Heatwaves inflict reproductive but not survival costs to male insects.

Climate change is having a dramatic effect on the environment, with rising global temperatures and more frequent extreme climatic events, such as heatwaves, that can hamper organisms' biological functions. Although it is clear that sudden and extreme temperatures can damage reproductive processes, there is limited understanding of the effects of heatwaves on male mating behaviour and reproductive success. We tested for the effects of heat stress induced by ecologically relevant heatwaves (33°C and 39°C for five consecutive days) on the mating behaviour, reproductive success, body mass and survival of male field crickets Gryllus bimaculatus, paired with untreated females. We predicted life-history and reproductive costs would increase with increasing heatwave intensity. Consistent with our expectations, males exposed to the highest heatwave temperature produced the fewest offspring, while having to increase courtship effort to successfully mate. Males also gained relatively more weight following heatwave exposure. Given that we found no difference in lifetime survival, our results suggest a potential trade-off in resource allocation between somatic maintenance and reproductive investment. Taken together, our findings indicate that sublethal effects of heatwaves could reduce the growth and persistence of animal populations by negatively impacting reproductive rates. These findings highlight the need for considering thermal ecologies, life history and behaviour to better understand the consequences of extreme climatic events on individuals and populations.

Pre- and post-copulatory sexual selection increase offspring quality but impose survival costs to female field crickets.

Whether sexual selection increases or decreases fitness is under ongoing debate. Sexual selection operates before and after mating. Yet, the effects of each episode of selection on individual reproductive success remain largely unexplored. We ask how disentangled pre- and post-copulatory sexual selection contribute to fitness of field crickets Gryllus bimaculatus. Treatments allowed exclusively for (i) pre-copulatory selection, with males fighting and courting one female, and the resulting pair breeding monogamously, (ii) post-copulatory selection, with females mating consecutively to multiple males and (iii) relaxed selection, with enforced pair monogamy. While standardizing the number of matings, we estimated a number of fitness traits across treatments and show that females experiencing sexual selection were more likely to reproduce, their offspring hatched sooner, developed faster and had higher body mass at adulthood, but females suffered survival costs. Interestingly, we found no differences in fitness of females or their offspring from pre- and post-copulatory sexual selection treatments. Our findings highlight the potential for sexual selection in enhancing indirect female fitness while concurrently imposing direct survival costs. By potentially outweighing these costs, increased offspring quality could lead to beneficial population-level consequences of sexual selection.

Sex roles and sex ratios in animals.

In species with separate sexes, females and males often differ in their morphology, physiology and behaviour. Such sex-specific traits are functionally linked to variation in reproductive competition, mate choice and parental care, which have all been linked to sex roles. At the 150th anniversary of Darwin's theory on sexual selection, the question of why patterns of sex roles vary within and across species remains a key topic in behavioural and evolutionary ecology. New theoretical, experimental and comparative evidence suggests that variation in the adult sex ratio (ASR) is a key driver of variation in sex roles. Here, we first define and discuss the historical emergence of the sex role concept, including recent criticisms and rebuttals. Second, we review the various sex ratios with a focus on ASR, and explore its theoretical links to sex roles. Third, we explore the causes, and especially the consequences, of biased ASRs, focusing on the results of correlational and experimental studies of the effect of ASR variation on mate choice, sexual conflict, parental care and mating systems, social behaviour, hormone physiology and fitness. We present evidence that animals in diverse societies are sensitive to variation in local ASR, even on short timescales, and propose explanations for conflicting results. We conclude with an overview of open questions in this field integrating demography, life history and behaviour.

Sperm competition intensity affects sperm precedence patterns in a polyandrous gift-giving spider.

Sperm competition drives traits that enhance fertilization success. The amount of sperm transferred relative to competitors is key for attaining paternity. Female reproductive morphology and male mating order may also influence fertilization, however the outcome for sperm precedence under intense sperm competition remains poorly understood. In the polyandrous spider Pisaura mirabilis, males offer nuptial gifts which prolong copulation and increase sperm transfer, factors proposed to alter sperm precedence patterns under strong sperm competition. First, we assessed the degree of female polyandry by genotyping wild broods. A conservative analysis identified up to four sires, with a mean of two sires per brood, consistent with an optimal mating female rate. Then we asked whether intense sperm competition shifts sperm precedence patterns from first male priority, as expected from female morphology, to last male advantage. We varied sexual selection intensity experimentally and determined competitive fertilization outcome by genotyping broods. In double matings, one male monopolised paternity regardless of mating order. A mating order effect with first male priority was revealed when females were mated to four males, however this effect disappeared when females were mated to six males, probably due to increased sperm mixing. The proportion of males that successfully sired offspring drastically decreased with the number of competitors. Longer copulations translated into higher paternity shares independently of mating order, reinforcing the advantage of traits that prolong copulation duration under intense competition, such as the nuptial gift. Sperm competition intensity enhances the impact of competitive sexual traits and imposes multiple effects on paternity.

Female mating rates and their fitness consequences in the common house spider Parasteatoda tepidariorum.

Mating systems, with varying female mating rates occurring with the same partner (monandry) or with multiple mates (polyandry), can have far reaching consequences for population viability and the rate of gene flow. Here, we investigate the mating rates of the common house spider Parasteatoda tepidariorum (Theridiidae), an emerging model for genetic studies, with yet undescribed reproductive behavior. It is hypothesized that spiders belonging to this family have low re-mating rates. We paired females twice with the same male (monandry) or with different males (polyandry), and recorded behaviors, mating success and fitness resulting from single- and double-matings, either monandrous or polyandrous. Despite the study being explorative in nature, we predict successful matings to be more frequent during first encounters, to reduce female risk of remaining unmated. For re-mating to be adaptive, we expect higher fitness of double-mated females, and polyandrous females to experience highest mating success and fitness if reproductive gains are achieved by mating with multiple partners. We show that the majority of the females did not mate, and those that did mated only once, not necessarily on their first encounter. The likelihood of re-mating did not differ between monandrous and polyandrous encounters and female mating experience (mated once, twice monandrous, twice polyandrous) did not affect fitness, indicated by similar offspring production. Female twanging of the web leads to successful matings suggesting female behavioral receptivity. Cannibalism rates were low and mostly occurred pre-copulatory. We discuss how the species ecology, with potentially high mating costs for males and limited female receptivity, may shape a mating system with low mating rates.

Silk-borne chemicals of spider nuptial gifts elicit female gift acceptance.

Chemical communication is important in a reproductive context for conveying information used for mate recognition and/or assessment during courtship and mating. Spider silk is a common vehicle for chemical communication between the sexes. However, despite being well described in females, male silk-borne chemicals remain largely unexplored. Males of the spider Pisaura mirabilis silk-wrap prey (i.e. nuptial gifts) that is offered to females during courtship and eaten by the female during mating. Interestingly, rejected males often add more silk to their gift which leads to successful mating, suggesting the presence of silk-borne chemicals that facilitate female gift acceptance. To test this hypothesis, we offered females standardized gifts covered with male silk that was either washed in solvents or unwashed, respectively, to remove or not any chemically active components. We scored female gift acceptance, and as expected in the case chemicals that mediate female mating behaviour are present in male silk, females were more likely to accept gifts covered with unwashed silk. Our findings suggest that silk-borne chemicals of nuptial gifts prime female responses, potentially signalling male quality or manipulating females into mating beyond their interests given the occurrence of male cheating behaviour via nutritionally worthless gifts in this system.

Food Limitation but Not Enhanced Rates of Ejaculate Production Imposes Reproductive and Survival Costs to Male Crickets.

Estimating costs of ejaculate production is challenging. Metabolic investment in ejaculates may come at the expense of other physiological functions and may negatively affect future reproduction and/or survival. These trade-offs are especially likely to occur under constrained resource pools (e.g., poor nutrition). Here, we investigated costs of ejaculate production via trade-offs in the field cricket Gryllus bimaculatus. We experimentally increased rates of ejaculate production, while keeping an unmanipulated group, in adult males kept at high and low feeding regimes and tested the effects of our treatments on (i) somatic maintenance (i.e., changes in male body mass), (ii) future reproduction (i.e., the likelihood of producing a spermatophore and the viability of its sperm), and (iii) lifetime survival and longevity. We predicted investment in ejaculates to impinge upon all measured responses, especially in low-fed individuals. Instead, we only found negative effects of food limitation, suggesting low or undetectable costs of spermatophore production. High mating rates may select for males to maximize their capacity of ejaculate production, making ejaculate traits less prone to trade-offs with other fitness-related life history traits. Nevertheless, males were impaired due to nutrient deficiency in producing viable ejaculates, suggesting condition-dependent costs for ejaculate production.

Sperm competition when transfer is dangerous.

Aggressive and cannibalistic female spiders can impose strong selection on male mating and fertilization strategies. Furthermore, the distinctive reproductive morphology of spiders is predicted to influence the outcome of sperm competition. Polyandry is common in spiders, leading to defensive male strategies that include guarding, plugging and self-sacrifice. Paternity patterns are highly variable and unlikely to be determined solely by mating order, but rather by relative copulation duration, deployment of plugs and cryptic female choice. The ability to strategically allocate sperm is limited, either by the need to refill pedipalps periodically or owing to permanent sperm depletion after mating. Further insights now rely on unravelling several proximate mechanisms such as the process of sperm activation and the role of seminal fluids. This article is part of the theme issue 'Fifty years of sperm competition'.

Reduced light avoidance in spiders from populations in light-polluted urban environments.

Increased urbanisation is leading to a rise in light pollution. Light pollution can disrupt the behaviour and physiology of animals resulting in increased mortality. However, animals may also benefit from artificial light sources, as these may aggregate prey or signal suitable environments. For example, spiders are commonly seen congregating around artificial light sources. Changes in selective pressures engendered by urban environments are driving changes in urban organisms, driving better adaptation to these environments. Here, we ask whether urban populations of the synanthropic spider Steatoda triangulosa show different responses to light compared to rural populations. Egg-sacs from urban and rural populations were collected and incubated in a common garden setting, and the emerging spiderlings tested for light preference. While rural spiderlings avoided light (37% built webs in the light), urban spiderlings were indifferent to it (49% built webs in the light). Reduced light avoidance may benefit spiders through increased prey capture, increased movement into suitable habitats, or due to a release from selection pressure from visually hunting predators which do not enter buildings.

Increased developmental density decreases the magnitude of indirect genetic effects expressed during agonistic interactions in an insect.

The expression of aggression depends not only on the direct genetic effects (DGEs) of an individual's 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.

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.

Resource availability, mating opportunity and sexual selection intensity influence the expression of male alternative reproductive tactics.

The expression of alternative reproductive tactics can be plastic and occur simultaneously depending on cues that vary spatially or temporally. For example, variation in resources and sexual selection intensity is expected to influence the pay-off of each tactic and shape the decision of which tactic to employ. Males of the nuptial gift-giving spider Pisaura mirabilis can adopt three tactics: offering a genuine prey gift, a 'worthless' non-nutritious gift or no gift. We hypothesized that resources and/or male body condition, and mating opportunity and sexual selection intensity, vary over the course of the mating season to shape the co-existence of alternative traits. We measured these variables in the field over two seasons, to investigate the predictions that as the mating season progresses, (i) males become more likely to employ a gift-giving tactic, and (ii) the likelihood of switching from worthless to genuine gifts increases. Prey availability increased over the season and co-varied with the propensity of males to employ the gift-giving tactic, but we found no support for condition-dependent gift giving. Males responded to an increase in female availability by increasing their mating effort (gift production). Furthermore, the frequency of genuine gift use increased with sexual selection intensity, consistent with the assumption that sperm competition intensity increases with time. Our results suggest that the frequency of alternative tactics is shaped by seasonal changes in ecological factors and sexual selection. This leads to relaxed selection for the gift-giving tactic early in the season when females are less choosy and resources more scarce, and increased selection for genuine gifts later in the season driven by mating opportunity and risk of sperm competition.

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.

Evidence for loss of nepotism in the evolution of permanent sociality.

Kin selected benefits of cooperation result in pronounced kin discrimination and nepotism in many social species and favour the evolution of sociality. However, low variability in relatedness among group members, infrequent competitive interactions with non-relatives, and direct benefits of cooperation may relax selection for nepotism. We tested this prediction in a permanently social spider, Stegodyphus dumicola that appears to fulfil these conditions. Sociality is a derived trait, and kin discrimination exists in sub-social closely related congeners and is likely a selective force in the sub-social route to permanent sociality in spiders. We examined whether social spiders show nepotism in cooperative feeding when genetic relatedness among group members was experimentally varied. We found no effect of relatedness on feeding efficiency, growth rate or participation in feeding events. Previous studies on sub-social species showed benefits of communal feeding with kin, indicating nepotistic cooperation. The lack of evidence for nepotism in the social species suggests that kin discrimination has been lost or is irrelevant in communal feeding. Our results are consistent with the hypothesis that the role of nepotism is diminished when cooperation evolves in certain genetic and ecological contexts, e.g. when intra-group genetic relatedness is homogeneous and encounters with competitors are rare.

Fitness consequences of outcrossing in a social spider with an inbreeding mating system.

Inbreeding mating systems are uncommon because of inbreeding depression. Mating among close relatives can evolve, however, when outcrossing is constrained. Social spiders show obligatory mating among siblings. In combination with a female-biased sex ratio, sib-mating results in small effective populations. In such a system, high genetic homozygosity is expected, and drift may cause population divergence. We tested the effect of outcrossing in the social spider Stegodyphus dumicola. Females were mated to sib-males, to a non-nestmate within the population, or to a male from a distant population, and fitness traits of F1s were compared. We found reduced hatching success of broods from between-population crosses, suggesting the presence of population divergence at a large geographical scale that may result in population incompatibility. However, a lack of a difference in offspring performance between inbred and outbred crosses indicates little genetic variation between populations, and could suggest recent colonization by a common ancestor. This is consistent with population dynamics of frequent colonizations by single sib-mated females of common origin, and extinctions of populations after few generations. Although drift or single mutations can lead to population divergence at a relatively short time scale, it is possible that dynamic population processes homogenize these effects at longer time scales.

Moderate multiple parentage and low genetic variation reduces the potential for genetic incompatibility avoidance despite high risk of inbreeding.

BACKGROUND: Polyandry is widespread throughout the animal kingdom. In the absence of direct benefits of mating with different males, the underlying basis for polyandry is enigmatic because it can carry considerable costs such as elevated exposure to sexual diseases, physical injury or other direct fitness costs. Such costs may be balanced by indirect genetic benefits to the offspring of polyandrous females. We investigated polyandry and patterns of parentage in the spider Stegodyphus lineatus. This species experiences relatively high levels of inbreeding as a result of its spatial population structure, philopatry and limited male mating dispersal. Polyandry may provide an opportunity for post mating inbreeding avoidance that reduces the risk of genetic incompatibilities arising from incestuous matings. However, multiple mating carries direct fitness costs to females suggesting that genetic benefits must be substantial to counter direct costs. METHODOLOGY/PRINCIPAL FINDINGS: Genetic parentage analyses in two populations from Israel and a Greek island, showed mixed-brood parentage in approximately 50% of the broods. The number of fathers ranged from 1-2 indicating low levels of multiple parentage and there was no evidence for paternity bias in mixed-broods from both populations. Microsatellite loci variation suggested limited genetic variation within populations, especially in the Greek island population. Relatedness estimates among females in the maternal generation and potentially interacting individuals were substantial indicating full-sib and half-sib relationships. CONCLUSIONS/SIGNIFICANCE: Three lines of evidence indicate limited potential to obtain substantial genetic benefits in the form of reduced inbreeding. The relatively low frequency of multiple parentage together with low genetic variation among potential mates and the elevated risk of mating among related individuals as corroborated by our genetic data suggest that there are limited actual outbreeding opportunities for polyandrous females. Polyandry in S. lineatus is thus unlikely to be maintained through adaptive female choice.

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.

Death feigning in the face of sexual cannibalism.

Pre-copulatory sexual cannibalism by females affects male and female reproductive success in profoundly different ways, with the females benefiting from a meal and the male facing the risk of not reproducing at all. This sexual conflict predicts evolution of traits to avoid cannibalism and ensure male reproductive success. We show that males of the nuptial gift-giving spider Pisaura mirabilis display a remarkable death feigning behaviour--thanatosis--as part of the courtship prior to mating with potentially cannibalistic females. Thanatosis is a widespread anti-predator strategy; however, it is exceptional in the context of sexual selection. When the female approached a gift-displaying male, she usually showed interest in the gift but would sometimes attack the male, and at this potentially dangerous moment the male could 'drop dead'. When entering thanatosis, the male would collapse and remain completely motionless while retaining hold of the gift so it was held simultaneously by both mates. When the female initiated consumption of the gift, the male cautiously 'came to life' and initiated copulation. Death feigning males were more successful in gaining copulations, but did not have prolonged copulations. We propose that death feigning evolved as an adaptive male mating strategy in conjunction with nuptial gift giving under the risk of being victimized by females.