Neuman & Schneider

Animal Behaviour 159 (2020) 59e67 Contents lists available at ScienceDirect Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav Males sacrifice their legs to pacify aggressive females in a sexually cannibalistic spider * Rainer Neumann, Jutta M. Schneider Institute of Zoology, Universitat€ Hamburg, Hamburg, Germany article info Monogynous male mating strategies have repeatedly evolved in spiders along with female-biased sexual fl Article history: size dimorphism (SSD) and extreme male mating investment. As a manifestation of sexual con ict, male Received 15 April 2019 African golden-silk spiders, Trichonephila fenestrata, are regularly attacked by females during copulation, Initial acceptance 16 July 2019 and sexual cannibalism is common. Curiously, attacked males actively cast off (autotomize) their front Final acceptance 9 October 2019 legs and copulation continues while the female is feeding on these legs. Since the loss of legs is costly in Available online 5 December 2019 reducing males’ ability to mate guard, it should yield significant benefits. In a series of experiments, we MS number 19-00268R investigated the behavioural mechanism of male leg ejection and tested three hypotheses. First, we performed feeding experiments to test whether conspecific male legs are particularly attractive for fe- Keywords: males and act as a sensory trap. Second, we conducted mating experiments with sibling and nonsibling Araneae pairings to test whether males preferentially invest in high-quality mates. Third, by offering male legs autotomy during copulations, we tested whether male leg ejection serves to distract and pacify females. In support male mating tactic fi fi fi mating system of the female paci er hypothesis, our results con rm a signi cantly reduced probability of attacks in monogyny females that had been offered a male leg, but we found no relationship between simulated leg ejection Nephilidae and male survival. While there was no evidence for special properties of male legs, females accepted polyandry male legs significantly more often than insect food. The degree of male leg sacrifice did not depend on sexual conflict maleefemale relatedness, but large males lost more legs than small males, and small males achieved sexual size dimorphism more copulations. However, total copulation duration was unrelated to male size. Male leg sacrifice in Trichonephila T. fenestrata may represent a rare example of an evolutionary transition in which the antipredation behaviour of autotomizing body parts has changed its function into a sexual context, here to pacify females and to facilitate undisturbed copulations. © 2019 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Monogynous mating systems are characterized by males that spark an antagonistic coevolution of female resistance and male invest maximally in paternity with a single female without persistence (Arnqvist & Rowe, 2005; Rice, 1996). providing paternal care (Fromhage, Elgar, & Schneider, 2005). The Monogynous mating systems occur in diverse taxa and have maximum reproductive success a monogynous male can achieve is evolved several times independently in spiders along with extreme to sire all offspring of a single female. The male's prospects of reversed sexual size dimorphism (SSD). The tiny males mate with gaining exclusive paternity will depend on his ability to find a only one or very few females and possess special traits to monop- virgin female and to defend her against rivals. However, monopo- olize paternity with a single female (Miller, 2007; Schneider & lization by a single male may not coincide with female interests. Fromhage, 2010). One such trait is the plugging of female genital Indeed, many studies have shown that females benefit from poly- openings with parts of the male copulatory organs. These chitinous andry by gaining direct and indirect fitness benefits (Arnqvist & plugs are broken-off fragments of the sperm-transferring struc- Nilsson, 2000; Slatyer, Mautz, Backwell, & Jennions, 2012). It is tures; hence mate plugging will usually render the copulatory or- also well established that sexual conflicts over mating rate can gan dysfunctional after mating (Fromhage & Schneider, 2006). Such ‘one-shot genitalia’ occur in various spider families, including the Nephilidae (Kuntner, Agnarsson, & Li, 2015). A typical female behaviour in monogynous spider species is the killing and consuming of males during or after copulation. The € * Correspondence: J. M. Schneider, Institute of Zoology, Universitat Hamburg, question why females kill their mates has been debated since Martin-Luther-King Platz 3, 20146, Hamburg, Germany. Darwin (Darwin, 1871; Elgar, 1992) and sexual cannibalism has E-mail address: [email protected] (J. M. Schneider). https://doi.org/10.1016/j.anbehav.2019.11.003 0003-3472/© 2019 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. 60 R. Neumann, J. M. Schneider / Animal Behaviour 159 (2020) 59e67 been called the pinnacle of sexual conflict (Elgar & Schneider, Thompson, Levine, & Wrinn, 2017; Wrinn & Uetz, 2008). Previous 2004); however, whether or not cannibalism is costly for the experiments with T. fenestrata have shown that male competitive male depends on whether it occurs before copulation, or after his ability was affected by the number of legs lost, as males with fewer first or second copulation. Males that have achieved their legs were less successful in maleemale contests and post- maximum possible insemination rate in their final copulation may copulatory mate guarding (Fromhage & Schneider, 2005b). Based be complicit and actively sacrifice their body to the female on the idea that copulatory male leg ejection (and female occupa- (Andrade, 1996; Andrade, Gu, & Stoltz, 2005; Schwartz, Wagner, & tion with feeding on the legs) serves to reduce the risk of sexual Hebets, 2014). Accordingly, male and female interests may diverge cannibalism, another study compared the frequency of cannibalism not simply over the event, but also over the timing of the male's between males that had their front legs removed before copulation death, so that the timing of cannibalism can be considered a trait and control groups in which males had either two other legs or no under sexually antagonistic selection (Fromhage & Schneider, legs removed (Fromhage & Schneider, 2006). Although males 2006). missing legs were cannibalized more than twice as often as intact Male counter-adaptations to sexual cannibalism are manifold males, the differences were not significant. However, a potential and comprise reducing harm during attempted cannibalism by relationship between leg ejection and cannibalism may have been means of a protective abdominal constriction (Andrade et al., obscured by a high degree of variation and limited sample sizes. 2005), feigning death (Bilde, Tuni, Elsayed, Pekar, & Toft, 2006), Expanding on our hypothesis regarding the function of copu- binding the female with silk (Zhang, Kuntner, & Li, 2011), mating latory male leg ejection, we propose that males sacrifice their legs with subadult females (Biaggio, Sandomirsky, Lubin, Harari, & as an investment in paternity success with a given female. We Andrade, 2016), remote copulation (i.e. continued sperm transfer performed a series of experiments to test the following hypotheses: by an autotomized mating organ; Li, Oh, Kralj-Fiser, & Kuntner, (1) the sensory trap hypothesis: conspecific male legs should be 2012), and mating with a moulting, and hence defenceless (Uhl, particularly attractive food items for females (possibly by means of Zimmer, Renner, & Schneider, 2015), or a feeding and hence occu- special cuticular substances); (2) the mating investment hypothe- pied and distracted female (Fromhage & Schneider, 2005a). sis: males should preferentially invest in high-quality mates; and Mating while the female is feeding has been experimentally (3), the female pacifier hypothesis: feeding on a male leg should shown to reduce sexual cannibalism in the African golden-silk reduce female aggression and resistance behaviour to the benefitof spider, Trichonephila fenestrata, resulting in significantly higher the male. We first compared female handling duration between paternity (Fromhage & Schneider, 2005a). (The name of the genus male legs and normal insect prey items, as well as between sani- has recently been changed from Nephila to Trichonephila, Kuntner tized (ethanol-washed) and untreated male legs, to test for specific et al., 2018.) Males in this species possess typical one-shot geni- properties of the latter. Second, we staged mating trials with sibling talia that break off during copulation to produce mating plugs and nonsibling pairings to vary relative mate quality and genetic (Fromhage & Schneider, 2006). However, these plugs do not always compatibility. We predicted males would invest more in unrelated, prevent successive copulations and rivals still pose a significant higher quality females and hence would eject more legs in non- threat to a male's paternity. It is therefore important for males to sibling trials. Third, we experimentally simulated copulatory male survive mating and to defend the female against rivals as a measure leg ejection by offering male legs to females during mating and of paternity protection (Fromhage & Schneider, 2005a). Consistent expected the probability of female attacks and cannibalism to be with this notion, males of T. fenestrata are not complicit in sexual reduced

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