Stressful environments favor deceptive alternative mating tactics to become dominant.

BACKGROUND: Deceptive 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. RESULTS: We 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. CONCLUSIONS: Overall, 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.

Linear Peptides-A Combinatorial Innovation in the Venom of Some Modern Spiders.

In the venom of spiders, linear peptides (LPs), also called cytolytical or antimicrobial peptides, represent a largely neglected group of mostly membrane active substances that contribute in some spider species considerably to the killing power of spider venom. By next-generation sequencing venom gland transcriptome analysis, we investigated 48 spider species from 23 spider families and detected LPs in 20 species, belonging to five spider families (Ctenidae, Lycosidae, Oxyopidae, Pisauridae, and Zodariidae). The structural diversity is extraordinary high in some species: the lynx spider Oxyopes heterophthalmus contains 62 and the lycosid Pardosa palustris 60 different LPs. In total, we identified 524 linear peptide structures and some of them are in lycosids identical on amino acid level. LPs are mainly encoded in complex precursor structures in which, after the signal peptide and propeptide, 13 or more LPs (Hogna radiata) are connected by linkers. Besides Cupiennius species, also in Oxyopidae, posttranslational modifications of some precursor structures result in the formation of two-chain peptides. It is obvious that complex precursor structures represent a very suitable and fast method to produce a high number and a high diversity of bioactive LPs as economically as possible. At least in Lycosidae, Oxyopidae, and in the genus Cupiennius, LPs reach very high Transcripts Per Kilobase Million values, indicating functional importance within the envenomation process.

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

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.

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.

Worthless and Nutritive Nuptial Gifts: Mating Duration, Sperm Stored and Potential Female Decisions in Spiders.

In nuptial gift-giving species females sometimes select their potential mates based on the presence and size of the gift. But in some species, such as the Neotropical polyandrous spider Paratrechalea ornate male gifts vary in quality, from nutritive to worthless, and this male strategy can be in conflict with female nutritional benefits. In this species, males without gifts experience a reduction in mating success and duration, while males that offer worthless or genuine nutritive gifts mate with similar frequencies and durations. The female apparently controls the duration of copulation. Thus, there is scope for females to favour males offering gifts and further if these are nutritious, via post-copulatory processes. We first tested whether females differentially store sperm from males that offer the highest nutritional benefits by experimentally presenting females with males that offer either nutritive or worthless gifts (uninterrupted matings). Second, we carried out another set of experiments to examine whether females can select sperm based only on gift presence. This time we interrupted matings after the first pedipalp insertion, thus matching number of insertions and mating duration for males that: offered and did not offer gift. Our results showed that the amount of sperm stored is positive related to mating duration in all groups, except in matings with worthless gifts. Gift presence itself did not affect the sperm stored by females, while they store similar number of sperm in matings with males offering either nutritive or worthless gifts. We discuss whether females prefer males with gifts regardless, if content, because it represents an attractive and/or reliable signal. Or alternatively, they prefer nutritive nuptial gifts, as they are an important source of food supply and/or signal of male donor ability.

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.

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.

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

BACKGROUND: 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). RESULTS: 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. CONCLUSION: 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.

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.