Cristina Tuni

Silk wrapping of nuptial gifts aids cheating behaviour in male spiders

Sexual traits, such as nuptial gifts, are costly and often condition-dependent. Males should be under selection to reduce these costs without impairing their reproductive success. Spider gifts consist of silk-wrapped food, but may also consist of worthless (non-nutritive) donations that successfully lead to mating, despite yielding shorter copulations. Worthless gifts may either represent a cheaper cheating strategy or the inability to produce genuine gifts due to resource limitations (i.e. poor body condition). Unless energetic constraints limit expenditure in silk, males should apply more silk to worthless gifts to compensate for their lower reproductive value. We ask whether in Pisaura mirabilis 1) worthless gifts are condition-dependent and 2) males strategically use silk based on gift type (genuine vs worthless). We tested whether male body condition explains the gift-giving strategy and compared silk amounts covering each gift type, in gifts collected from the field and produced in the laboratory by males given different feeding regimes. Our findings show that worthless gifts are not promoted by poor body condition or limited resources. They rather result from a cheating strategy evolved to opportunistically reduce the costs of genuine gifts while ensuring nutritional advantages, with cheaters gaining body mass. Males applied more silk to worthless gifts regardless of their body condition or feeding state, suggesting they can strategically adjust silk expenditure despite its costs. By masking gift contents and prolonging female feeding, silk is crucial for the maintenance of cheating, likely resulting from an evolutionary arms race between male deception and female assessment.

Good reasons to leave home: proximate dispersal cues in a social spider

Natal dispersal is a successful tactic under a range of conditions in spite of significant costs. Habitat quality is a frequent proximate cause of dispersal, and studies have shown that dispersal increases both when natal habitat quality is good or poor. In social species kin competition, favouring dispersal may be balanced by the benefits of group living, favouring philopatry. We investigated the effect of changes in the local environment on natal dispersal of adult females in a social spider species, Stegodyphus dumicola (Araneae, Eresidae), with a flexible breeding system, where females can breed either within the colony or individually following dispersal. We manipulated foraging opportunities in colonies by either removing the capture webs or by adding prey and recorded the number of dispersing females around each focal colony, and their survival and reproductive success. We predicted that increasing kin competition should increase dispersal of less-competitive individuals, while reducing competition could cause either less dispersal (less competition) or more dispersal (a cue indicating better chances to establish a new colony). Dispersal occurred earlier and at a higher rate in both food-augmented and web-removal colonies than in control colonies. Fewer dispersing females survived and reproduced in the web-removal group than in the control or food-augmented groups. The results support our prediction that worsening conditions in web-removal colonies favour dispersal, whereby increased kin competition and increased energy expenditure on web renewal cause females to leave the natal colony. By contrast, prey augmentation may serve as a habitat-quality cue; when the surrounding habitat is expected to be of high quality, females assess the potential benefit of establishing a new colony to be greater than the costs of dispersal.

Paternal‐effects in a terrestrial ectotherm are temperature dependent but no evidence for adaptive effects

Global rising of average temperatures and increase in extreme climatic events may largely impact animal survival and reproduction. Yet, how variation in temperature may affect male fertility, in particular ejaculate traits, and whether this can in turn affect offspring fitness, is seldom addressed. Paternal effects may be of key importance as they could impact the rate and direction of evolutionary change in response to climate change. We tested the effects of temperature experienced by males on sperm traits, and asked whether the paternal environmental temperature affected offspring phenotype. We further explored the potential for paternal effects to be adaptive, which would occur when offspring fitness increased under the same environmental conditions experienced by the fathers. We exposed male field crickets to high or low temperatures at two life stages, either throughout development or as adults, and tested sperm traits (number and quality) and offspring fitness (hatching success and survival). We further assessed sperm traits in offspring, after they had also been exposed to the same or different temperature experienced by their father. We found that temperature affected sperm traits depending on the life-stage of individuals. When the exposure was given during adulthood, males exposed to high temperature produced less sperm and of lower quality compared to males exposed to lower temperature, while if exposure was given during development, males exposed to high temperature produced more sperm and of better quality compared to males exposed to low temperatures. Offspring fitness was significantly affected by paternal temperature, evidence for anticipatory paternal effects on sperm traits was not found. Our study indicates that temperature can mediate cross-generational effects, and that paternal effects may be mediated by changes in temperature and therefore much more widespread in nature than previously assumed.

Male spiders reduce pre- and postmating sexual investment in response to sperm competition risk

The interplay between pre- and postmating responses to intrasexual competition remains enigmatic. Sperm competition models often assume a trade-off between pre- and postmating traits that enhance mate acquisition and fertilization success, respectively. However, when males court females through food donations (i.e., nuptial gifts), pre- and postmating responses may be aligned, as nuptial gifts have the dual function of facilitating both mate acquisition and sperm transfer. In the spider Pisaura mirabilis, nuptial gifts consist of silk-wrapped prey. We tested whether males respond to a competitor by altering: 1) premating investment in the gift, 2) postmating sperm investment, and 3) whether pre- and postmating responses are coupled and respond to competition in the same direction or not. Under competition risk males silk-wrapped their gifts for significantly shorter time and transferred less sperm to females, pointing to a reduction of both pre- and postmating responses. Because silk is not a target of female choice, reducing gift construction may speed up mate acquisition. In accordance with models of sperm allocation, perceived high levels of competition and/or sperm priority patterns may explain the reduced patterns of sperm transfer found in our study. Overall, our findings suggest that in competitive environments pre- and postmating traits are coupled and respond in the same direction.

Multiple biological mechanisms result in correlations between pre- and post-mating traits that differ among versus within individuals and genotypes

Reproductive traits involved in mate acquisition (pre-mating traits) are predicted to covary with those involved in fertilization success (post-mating traits). Variation in male quality may give rise to positive, and resource allocation trade-offs to negative, covariances between pre- and post-mating traits. Empirical studies have yielded mixed results. Progress is hampered as researchers often fail to appreciate that mentioned biological mechanisms can act simultaneously but at different hierarchical levels of biological variation: genetic correlations may, for example, be negative due to genetic trade-offs but environmental correlations may instead be positive due to individual variation in resource acquisition. We measured pre-mating (aggression, body weight) and post-mating (ejaculate size) reproductive traits in a pedigreed population of southern field crickets (Gryllus bimaculatus). To create environmental variation, crickets were raised on either a low or a high nymphal density treatment. We estimated genetic and environmental sources of correlations between pre- and post-mating traits. We found positive genetic correlations between pre- and post-mating traits, implying the existence of genetic variation in male quality. Over repeated trials of the same individual (testing order), positive changes in one trait were matched with negative changes in other traits, suggesting energy allocating trade-offs within individuals among days. These findings demonstrate the need for research on pre- and post-mating traits to consider the hierarchical structure of trait correlations. Only by doing so was our study able to conclude that multiple mechanisms jointly shape phenotypic associations between pre- and post-mating traits in crickets.

Increased developmental density decreases the magnitude of indirect genetic effects expressed during agonistic interactions in an insect: DENSITY-DEPENDENT INDIRECT GENETIC EFFECTS

The expression of aggression depends not only on the direct genetic effects (DGEs) of an individuals genes on its own behavior, but also on indirect genetic effects (IGEs) caused by heritable phenotypes expressed by social partners. IGEs can affect the amount of heritable variance on which selection can act. Despite the important roles of IGEs in the evolutionary process, it remains largely unknown whether the strength of IGEs varies across life stages or competitive regimes. Based on manipulations of nymphal densities and > 3000 pair‐wise aggression tests across multiple life stages, we experimentally demonstrate that IGEs on aggression are stronger in field crickets (Gryllus bimaculatus) that develop at lower densities than in those that develop at higher densities, and that these effects persist with age. The existence of density‐dependent IGEs implies that social interactions strongly determine the plastic expression of aggression when competition for resources is relaxed. A more competitive (higher density) rearing environment may fail to provide crickets with sufficient resources to develop social cognition required for strong IGEs. The contribution of IGEs to evolutionary responses was greater at lower densities. Our study thereby demonstrates the importance of considering IGEs in density‐dependent ecological and evolutionary processes.

Does silk mediate chemical communication between the sexes in a nuptial feeding spider

Chemical signals play a crucial role in reproduction as a means for locating mates and/or gaining information about their quality, ultimately affecting mating system dynamics and mate choice. In spiders, one of the potential sources of chemical signalling is silk. However, while female silk is known to attract mates and/or elicit courtship, due to sex-specific roles in mate searching, male silk-related signals are often neglected. In the hunting spider Pisaura mirabilis (Pisauridae), both sexes leave silk draglines during movements while males additionally use silk to wrap nuptial gifts (food donations to females at mating). We explored the potential for both silk types (draglines and gift silk) to release signals and tested the hypothesis that chemical compounds bound to gifts’ silk serve to elicit female attraction. We conducted behavioural choice assays for dragline and gift silk, and their putative transmission mode (airborne or contact) by testing (i) male and female attraction towards draglines of the opposite sex and (ii) female attraction towards gift silk. Whereas males were attracted to female draglines (contact cues), females did not respond to male silk of any type. We suggest that females use draglines for advertisement to secure copulation and foraging of nuptial gifts. If these signals ease male mate searching, attractive male draglines are unnecessary. Overall, males may not invest in chemical stimulation but rather exploit female foraging interests through gift giving. Alternatively, they may release signals that prime other female sexual behaviours or towards which females may have evolved resistance.Significance statementAnimals commonly use chemical signals to communicate during reproduction, and spiders have the potential to release such signals from their silk. We investigated whether two silk types, draglines released during movements and silk covering male nuptial gifts (prey offered to females at mating) are attractive to the opposite sex in a hunting spider. While males were attracted to female draglines, females did not respond to male silk of any type. Females may be using silk to advertise themselves to secure matings and food through reception of nuptial gifts. If males can successfully locate females, attracting females through draglines may be unnecessary. The finding that males do not release attractant signals in the silk cover of their nuptial gifts further suggests that rather than attempting to increase their attractiveness by using chemical stimulation, males may be uniquely exploiting females’ interest in food through gift giving behaviour.