Risky mate search and male self-sacrifice in redback spiders

Male redback spiders twist their abdomens onto the fangs of their mates during copulation and, if cannibalized (65% of matings), increase their paternity relative to males that are not cannibalized. The adaptive male sacrifice hypothesis proposes that this increased reproductive payoff from a single mating outweighs the residual reproductive value of a cannibalized male, because high mortality during mate searching restricts alternative mating opportunities. It has been reported that redback male residual reproductive value is low because males are functionally sterile after one mating--a putative intrinsic constraint that could arguably favor self-sacrifice in the absence of ecological restrictions on multiple mating. However, sterility and self-sacrifice may both arise as aspects of a terminal investment strategy if the probability of multiple mating is sufficiently low. Here I report field data that support the adaptive male sacrifice hypothesis. More than 80% of redback males die without finding a potential mate in nature. Data from two observational field studies and one release experiment suggest that in the absence of cannibalism, male redbacks would expect fewer than one mating opportunity in a lifetime. This expectation was not significantly higher for a large male or one in good condition. A simple quantitative analysis confirms that even if males are assumed to be fertile throughout life, the measured mortality rate during mate search in combination with previously documented paternity benefits of cannibalism is sufficient to ensure that self-sacrifice is adaptive for male redback spiders. Copyright 2003.constraint; Latrodectus; mate searching; redback; self-sacrifice; sexual cannibalism; spider

Does female control and male mating system predict courtship investment and mating outcomes? A comparative study in five widow spider species (genus Latrodectus) tested under similar laboratory conditions

Abstract Background Male courtship investment may evolve in response to the male’s expectation of future mating opportunities or the degree of female control during mating interactions. We used a comparative approach to test this hypotheses by assessing the courtship and mating behaviors of five widow spider species (genus Latrodectus) under common laboratory conditions. We predicted male investment in courtship would be higher in species where males mate only once because of high cannibalism rates (monogyny, L. geometricus, L. hasselti, L. mirabilis), compared to species with rare cannibalism (L. mactans, L. hesperus) in which males should reserve energy for future mating opportunities. Increased male investment, measured as courtship duration, might also evolve with increased female control over mating outcomes if females prefer longer courtships. We tested this by assessing the frequency of copulations, timing of sexual cannibalism, and the degree of female-biased size dimorphism, which is expected to be negatively correlated with the energetic cost of rebuffing male mating attempts. Results Copulation frequency was consistently lower in species with extreme female-skewed size dimorphism, and where sexual cannibalism was more prevalent, suggesting the importance of female control for mating outcomes. We confirmed significant interspecific variation in average courtship duration, but contrary to predictions, it was not predicted by male mating system, and there was no consistent link between courtship duration and sexual size dimorphism. Conclusion We show that the degree of sexual dimorphism is not only correlated with sexual cannibalism, but also with mating success since restriction of male copulation frequency by female Latrodectus affects paternity. However, predictions about male mating system or female control affecting courtship duration were not supported. We propose that the form of female control over mating and cannibalism, and male responses, might be more informative for understanding the evolution of courtship duration. For example, male tactics to avoid female aggression may drive lower courtship duration in species like L. mirabilis. Nonetheless, our results differ from inferences based on published studies of each species in isolation, illuminating the need for standardized data collection for behavioural comparative studies

Neutral fitness outcomes contradict inferences of sexual ‘coercion’ derived from male’s damaging mating tactic in a widow spider

Abstract Sexual conflict over mating frequency has driven the evolution of morphological and behavioural traits across taxa. Interactions may be termed ‘coercive’ and assumed to arise from conflict when male mating behaviours cause physical injury to females and females appear to resist injurious matings.However, coercion per se occurs only if the behaviour reduces female fitness; and such outcomes are rarely measured. Here we show that a damaging mating tactic, apparently adaptive for males, is not coercive for females. Adult male Latrodectus spiders mate with immature females after tearing the exoskeleton covering the female’s recently-developed reproductive tract, which can cause haemolymph bleeding. We show that, relative to pairings with adult females, males use reduced courtship displays when approaching immature females, which in some cases respond with elevated deterrent behavioural responses. Nevertheless, we found no reproductive cost for immature-mated females in terms of longevity, fertility or fecundity. Moreover, most immature-mated females did not produce sex pheromones as adults, so did not seek additional matings. Thus, despite the appearance of conflict there is no evidence that immature-mating is coercive. These results show it is critical to measure fitness outcomes, in addition to behavioural responses, to test for coercion

Data from: Neutral fitness outcomes contradict inferences of sexual ‘coercion’ derived from male’s damaging mating tactic in a widow spider

Sexual conflict over mating frequency has driven the evolution of morphological and behavioural traits across taxa. Interactions may be termed ‘coercive’ and assumed to arise from conflict when male mating behaviours cause physical injury to females and females appear to resist injurious matings.However, coercion per se occurs only if the behaviour reduces female fitness; and such outcomes are rarely measured. Here we show that a damaging mating tactic, apparently adaptive for males, is not coercive for females. Adult male Latrodectus spiders mate with immature females after tearing the exoskeleton covering the female’s recently-developed reproductive tract, which can cause haemolymph bleeding. We show that, relative to pairings with adult females, males use reduced courtship displays when approaching immature females, which in some cases respond with elevated deterrent behavioural responses. Nevertheless, we found no reproductive cost for immature-mated females in terms of longevity, fertility or fecundity. Moreover, most immature-mated females did not produce sex pheromones as adults, so did not seek additional matings. Thus, despite the appearance of conflict there is no evidence that immature-mating is coercive. These results show it is critical to measure fitness outcomes, in addition to behavioural responses, to test for coercion

Data from: Copulation with immature females increases male fitness in cannibalistic widow spiders

Copulatory cannibalism of male ‘widow’ spiders (genus Latrodectus) is a model example of the extreme effects of sexual selection, particularly in L. hasselti and L. geometricus where males typically facilitate cannibalism by females and mate only once. We show that these males can increase their reproductive success by copulating with final-instar, immature females after piercing the female's exoskeleton to access her newly developed sperm storage organs. Females retain sperm through their final moult and have similar fecundity to adult-mated females. This is an adaptive male tactic because immature mating increases insemination success relative to adult mating (which predicts higher paternity) and moreover, rarely ends in cannibalism, so males can mate again. Although successful only during a brief period before the female's final moult, males may employ this tactic when they associate with final-instar females in nature. Consistent with this, one-third of L. hasselti females collected as immatures in nature were already mated. Immature mating alters sexual selection on these otherwise monogynous males, and may explain male traits allowing facultative polygyny in Latrodectus. Since male cohabitation with immature females is common among invertebrates, immature mating may be a widespread, previously unrecognized mating tactic, particularly when unmated females are of high reproductive value

Pattern of sperm transfer in redback spiders: implications for sperm competition and male sacrifice

Many sperm competition studies have identified copulation duration as an important predictor of paternity. This result is often interpreted as a sperm transfer effect--it is assumed that sperm transfer is limited by copulation duration. Here we test the assumption of duration-dependent sperm transfer in the Australian redback spider, Latrodectus hasselti, in which a correlation between copulation duration and paternity has been implicated in the evolution of a rare male self-sacrifice behavior. Male redbacks facilitate sexual cannibalism by females during copulation. Sexual cannibalism is apparently adaptive for redback males, in part because it results in longer copulations (25 versus 11 min.), and copulation duration is positively correlated with paternity. We assessed sperm transfer in normal copulations and in copulations that we terminated at 5, 10, or 20 min. Our results show that the paternity advantage of sexual cannibalism is not owing to time-dependent sperm transfer, as redback males transfer the majority of their sperm within the first 5 min of copulation. This suggests that the link between copulation duration and paternity may instead be owing to cryptic female choice or the transfer of nongametic ejaculatory substances. Results further indicate that the act of cannibalism itself might play a role in mediating sperm transfer. This study highlights the importance of understanding mechanisms of sperm transfer when attempting to interpret the outcome of sperm competition studies. Copyright 2004.copulation duration; Latrodectus hasselti; redback spider; sexual cannibalism; sperm competition; sperm transfer

Subtle pedipalp dimorphism: a reliable method for sexing juvenile spiders

Volume: 36Start Page: 513End Page: 51

Juvenile Experience with Male Cues Triggers Cryptic Choice Mechanisms in Adult Female Redback Spiders

Female choice may be linked to population density if the expected encounter rates with potential mates affects choosiness (the energy and risk engaged to express mate preferences). Choosiness should covary with male availability, which could be assessed using the social cues available during development. We tested whether the exposure of juvenile females to cues of male density affected the mechanisms of choosiness of adult Latrodectus hasselti spiders in two experiments simulating natural contexts. The juvenile females were exposed to (1) volatile chemicals from two densities of adult males (airborne cues), and (2) tactile, vibrational and chemical cues from adult males or other females (cohabitation cues). As adults, the females mated readily, regardless of the treatment, but there was strong evidence for post-copulatory mechanisms of choosiness in females exposed to cues of high male availability. These included abbreviated matings (in both experiments), cannibalism of the males before the mating was complete (cohabitation), and, remarkably, a reduction in the successful placement of internal sperm plugs (cohabitation). These shifts decrease the likelihood that the first mate would monopolize paternity if the female chose to mate again. We conclude that female choosiness may impose a strong selection on males despite the high mating rates, and these effects can hinge on the cues of male availability detected by juveniles