulatory courtship in spiders. This positive differential allocation is likely associated with the benefits of copulating with females in good body condition. These females are more fecund and oviposit faster after copulation than females in poor body condition, which under natural field conditions probably reduces the risk of multiple matings and thus the level of sperm competition faced by the males. As a final remark, our findings indicate that the hypothesis of differential allocation also applies to species with a scramble competition mating system, in which males heavily invest in nuptial gift construction, but not in parental care.

Males of a Neotropical spider adjust prey‐gift construction but not mate search in response to sperm competition

AbstractIn scramble competition mating systems, males do not guard females and females usually mate polyandrously, leading to high levels of sperm competition. Mathematical models predict that males facing sperm competition can either decrease or increase their reproductive effort. To test how male reproductive responses vary according to sperm competition risk, we ran two experiments using the polyandrous gift‐giving spiderParatrechalea ornata. First, we tested whether males prefer substrates containing silk of unmated females than substrates containing silk of once‐mated females, competitor males or without silk. Males spent more time on substrates containing silk of females but showed no preference for unmated females, which indicates that males may optimize mate search by prioritizing substrates containing cues of potential mating partners. The lack of preference for unmated females suggests that males cannot detect female mating status from silk or that the costs of searching preferentially for unmated females are high in the field. Second, we tested whether males adjust prey‐gift construction when facing sperm competition risk. Experimental groups (substrate containing silk of an unmated female and silk of another malevs. substrate containing only silk of an unmated female) did not differ in the frequency of gift construction, latency to gift construction and number of flies added to the gift. However, males facing sperm competition risk constructed gifts with less silk, suggesting the occurrence of a less evident form of male mate choice based on differential allocation of resources to prey‐gift. Additionally, given the trade‐off between investing in prey‐gifts quantity or quality, a lower silk investment should enable males to increase the number of gifts constructed and the number of courted females. Taken together, our results indicate that males detect female and male pheromones on substrate and adjust the construction of prey‐gifts in response to apparent sperm competition risk.

Characterization of four hypervariable microsatellite loci in a nuptial gift-giving spider and its prospect for paternity analyses

In the gift-giving spider Paratrechalea ornata, females mate multiple times and apparently may bias the paternity according to the nuptial gift content (nutritive or worthless). Paternity studies using microsatellite markers would, therefore, be ideal for studying male fertilization success for female offspring. We genotyped four microsatellites previously reported in one species of the genus using 43 individuals from four different localities in Uruguay. We describe the allelic and genotypic variation in all loci, and compare the findings to the reported variation for the genus. Except for one locus, all loci showed significant departure from the Hardy-Weinberg equilibrium due to heterozygote deficit. This could possibly be explained by the mixed nature of the sample and the effect of the population structure. These loci, and especially those that are highly hypervariable, are an important tool for paternity assessment and would allow a better understanding of the role of post-copulatory processes in P. ornata.

Female foraging impairment related to reproduction in a neotropical spider

Females not only produce costly gametes, but also store the eggs until laying them, a period called gravidity. The volume that eggs occupy in the female abdomen may decrease female foraging ability by making them slower. Although females of all species are subjected to these potential costs, it remains an unexplored matter in invertebrates. Females of the spider Paratrechalea ornata carry their egg sac after oviposition and thus represent a unique opportunity to evaluate gravidity costs because females carry an extra volume before and after laying eggs. We conducted foraging ability experiments using P. ornata females on different treatments regarding gravidity and maternal care. We first hypothesized that internal egg load and egg sac carrying decrease female foraging ability. We also hypothesized that greater egg sac size decreases female foraging ability. We found that both internal egg load and egg sac carrying decreased female foraging ability, and females about to oviposit had a similar foraging ability to females carrying an egg sac. Egg sac size did not influence female foraging ability. Our results show that females’ foraging ability changes before the maternal care period and therefore may influence their life-history evolution. The little support for our second hypothesis may also suggest that the decrease in foraging ability is not due to the volume being carried per se, but possibly an associated physiological state.

Females of a gift-giving spider do not trade sex for food gifts: a consequence of male deception?

BackgroundPolyandry 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.ResultsThough 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.ConclusionsIn 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.

Negative effects of prolonged dietary restriction on male mating effort: nuptial gifts as honest indicators of long-term male condition.

The handicap principle proposes that sexual signals must be costly to be honest. Honesty may be maintained by the costs paid by honest signallers or by the potential costs of cheating. In the latter, handicaps should emerge as a consequence of specific biological constraints, such as life-history trade-offs. Nuptial prey-giving arthropods are good systems to investigate the honesty of sexual signals taking into account trade-offs between self-maintenance and mating effort. We experimentally evaluated if prolonged food shortage during early adulthood imposes long-term negative effects on gift construction by males of the spider Paratrechalea ornata. We also evaluated whether a burst of food availability improved body condition of poorly fed males, increasing their frequency of gift construction. Poorly fed males hardly constructed gifts, even after a marked increase in feeding rate, which clearly improved their body condition. Moreover, initially poorly fed males that latter received high food intake constructed lighter gifts than continuously well fed males. The long-term effects of prolonged dietary restriction on male propensity to construct a gift and on the size of this gift may increase the honesty of this sexually selected signal. From the female’s perspective the offer of a gift may bring information on male quality.

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.

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.

Nuptial gift size, mating duration and remating success in a Neotropical spider

In many species the function and evolution of nuptial gifts have been explained by the male mating effort hypothesis; i.e., males increase their fertilization success by donating gifts to females. The gift size may determine copulation duration and consequently affects male fertilization rate. In the well-known spider Pisaura mirabilis, previous studies suggested that the brightness of the gift (a prey wrapped in silk) affects female acceptance and larger gifts promote longer matings, but little is known from other gift-giving spider species. In this paper we test if gift size affects mating and remating success in the Neotropical and semi-aquatic spider Paratrechalea ornata (Trechaleidae). We exposed virgin females to males offering one fly (OF group) or four flies (FF group) wrapped in silk, and afterwards mated females were exposed to remating. Males from FF showed both longer courtship and mating than males from OF. We found a positive linear relationship between insertion duration of male intromittent organs (during which sperm transfer occurs) and mating duration in both groups. Mated females were more reluctant to mate than virgin females, but contrary to our prediction, gift size and mating duration did not seem to influence remating success. Our findings show that large gifts prolong mating duration in P. ornata, supporting the mating effort hypothesis. Females would favour polyandry to gain direct benefits from the gifts, while males may improve success in sperm competition by inducing female reluctance for remating.

Reproductive interference between two sibling species of gift-giving spiders

We investigated the possibility of reproductive interference between two sibling spider species, Paratrechalea azul and Paratrechalea ornata , which occur syntopically and reproduce synchronously. Males of both species offer a nuptial gift composed of prey wrapped in silk to females. Through laboratory experiments, we evaluated possible asymmetries in the outcome of heterospecific encounters between males and females, and investigated whether chemical signalling could function as a premating barrier between the two species. Males of P. azul were unable to discriminate conspecific from heterospecific female draglines, which resulted in wasted time and energy in nuptial gift construction. Males of P. ornata incurred a higher cost for discrimination mistakes because most of them were attacked by heterospecific females; 95% lost the nuptial gift upon the attack and 33% were preyed upon. This pattern is probably a consequence of differences in body size between males and females of each species. Both species showed erroneous female choice, but only P. ornata females courted heterospecific males, which are considerably larger than conspecific males and may resemble high-quality mating partners. Males of P. ornata also made discrimination mistakes, but at a much lower frequency compared to P. azul males. The selective pressure for precise recognition of conspecific female signs is probably stronger on P. ornata males because misdirected courtship may increase their chances of encountering predatory heterospecific females. This study provides the first detailed evidence of reproductive interference between two reproductively isolated spider species, showing that the costs paid by individuals of different sexes and different species are highly asymmetric. ► We provide evidence of reproductive interference between two spider species. ► Males of both species offer a prey wrapped in silk as a nuptial gift to females. ► Nuptial gift construction and acceptance is induced by species-specific cues. ► Individuals of different sexes and different species pay highly asymmetric costs. ► Selective pressure for species recognition is stronger on the smaller species.

Sexual receptivity varies according to female age in a Neotropical nuptial gift-giving spider

Abstract For many spiders, sex pheromones associated with female silk are important stimuli that elicit male searching and courtship behaviors. In that context, female sexual receptivity and chemical attractiveness can depend on age and reproductive status. In Paratrechalea ornata (Mello-Leitao 1943) (Araneae: Trechaleidae), males offer females a nuptial gift (a prey wrapped in silk) during courtship. Gift construction is elicited by the presence of female silk, and silk attractiveness is influenced by female age, increasing from 20 days after the female reaches adulthood. Our goal was to investigate whether female age affects female sexual receptivity and to discuss the relationship between receptivity and silk attractiveness. We exposed 26 virgin females, from 2 to 28 days after the final molt, to males offering a nuptial gift. Female sexual receptivity was age dependent and increased with adult female age. Females over 15 days from adulthood accepted more gifts than younger females, but the latency of ...

It is a matter of taste: chemical signals mediate nuptial gift acceptance in a neotropical spider

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.

Sex chromosomes behavior and G‐banding treatment of male meiosis in nuptial gift‐giving spiders of the family Trechaleidae

Preliminary genetic studies in Trechaleidae spider family show high variation in sex chromosomes and high heterocigocity, suggesting high chromatin plasticity. The trechaleids Paratrechalea ornata, Trechalea bucculenta and Trechaleoides biocellata are present in Uruguay. Males offering nuptial gifts during courtship have been reported in P. ornata and T. bucculenta but not in T. biocellata. Nuptial gifts are an inherited trait probably highly affected by environmental factors, which play an important role in gene expression. We hypothesize that this trait could be associated with tissue-specific genes existing in G-bands. We investigate the male meiosis in these 3 species, their sex chromosome system and the effects of G-banding on their chromosomes, and elucidate genetic differences among them. Meiotic stages of the 3 species were submitted to Giemsa-staining and G-banding treatments. We observed a haploid number of n= 11 in P. ornata and n= 13 in both T. bucculenta and T. biocellata. Males from the 3 species presented an X(1) X(2) 0 sex chromosome system, which is suggested as ancestral in Araneae. In P. ornata and T. bucculenta, both sex chromosomes were together and aligned in parallel until the segregation during anaphase I. In contrast to these species, sex chromosomes of T. biocellata usually remained distant from each other until diakinesis when they were observed associated in parallel disposition. Interstitial G-bands were similar in P. ornata and T. bucculenta, and they both differed from those in T. biocellata. The special behavior of sex chromosomes in T. biocellata as well as the different G-banding pattern of this species suggests the existence of novel modifications in this species.

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

To feed or to wrap? Female silk cues elicit male nuptial gift construction in a semiaquatic trechaleid spider

AbstractBy 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.

Sexual dimorphism in chelicerae size in three species of nuptial‐gift spiders: a discussion of possible functions and driving selective forces

AbstractPositive allometric patterns observed for intersexual signalling characters are related to directional sexual selection, and supported by theoretical and empirical data. Recent models have shown that positive allometry may not hold as a rule if the influence of natural selection is added to the model. Here we tested these models applying traditional morphometrical techniques for the analysis of chelicerae sexual dimorphism and allometric patterns within the genus Paratrechalea: Paratrechalea azul, Paratrechalea galianoae and Paratrechalea ornata. Spider chelicerae are basically used for prey capture, but males of Paratrechalea also use the chelicerae to offer a nuptial gift during courtship, also presenting a clear size and colour sexual dimorphism supporting a possible role as a signal. Chelicerae size was male biased for all the variables studied and showed an isometric pattern, while females showed a higher variation. Our findings are in accordance with models of viability‐related function for prey capture, questioning some statements proposed by the positive allometry model.