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Eunuchs are better fighters

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Abstract

Genital amputation, that is, genital damage or loss, seems maladaptive because it renders the amputee functionally sterile, but is nevertheless common in sexually dimorphic spiders. In these species, male genital amputation correlates with plugging of female genitals and with sexual cannibalism. Genital amputation in male spiders may be partial or full; the latter is known as the eunuch phenomenon. We tested two adaptive hypotheses about eunuch behaviour in an orb web spider, Nephilengys malabarensis: (1) the plugging hypothesis (i.e. broken male genitals (palps) effectively plug the female genitals) and (2) the better fighter hypothesis (i.e. eunuch males are better fighters than their intact rivals). By staging mating trials, we documented genital amputation (occurrence and frequency), sexual cannibalism and genital organ reuse, morphologically examined plugs to infer their effectiveness, and conducted a series of male-male contests to determine whether eunuch males were better fighters. Copulations always resulted in amputation of the palps: 87.5% of males became eunuchs directly during copulation and plugged females, while 12.5% of males first partially damaged the palps and then severed them after copulation. Sexual cannibalism and plugging effectiveness both reached 75%. Eunuchs guarded females, were highly aggressive and active, and initiated and won contests more often, whereas intact males and half-eunuchs showed significantly lower levels of guarding behaviour, aggression and general activity. Thus, both hypotheses are supported and we conclude that the eunuch phenomenon is adaptive.

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... Under both natural and sexual selection traits are expected to evolve that increase the likelihood of successful transfer of genes to the next generation. Traits securing paternity or maternity often appear to be self-sacrificial, such as selfless parental care defending offspring against predators (Svagelj, Trivellini & Quintana, 2012), the often risky male defence of females against competing males (Milner, Jennions & Backwell, 2010;Kralj-Fišer et al., 2011), and in some cases pure self-sacrifice such as a mother offering herself as food for her offspring (matriphagy) (Schneider, Salomon & Lubin, 2003), or a male offering himself as food for his mate (male complicity to sexual cannibalism) (Andrade, 1996). Emasculation, where males break off their genitals to become eunuchs (Lee et al., 2012) may be seen as an extreme case of organic sacrifice. ...
... However, being known only in very few groups of dipterans (Downes, 1978) and spiders (reviewed here) the phenomenon has received too limited attention, despite its repeated origins suggesting evolutionary significance through common selection pressures. For example, both in ceratopogonine dipterans and orb-web spiders emasculation seems to be associated with female-biased sexual size dimorphism (SSD) and sexual cannibalism (Downes, 1978;Knoflach & van Harten, 2001;Knoflach, 2002;Ramos, Irschick & Christenson, 2004;Agnarsson, 2006;Miller, 2007;Kuntner, Agnarsson & Gregorič, 2009;Kuntner, Coddington & Schneider, 2009;Kralj-Fišer et al., 2011Lee et al., 2012;Li et al., 2012). The lack of literature reports in other animal clades does not necessarily mean that the phenomenon is not more widespread than currently understood. ...
... Spiders represent excellent models to study emasculation in an evolutionary context for several reasons. First, our understanding of emasculation in spiders has seen recent phylogenetic, observational and experimental advances (Knoflach & van Harten, 2001;Agnarsson, 2006;Kralj-Fišer et al., 2011;Lee et al., 2012;Li et al., 2012). Second, because they possess paired genitalia (Fig. 1A, B), spiders make interesting models for sexual selection research (Eberhard, 2004); specifically in the emasculation context, losing one organ does not mean zero chances to remate. ...
... Under both natural and sexual selection traits are expected to evolve that increase the likelihood of successful transfer of genes to the next generation. Traits securing paternity or maternity often appear to be self-sacrificial, such as selfless parental care defending offspring against predators (Svagelj, Trivellini & Quintana, 2012), the often risky male defence of females against competing males (Milner, Jennions & Backwell, 2010;Kralj-Fišer et al., 2011), and in some cases pure self-sacrifice such as a mother offering herself as food for her offspring (matriphagy) (Schneider, Salomon & Lubin, 2003), or a male offering himself as food for his mate (male complicity to sexual cannibalism) (Andrade, 1996). Emasculation, where males break off their genitals to become eunuchs (Lee et al., 2012) may be seen as an extreme case of organic sacrifice. ...
... However, being known only in very few groups of dipterans (Downes, 1978) and spiders (reviewed here) the phenomenon has received too limited attention, despite its repeated origins suggesting evolutionary significance through common selection pressures. For example, both in ceratopogonine dipterans and orb-web spiders emasculation seems to be associated with female-biased sexual size dimorphism (SSD) and sexual cannibalism (Downes, 1978;Knoflach & van Harten, 2001;Knoflach, 2002;Ramos, Irschick & Christenson, 2004;Agnarsson, 2006;Miller, 2007;Kuntner, Agnarsson & Gregorič, 2009;Kuntner, Coddington & Schneider, 2009;Kralj-Fišer et al., 2011Lee et al., 2012;Li et al., 2012). The lack of literature reports in other animal clades does not necessarily mean that the phenomenon is not more widespread than currently understood. ...
... Spiders represent excellent models to study emasculation in an evolutionary context for several reasons. First, our understanding of emasculation in spiders has seen recent phylogenetic, observational and experimental advances (Knoflach & van Harten, 2001;Agnarsson, 2006;Kralj-Fišer et al., 2011;Lee et al., 2012;Li et al., 2012). Second, because they possess paired genitalia (Fig. 1A, B), spiders make interesting models for sexual selection research (Eberhard, 2004); specifically in the emasculation context, losing one organ does not mean zero chances to remate. ...
Article
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Under natural and sexual selection traits often evolve that secure paternity or maternity through self-sacrifice to predators, rivals, offspring, or partners. Emasculation—males removing their genitals—is an unusual example of such behaviours. Known only in insects and spiders, the phenomenon's adaptiveness is difficult to explain, yet its repeated origins and association with sexual size dimorphism (SSD) and sexual cannibalism suggest an adaptive significance. In spiders, emasculation of paired male sperm-transferring organs — secondary genitals — (hereafter, palps), results in ‘eunuchs’. This behaviour has been hypothesized to be adaptive because (i) males plug female genitals with their severed palps (plugging hypothesis), (ii) males remove their palps to become better fighters in male–male contests (better-fighter hypothesis), perhaps reaching higher agility due to reduced total body mass (gloves-off hypothesis), and (iii) males achieve prolonged sperm transfer through severed genitals (remote-copulation hypothesis). Prior research has provided evidence in support of these hypotheses in some orb-weaving spiders but these explanations are far from general. Seeking broad macroevolutionary patterns of spider emasculation, we review the known occurrences, weigh the evidence in support of the hypotheses in each known case, and redefine more precisely the particular cases of emasculation depending on its timing in relation to maturation and mating: ‘pre-maturation’, ‘mating’, and ‘post-mating’. We use a genus-level spider phylogeny to explore emasculation evolution and to investigate potential evolutionary linkage between emasculation, SSD, lesser genital damage (embolic breakage), and sexual cannibalism (females consuming their mates). We find a complex pattern of spider emasculation evolution, all cases confined to Araneoidea: emasculation evolved at least five and up to 11 times, was lost at least four times, and became further modified at least once. We also find emasculation, as well as lesser genital damage and sexual cannibalism, to be significantly associated with SSD. These behavioural and morphological traits thus likely co-evolve in spiders. Emasculation can be seen as an extreme form of genital mutilation, or even a terminal investment strategy linked to the evolution of monogyny. However, as different emasculation cases in araneoid spiders are neither homologous nor biologically identical, and may or may not serve as paternity protection, the direct link to monogyny is not clear cut. Understanding better the phylogenetic patterns of emasculation and its constituent morphologies and behaviours, a clearer picture of the intricate interplay of natural and sexual selection may arise. With the here improved evolutionary resolution of spider eunuch behaviour, we can more specifically tie the evidence from adaptive hypotheses to independent cases, and propose promising avenues for further research of spider eunuchs, and of the evolution of monogyny.
... In response to intense sperm competition males of sexually size dimorphic orb weavers evolved strategies to monopolize females, thereby securing paternity, i.e. mate guarding [16][17][18] , opportunistic mating 18,19 , plugging of female genitalia [20][21][22] , genital self-mutilation [23][24][25] , and remote copulation 26 . Most such male strategies are present in C. darwini. ...
... These males then chew-off the remaining palpal bulbs to become eunuchs 6,27 . Mate-plugging is hypothesized to be adaptive because genital plugs might prevent subsequent males to copulate with the same female (plugging hypothesis), while removal of entire palps might render the eunuch male to become a better fighter in male-male contests, either through increased aggression (better-fighter hypothesis) or increased agility (gloves-off hypothesis) 17,25,27,28 . However, in C. darwini, genital plugs are likely removed by subsequent males, enabling females to remate into previously used copulatory openings. ...
... . On the other hand, mating systems in other species range from almost complete monogamy (e.g. Herennia, Nephilengys, Nephilingis17,28,34 ) to polygamy (e.g. some Latrodectus and Nephila 28,31,32,35,36 ). ...
... In several nephilid spiders, males plug female genitalia during copulation, thereby reducing their chance of remating with other males Nessler et al. 2007;Kuntner et al. 2009b;Uhl et al. 2009). Males that survive copulation guard their mates, additionally reducing female polyandry (Kuntner et al. 2009a, b;Kralj-Fišer et al. 2011). We propose that in species where males plug female genitals and then guard them, females may consume the mate to avoid being monopolized, in particular after the first mating encounter Kralj-Fišer et al. 2011). ...
... Males that survive copulation guard their mates, additionally reducing female polyandry (Kuntner et al. 2009a, b;Kralj-Fišer et al. 2011). We propose that in species where males plug female genitals and then guard them, females may consume the mate to avoid being monopolized, in particular after the first mating encounter Kralj-Fišer et al. 2011). On the other hand, if the (guarding) male is of superior quality (e.g., large, aggressive), females may not oppose monopolization due to heritable advantages of sired offspring in foraging and mating contexts (Elgar 1998;Persons and Uetz 2005;Kralj-Fišer et al. 2011). ...
... We propose that in species where males plug female genitals and then guard them, females may consume the mate to avoid being monopolized, in particular after the first mating encounter Kralj-Fišer et al. 2011). On the other hand, if the (guarding) male is of superior quality (e.g., large, aggressive), females may not oppose monopolization due to heritable advantages of sired offspring in foraging and mating contexts (Elgar 1998;Persons and Uetz 2005;Kralj-Fišer et al. 2011). ...
Article
Full-text available
Sexual cannibalism particularly before mating is costly for the male victim but also for the female aggressor if she risks remaining unmated. The aggressive spillover hypothesis explains the persistence of this behavior as a maladaptive side effect of positive selection on aggressiveness in a foraging context. The hypothesis predicts that the occurrence of sexual cannibalism is explained by female aggressiveness but is not related to male phenotype or behavioral type. An alternative hypothesis invokes sexual selection and makes the opposite prediction namely that sexual cannibalism is an expression of female choice and should hence mainly target males of low quality. We tested the above hypotheses on a sexually dimorphic nephilid spider Nephilengys livida, known for male monopolization of females via genital damage, female genital plugging, and mate guarding, by staging mating trials during which we recorded mating behaviors and occurrences of pre- and postcopulatory cannibalism. We did not restrict assessment of aggressiveness to the mating and foraging context but also included aggression against same sex conspecifics. To assess female personalities, i. e., consistent individual differences in behavior including aggressiveness, we repeatedly tested them for intra-sex aggression, voracity towards prey, locomotory activity, and boldness. Females exhibited consistent differences in intra-sex aggressiveness, latency to attack prey, and boldness. Aggressive females had shorter latencies to attack prey and were more active than non-aggressive ones. In contrast to the predictions of the aggressive spillover hypothesis, females that were aggressive towards prey and towards other females were not more likely to attack a male than non-aggressive females. In support of the mate choice hypothesis, less aggressive males were more likely attacked and cannibalized than more aggressive ones. This hints at sexual selection for aggressiveness in males and raises the question of mechanisms that maintain variation in male aggressiveness.
... In several nephilid spiders, males plug female genitalia during copulation, thereby reducing their chance of remating with other males (Fromhage and Schneider 2006; Nessler et al. 2007; Kuntner et al. 2009b; Uhl et al. 2009). Males that survive copulation guard their mates, additionally reducing female polyandry (Kuntner et al. 2009a, b; Kralj-Fišer et al. 2011). We propose that in species where males plug female genitals and then guard them, females may consume the mate to avoid being monopolized, in particular after the first mating encounter (Schneider et al. 2006; Kralj-Fišer et al. 2011). ...
... Males that survive copulation guard their mates, additionally reducing female polyandry (Kuntner et al. 2009a, b; Kralj-Fišer et al. 2011). We propose that in species where males plug female genitals and then guard them, females may consume the mate to avoid being monopolized, in particular after the first mating encounter (Schneider et al. 2006; Kralj-Fišer et al. 2011). On the other hand, if the (guarding) male is of superior quality (e.g., large, aggressive), females may not oppose monopolization due to heritable advantages of sired offspring in foraging and mating contexts (Elgar 1998; Persons and Uetz 2005; Kralj-Fišer et al. 2011). ...
... We propose that in species where males plug female genitals and then guard them, females may consume the mate to avoid being monopolized, in particular after the first mating encounter (Schneider et al. 2006; Kralj-Fišer et al. 2011). On the other hand, if the (guarding) male is of superior quality (e.g., large, aggressive), females may not oppose monopolization due to heritable advantages of sired offspring in foraging and mating contexts (Elgar 1998; Persons and Uetz 2005; Kralj-Fišer et al. 2011). Sexual selection can act directly through female aggression targeting undesired suitors or indirectly if females are indiscriminately aggressive towards mates, but only highquality males survive attacks. ...
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Sexual cannibalism particularly before mating is costly for the male victim but also for the female aggressor if she risks remaining unmated. The aggressive spillover hypothesis explains the persistence of this behavior as a maladaptive side effect of positive selection on aggressiveness in a foraging context. The hypothesis predicts that the occurrence of sexual cannibalism is explained by female aggressiveness but is not related to male phenotype or behavioral type. An alternative hypothesis invokes sexual selection and makes the opposite prediction namely that sexual cannibalism is an expression of female choice and should hence mainly target males of low quality. We tested the above hypotheses on a sexually dimorphic nephilid spider Nephilengys lívida, known for male monopolization of females via genital damage, female genital plugging, and mate guarding, by staging mating trials during which we recorded mating behaviors and occurrences of pre-and postcopulatory cannibalism. We did not restrict assessment of aggressiveness to the mating and foraging context but also included aggression against same sex conspecifics. To assess female personalities, i.e., consistent individual differences in behavior including aggressiveness, we repeatedly tested them for intra-sex aggression, voracity towards prey, locomotory activity, and boldness. Females exhibited consistent differences in intra-sex aggressiveness, latency to attack prey, and boldness. Aggressive females had shorter latencies to attack prey and were more active than nonaggressive ones. In contrast to the predictions of the aggressive spillover hypothesis, females that were aggressive towards prey and towards other females were not more likely to attack a male than non-aggressive females. In support of the mate choice hypothesis, less aggressive males were more likely attacked and cannibalized than more aggressive ones. This hints at sexual selection for aggressiveness in males and raises the question of mechanisms that maintain variation in male aggressiveness.
... This is especially common in polyandrous systems in which a female can mate multiple times with several males (Schaefer & Uhl, 2003;Schneider & Andrade, 2011). Under such circumstances, the fertilization success gained by a male of inferior physical condition may be determined by how successfully it can defend the female from other mate-searching males during postcopulatory mate guarding (Fromhage & Schneider, 2005;Kralj-Fišer et al., 2011). ...
... Riechert (1984) showed that in jumping spiders, previous owners of a contested resource (e.g. a mate) are also more likely to defeat their opponents in contests. In polyandrous spider species, mated males usually win contests against virgin competitors even when the latter are physically superior, especially in species in which the males damage their palps, the sexual organs, permanently to serve as mating plugs during mating, such as in Trichonephila fenestrata (formerly Nephila fenestrata) (Fromhage & Schneider, 2005) and Nephilengys malabarensis (Kralj-Fišer et al., 2011). However, unlike our study system, mated males in these polyandrous species may be winners (i.e. ...
... In addition, mated males in these polyandrous species have limited opportunities to fertilize other females because searching for new mates is very risky and greatly reduces their numbers; thus, putting more effort into guarding mated females is more effective in ensuring fitness than searching for other receptive females. Moreover, because of selfemasculation, the mated males have nothing to lose, rendering them more willing to escalate contests ( Kralj-Fišer et al., 2011;Kuntner et al., 2015). However, in our study system, male palps were not damaged during mating, and males were able to mate repeatedly, so theoretically males could fertilize many other females, and the palps could still be charged by newly produced sperm. ...
Article
Full-text available
Mating may change a male’s behaviour by increasing its motivation to engage in a contest, and enabling it to win in subsequent male–male contests. To test this hypothesis, we recorded male contests in the wolf spider, Venonia coruscans (Araneae: Lycosidae), testing a male’s motivation to fight under three different resource value conditions. First, we staged contests between two males in two different resource value conditions, on an egg-produced female’s web and then on a virgin female’s web, to test a male’s fighting ability. After determining each male’s fighting ability, we allowed each loser that lost its contests under both resource value conditions to mate with a virgin female and then introduced the previous contest winner to the web where the loser had mated. We found that without mating, the losers always lost their contests, regardless of the resource value conditions. However, once they had mated, the losers fiercely attacked the previous winners, and most won the contests back. Our study therefore provides evidence that a male’s motivation to fight can be changed under certain circumstances (e.g. mating) and can greatly influence contest outcomes in male–male competition in a mating context.
... In spiders, preliminary reports of arms races encompass the evolution of extreme phenotypes 14 . Among them are sexual size dimorphism (SSD), male-biased sex ratios that underlie high sperm competition, polyandry, monogyny, genital mutilation, and sexual cannibalism 11,12,[14][15][16][17][18][19][20][21] . Sexual cannibalism is widespread in sexually dimorphic spider lineages 12,14,18,22 . ...
... Choosing the palp with more sperm is logically expected in species with palpal mutilation, a common mating strategy in monogynous males facing sexually cannibalistic females (e.g., Araneidae and Theridiidae 19,35,36 ). Within our comparative sample, only N. malabarensis males engage in full emasculation, i.e., severing one or both palps entirely ("half-eunuchs" and "eunuchs", respectively 17,18 ). Unlike full eunuchs, half-eunuchs may have another potential shot at mating if they successfully escaped a cannibalistic female. ...
... Because of this, male Nephilengys often break off their palps during copulation (Supplementary Fig. 5) to avoid being cannibalised while continuing to transfer sperm into the female's spermatheca to increase male chances of producing progeny 37 . Eunuch males also benefit from being lighter and agile: the 'gloves-off' hypothesis predicts enhancement of eunuch survival through higher physical stamina and endurance 17 . Since the advantages of palp severance appear to exceed its cost, most males break off their palps. ...
Article
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When sexual conflict selects for reproductive strategies that only benefit one of the sexes, evolutionary arms races may ensue. Female sexual cannibalism is an extreme manifestation of sexual conflict. Here we test two male mating strategies aiming at countering sexual cannibalism in spiders. The “better charged palp” hypothesis predicts male selected use of the paired sexual organ (palp) containing more sperm for their first copulation. The “fast sperm transfer” hypothesis predicts accelerated insemination when cannibalism is high. Our comparative tests on five orbweb spider species with varying levels of female sexual cannibalism and sexual size dimorphism (SSD) reveal that males choose the palp with more sperm for the first copulation with cannibalistic females and that males transfer significantly more sperm if females are cannibalistic or when SSD is biased. By supporting the two hypotheses, these results provide credibility for male mating syndrome. They, however, open new questions, namely, how does a male differentiate sperm quantities between his palps? How does he perform palp choice after assessing his cannibalistic partner? By conducting follow-up experiments on Nephilengys malabarensis, we reveal that it is sperm volume detection, rather than left-right palp dominance, that plays prominently in male palp choice.
... In general support of the plugging hypothesis, numerous studies demonstrate paternity benefits of plugs made of male genital parts. For example, empirical research has shown adaptive function of lesser genital damage in Nephila (Fromhage and Schneider 2006), Argiope (Nessler et al. 2007(Nessler et al. , 2009Ghione and Costa 2011;Herberstein et al. 2012), and Latrodectus (Snow et al. 2006) and of emasculation in Tidarren (Knoflach and van Harten 2001;Ramos et al. 2004) and in two nephilid species, the SE Asian Nephilengys malabarensis and the Malagasy Nephilingis livida (Kralj-Fišer et al. 2011;Kralj-Fišer and Kuntner 2012;Lee et al. 2012;Li et al. 2012). However, mating plugs consisting of male spider genital parts are not always fully effective in preventing female remating (Schneider and Elgar 2001;Schneider and Elgar 2002;Kralj-Fišer et al. 2011;Fromhage and Schneider 2012) and thus the plugging spider male may increase his monopolization of the female through postcopulatory mate guarding (Robinson and Robinson 1980;Fromhage and Schneider 2006;Kralj-Fišer et al. 2011). ...
... For example, empirical research has shown adaptive function of lesser genital damage in Nephila (Fromhage and Schneider 2006), Argiope (Nessler et al. 2007(Nessler et al. , 2009Ghione and Costa 2011;Herberstein et al. 2012), and Latrodectus (Snow et al. 2006) and of emasculation in Tidarren (Knoflach and van Harten 2001;Ramos et al. 2004) and in two nephilid species, the SE Asian Nephilengys malabarensis and the Malagasy Nephilingis livida (Kralj-Fišer et al. 2011;Kralj-Fišer and Kuntner 2012;Lee et al. 2012;Li et al. 2012). However, mating plugs consisting of male spider genital parts are not always fully effective in preventing female remating (Schneider and Elgar 2001;Schneider and Elgar 2002;Kralj-Fišer et al. 2011;Fromhage and Schneider 2012) and thus the plugging spider male may increase his monopolization of the female through postcopulatory mate guarding (Robinson and Robinson 1980;Fromhage and Schneider 2006;Kralj-Fišer et al. 2011). In accordance with the "asset protection principle" (Clark 1994), predicting that a male should adjust his behavior to its future residual reproductive potential, the better-fighter hypothesis predicts escalated eunuch aggressiveness toward rival males with intact genitals (Kralj-Fišer et al. 2011). ...
... For example, empirical research has shown adaptive function of lesser genital damage in Nephila (Fromhage and Schneider 2006), Argiope (Nessler et al. 2007(Nessler et al. , 2009Ghione and Costa 2011;Herberstein et al. 2012), and Latrodectus (Snow et al. 2006) and of emasculation in Tidarren (Knoflach and van Harten 2001;Ramos et al. 2004) and in two nephilid species, the SE Asian Nephilengys malabarensis and the Malagasy Nephilingis livida (Kralj-Fišer et al. 2011;Kralj-Fišer and Kuntner 2012;Lee et al. 2012;Li et al. 2012). However, mating plugs consisting of male spider genital parts are not always fully effective in preventing female remating (Schneider and Elgar 2001;Schneider and Elgar 2002;Kralj-Fišer et al. 2011;Fromhage and Schneider 2012) and thus the plugging spider male may increase his monopolization of the female through postcopulatory mate guarding (Robinson and Robinson 1980;Fromhage and Schneider 2006;Kralj-Fišer et al. 2011). In accordance with the "asset protection principle" (Clark 1994), predicting that a male should adjust his behavior to its future residual reproductive potential, the better-fighter hypothesis predicts escalated eunuch aggressiveness toward rival males with intact genitals (Kralj-Fišer et al. 2011). ...
Article
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Emasculation—males becoming effectively sterile by self-removing their genitals—has long been considered a peculiar evolutionary phenomenon with unknown function, taxonomically restricted to few spiders and flies. In spiders, emasculation results in half or full eunuchs when males sever one or both sperm transferring organs, palps. Three types of emasculation, pre-maturation, mating, and post-mating are known in spiders, all having evolved multiple times. Males practicing pre-maturation emasculation sever one of their palps while still immature, then engage in strict monogyny via genital plugging and spontaneous death. Emasculation during mating also results in genital plugs, but half eunuchs have another chance to mate. So far, the behavior of those males that become eunuchs post-mating by self-removing disfigured palps has not been investigated empirically. We test the mechanism and adaptive significance of post-mating emasculation in coin spiders (Herennia multipuncta) and use phylogenetic reconstruction to understand its evolutionary history. Our laboratory assays corroborate three hypotheses related to mate monopolization: (1) The plugging hypothe-sis—predicting genital plugs to prevent female remating; (2) The better-fighter hypothesis—predicting enhanced eunuch aggressiveness toward rivals; and (3) The gloves-off hypoth-esis—predicting increased eunuch endurance. The support for these hypotheses in spiders practicing emasculation during and after mating reinforces recent phylogenetic interpretations of these two emasculation types being evolutionarily linked in the family Nephilidae. We weigh the evidence in support of three different, but equally parsimonious scenarios of nephilid emasculation evolution. We conclude that emasculation is an adaptive, sexually selected trait that calls for further compar-ative and experimental research.
... The vast majority of documented invertebrate mating plugs are produced by males either through glandular secretions15161718192021222324252627 or ejaculates13141516171819202122232425262728293031, or by utilizing severed male somatic [23] or genital parts [32] as copulatory barriers. The latter phenomenon, termed 'mate plugging through genital mutilation' [33,34], or simply 'emasculation' [35], has been shown to serve male's paternity protection [35]. Male initiated plugging is an adaptation to sperm competition [36] , because plugged females are monopolized and are thus unavailable to subsequent males as long as plugs remain effective [16,20,23,27,35] . ...
... In spiders, it seems that the vast majority of plugs are indeed male produced while female plug (co)production is rare [24,41,43]. The best documented are those spider plugs that arise through male genital mutilation32333435364445464748, and several studies also document amorphous plugs consisting of male glandular or sperm secretions [24,27]. In fact, the literature is nearly devoid of any evidence of female produced plugs in spiders. ...
Article
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Males usually produce mating plugs to reduce sperm competition. However, females can conceivably also produce mating plugs in order to prevent unwanted, superfluous and energetically costly matings. In spiders-appropriate models for testing plugging biology hypotheses-mating plugs may consist of male genital parts and/or of amorphous covers consisting of glandular or sperm secretions. In the giant wood spider Nephila pilipes, a highly sexually dimorphic and polygamous species, males are known to produce ineffective embolic plugs through genital damage, but nothing is known about the origin and function of additional conspicuous amorphous plugs (AP) covering female genitals. We tested alternative hypotheses of the nature and function of AP in N. pilipes by staging mating trials with varying degrees of polyandry. No APs were ever formed during mating trials, which rules out the possibility of male AP formation. Instead, those females that oviposited produced the AP from a liquid secreted during egg sac formation. Polyandrous females were more likely to lay eggs and to produce the AP, as were those that mated longer and with more total insertions. Our further tests revealed that, in spite of being a side product of egg sac production, AP, when hardened, prevented any subsequent copulation. We conclude that in the giant wood spider (Nephila pilipes), the amorphous mating plugs are not produced by the males, that repeated copulations (most likely polyandrous) are necessary for egg fertilization and AP formation, and that the AP represents a female adaptation to sexual conflict through prevention of unwanted, excessive copulations. Considering the largely unknown origin of amorphous plugs in spiders, we predict that a similar pattern might be detected in other clades, which would help elucidate the evolutionary interplay of various selection pressures responsible for the origin and maintenance of mating plugs.
... Postcopulatory mate guarding (Figure 4c-e) is one way to monopolize a female, but plugging of the female genital tract, by male genital breakage or even full emasculation, is another (82). Coin and hermit spider males-all approximately four times smaller than their females-use their severed genitalia physically to block females from remating (71,72,88,89). Curiously, N. pilipes males have hair-like genitalic termini that are ineffective plugs, even though they break off inside the female (88). ...
... These eunuch males are superior fighters and fiercely defend the female from intruders (89). Eunuch male hermit spiders endure longer and fight more aggressively than intact males (71,92). The severed palp stuck in the female genitalia still contains the male sperm reservoir, as well as the sclerites that help to transfer sperm. ...
Article
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Sexual size dimorphism is one of the most striking animal traits, and among terrestrial animals, it is most extreme in certain spider lineages. The most extreme sexual size dimorphism (eSSD) is female biased. eSSD itself is probably an epiphenomenon of gendered evolutionary drivers whose strengths and directions are diverse. We demonstrate that eSSD spider clades are aberrant by sampling randomly across all spiders to establish overall averages for female (6.9 mm) and male (5.6 mm) size. At least 16 spider eSSD clades exist. We explore why the literature does not converge on an overall explanation for eSSD and propose an equilibrium model featuring clade- and context-specific drivers of gender size variation. eSSD affects other traits such as sexual cannibalism, genital damage, emasculation, and monogyny with terminal investment. Coevolution with these extreme sexual phenotypes is termed eSSD mating syndrome. Finally, as costs of female gigantism increase with size, eSSD may represent an evolutionary dead end. Expected final online publication date for the Annual Review of Entomology, Volume 65 is January 7, 2020. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
... They may also exhibit behaviours that may not simply be nociceptive reflexes; e.g. jumping (Suter and Gruenwald 2000), shaking web (Jackson et al. 1992;Kralj-Fišer et al. 2011) and autotomy (Eisner and Camazine 1983;Punzo 1997). Their antipredator behaviour includes thanatosis (feigning death-this behaviour is characterized by curling legs and freezing, resulting in a body posture very similar to that of a dead spider) (Bilde et al. 2006;Kralj-Fišer and Schneider 2012) and "bailing out", in which the spider drops from the web and hangs motionless from a dragline with huddled legs . ...
... grasped by a predator or a conspecific during fight, in order to escape more easily (Punzo 1997;Foelix 2011). Furthermore, they self-amputate injured appendages (Kralj-Fišer et al. 2011;Kralj-Fišer and Kuntner 2012;Kuntner et al. 2014), and they "lick" or rub their wounds. Missing appendages may negatively affect development, web building, foraging success, competitive abilities and mating success in some species, whereas in several species it has no apparent costs (reviewed in Fleming et al. 2007). ...
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Spiders with around 48,000 recorded species are major terrestrial predators and thus crucially important for ecosystem functioning. They are widely used as research models and for biodiversity displays and sometimes also kept as pets. Nevertheless, we are not aware of any legal ethical rules bound to spider welfare during rearing or research. To set ethical standards, we first need to detect and assess how spiders “perceive” the external world. Based on the current knowledge of spiders’ sensory and nervous system, it is difficult to judge whether spiders feel pain, distress and suffering, although their behaviours like thanatosis, “bailing out”, autotomy and associative avoidance learning imply so. As is now known, arthropods are not simply mini-robots as traditionally believed. Thus, spider welfare deserves more research effort, and the ethical standards for rearing or using spiders in research need to be set. Here, we describe the variety of spider physiological and behavioural characteristics and how they apply to their rearing, housing, handling and experimental use. We hope reporting these methods will help ensuring welfare and well-being of spiders in captivity.
... Our morphological examinations on the prevalence of genital plugs, consisting of palpal parts from a single versus multiple males [43,44], helped score for male genital damage presence or absence for most taxa in the phylogeny (Additional file 1: Table S1). Additional evidence comes from detailed species level experimental studies [39,41,[48][49][50][51][52][53]. ...
... We define polygyny as male mating with more than one female, whereas monogynous males invest into repeated mating with the same female in an attempt to plug both of her copulatory openings. We based the inferred mating rates in nephilids and outgroups (Additional file 1: Table S1) on available experimental studies [13,[39][40][41] and on genital damage data where single versus multiple male mating plugs per female copulatory opening predict monandry and polyandry, respectively [26,35,40,41,53]. Most Nephila species, and Phonognatha graeffei, are polyandrous [49,61]. ...
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Background Genital diversity may arise through sexual conflict over polyandry, where male genital features function to manipulate female mating frequency against her interest. Correlated genital evolution across animal groups is consistent with this view, but a link between genital complexity and mating rates remains to be established. In sexually size dimorphic spiders, golden orbweaving spiders (Nephilidae) males mutilate their genitals to form genital plugs, but these plugs do not always prevent female polyandry. In a comparative framework, we test whether male and female genital complexity coevolve, and how these morphologies, as well as sexual cannibalism, relate to the evolution of mating systems. Results Using a combination of comparative tests, we show that male genital complexity negatively correlates with female mating rates, and that levels of sexual cannibalism negatively correlate with male mating rates. We also confirm a positive correlation between male and female genital complexity. The macroevolutionary trajectory is consistent with a repeated evolution from polyandry to monandry coinciding with the evolution towards more complex male genitals. Conclusions These results are consistent with the predictions from sexual conflict theory, although sexual conflict may not be the only mechanism responsible for the evolution of genital complexity and mating systems. Nevertheless, our comparative evidence suggests that in golden orbweavers, male genital complexity limits female mating rates, and sexual cannibalism by females coincides with monogyny. Electronic supplementary material The online version of this article (doi:10.1186/s12862-016-0821-y) contains supplementary material, which is available to authorized users.
... In the family Nephilidae, genital damage and one-shot genitalia seem to have evolved relatively early and are a common pattern in the genera Herennia and Nephi- lengys [13]. In both genera males not only damage their sperm transferring structure, the embolic conductor, but they ectomise the entire pedipalp after copulation, an adaptation termed " eunuch phenomenon " [14,15]. Recent molecular and combined phylogenetic analyses suggest Nephila to be the sistergroup of Nephilengys + Herennia and thus the " eunuch phenomenon " might be a synapomorphy for this clade [16,17] The genus Nephila contains 15 species and their relationships were addressed in recent phylogenetic studies which revealed that either N. fenestrata [18] or a clade with N. pilipes and N. constricta [17] is sister to all remaining Nephila. ...
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Monogynous mating systems with extremely low male mating rates have several independent evolutionary origins and are associated with drastic adaptations involving self-sacrifice, one-shot genitalia, genital damage, and termination of spermatogenesis immediately after maturation. The combination of such extreme traits likely restricts evolutionary potential perhaps up to the point of making low male mating rates irreversible and hence may constitute an evolutionary dead end. Here, we explore the case of a reversion to multiple mating from monogynous ancestry in golden orb-web spiders, Nephila senegalensis. Male multiple mating is regained by the loss of genital damage and sexual cannibalism but spermatogenesis is terminated with maturation, restricting males to a single loading of their secondary mating organs and a fixed supply of sperm. However, males re-use their mating organs and by experimentally mating males to many females, we show that the sperm supply is divided between copulations without reloading the pedipalps. By portioning their precious sperm supply, males achieve an average mating rate of four females which effectively doubles the maximal mating rate of their ancestors. A heritage of one-shot genitalia does not completely restrict the potential to increase mating rates in Nephila although an upper limit is defined by the available sperm load. Future studies should now investigate how males use this potential in the field and identify selection pressures responsible for a reversal from monogynous to polygynous mating strategies.
... Therefore, males with damaged genitalia benefit from guarding their female. These eunuchs, which have no reproductive future at stake, will readily escalate a fight and succeed in chasing away much larger opponents (Fromhage and Schneider 2005a;Kralj-Fišer et al. 2011). Males of Nephilengys malabarensis copulate by detaching the entire pedipalp, which will continue to transfer sperm into the female independently . ...
Article
Sexual cannibalism is a well-known example for sexual conflict and has many facets that determine the costs and benefits for the cannibal and the victim. Here, I focus on species in which sexual cannibalism is a general component of a mating system in which males invest maximally in mating with a single (monogyny) or two (bigyny) females. Sexual cannibalism can be a male strategy to maximize paternity and a female strategy to prevent paternity monopolization by any or a particular male. Considerable variation exists between species (1) in the potential of males to monopolize females, and (2) in the success of females in preventing monopolization by males. This opens up exciting future possibilities to investigate sexually antagonistic coevolution in a largely unstudied mating system.
... Males with broken or missing genitals are functionally sterile after one or two copulations (spiders have paired genitals; Kuntner, Kralj-Fi ser, Schneider, & Li, 2009), and have no further reproductive options. It has been shown that such emasculated males change their aggression and boldness according to the 'extended' asset protection principle (see above), that is, they fight more and take more risk (Kralj-Fi ser, Gregori c, Zhang, Li, & Kuntner, 2011). By vigorously guarding the female they mated with prior to their emasculation (i.e. ...
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Research on animal personality variation has been burgeoning in the last 20 years but surprisingly few studies have investigated personalities in invertebrate species although they make up 98% of all animal species. Such lack of invertebrate studies might be due to a traditional belief that invertebrates are just ‘minirobots’. Lately, studies highlighting personality differences in a range of invertebrate species have challenged this idea. However, the number of invertebrate species investigated still contrasts markedly with the effort that has been made studying vertebrates, which represent only a single subphylum. We describe how investigating proximate, evolutionary and ecological correlates of personality variation in invertebrates may broaden our understanding of personality variation in general. In our opinion, personality studies on invertebrates are much needed, because invertebrates exhibit a range of aspects in their life histories, social and sexual behaviours that are extremely rare or absent in most studied vertebrates, but that offer new avenues for personality research. Examples are complete metamorphosis, male emasculation during copulation, asexual reproduction, eusociality and parasitism. Further invertebrate personality studies could enable a comparative approach to unravel how past selective forces have driven the evolution of personality differences. Finally, we point out the advantages of studying personality variation in many invertebrate species, such as easier access to relevant data on proximate and ultimate factors, arising from easy maintenance, fast life cycles and short generation times.
... Female resistance to mating/remating and sexual cannibalism are comparatively common in spiders (Elgar 1992; Schneider & Lubin 1998; Elgar & Schneider 2004; Prenter et al. 2006; Wilder et al. 2009; Schneider & Andrade 2011), where a variety of behavioural male traits may serve as counteradaptations. These include elaborate courtship displays (Elgar & Nash 1988), nuptial gifts during courtship (Albo & Costa 2010), opportunistic mating with feeding, hunting or moulting females (Moya-Larano et al. 2004; Fromhage & Schneider 2005), genital mutilation and plugging (Segoli et al. 2008; Nessler et al. 2009; Kralj-Fi ser et al. 2011), mate guarding (Fromhage & Schneider 2005; Kralj-Fi ser et al. 2011), abdominal constriction (Andrade et al. 2005) and mate binding, in which the male deposits fine silk onto the female's body in between Contents lists available at SciVerse ScienceDirect ...
Article
To counter female resistance to mating and cannibalism, males of many animal species have evolved a variety of behavioural adaptations. Here we investigated a novel copulatory courtship behaviour, mate binding, in which the male deposits fine silk onto the female's body in between copulation bouts, in an orb-web nephilid spider, Nephila pilipes. We hypothesized that mate binding might reduce female aggressiveness and sexual cannibalism and that both tactile and chemical cues play a role. We performed a series of mating trials, in which we blocked (1) the females' tactile perception, (2) the females' chemoreceptors, and (3) both types of communication. We also manipulated male spinnerets and thus male silk production. As predicted, mate binding reduced both female resistance to repeated mating and levels of sexual cannibalism. Our results suggest that both tactile and chemical cues are crucial for mate binding to succeed in rendering females less aggressive, but that tactile cues are more important. We conclude that mate binding prolongs total copulation duration, whereby the male maximizes his paternity. Therefore, mate binding may serve as a mechanism countering sexual conflict over repeated mating and sexual cannibalism.
... Interestingly, despite their higher aggressiveness, virgin males nevertheless retreated more often than eunuchs. Such higher risk aversion in virgin males compared with mated ones is in accordance with game theory (Fromhage and Schneider 2005a; Kralj-Fišer et al. 2011a). ...
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Male-male competition for females can significantly affect a male's reproductive success and hence his fitness. Game theory predicts that an individual should avoid fighting when its future reproductive potential is high, but should fight forcefully when its future reproductive potential is insignificant. When mates are scarce, extreme competition and fatal fighting is expected. We recently showed that Nephilengys malabarensis eunuchs, i.e. sterile spider males that lost their genitals during copulation, become more aggressive during male-male contests. Here, we add crucial comparative data by exploring eunuch fighting behaviour in Nephilengys livida from Madagascar, specifically by testing the 'better fighter hypotheses' in a laboratory setting. Similar to N. malabarensis, N. livida copulations resulted in total male castration with the severed palp plugging the female genitals in 70.83% cases, which mostly (63.63%) prevented subsequent copulations. Unexpectedly, however, N. livida eunuchs exhibited lower aggressiveness than virgin males. We interpret these results in the light of different mating biology between the so far studied species known for the eunuch phenomenon, which might reflect differing plug effectiveness due to variation in genital anatomy in N. livida, N. malabarensis and Herennia multipuncta. However, detected differences in aggressive behaviour of N. livida versus N. malabarensis eunuchs might also be explained by the species' ecology, with lower population densities resulting in a relaxed male-male competition making excessive aggression and mate guarding redundant. This study thus questions the generality of overt aggressiveness in mated males with no reproductive value, and highlights the importance of understanding the natural history of species in the question.
... 15 cm from a female). In intrasex contests that lasted 20 min, aggressiveness was measured as a sum of scores based on the frequency of aggressive behavior such as approaching (score = 1), web-shaking (score = 1), attacking (score = 2), chasing (score = 3), and biting (score = 3) (Kralj-Fišer, Gregorič, et al. 2011; Kralj-Fišer, Schneider, et al. 2011). " Approach " was defined as a movement by one spider with the result of shortening the distance to the other individual and " chasing " as a quick move in the direction of the other individual resulting in a successful attack or its escape. ...
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Animals within a population differ consistently in behavior over time and/or across conditions. A general question is how such differences referred to as personalities are maintained through evolution. One suggested mechanism is a nonrandom mate choice, which has been supported in species in which mate choice associates with direct material benefits. Much less is known about mating patterns and personality in species where males provide only sperm and in which the benefits of female choice are based only on good and/or compatible genes. The bridge spider Larinioides sclopetarius Clerck (Araneidae) exhibits heritable between-individual differences in intrasex aggressiveness. We studied mating probabilities by aggressiveness type of both sexes, and success in sperm competition of aggressive versus nonaggressive males. We staged trials that resemble field conditions: 4 males (2 aggressive and 2 nonaggressive) had simultaneous choice between an aggressive and a nonaggressive female. Although there were no differences in initial approaches of male types toward female types, aggressive males mainly mated with aggressive females, and nonaggressive males more likely mated with nonaggressive females. Female aggressiveness type was not related to fecundity, which may be a consequence of equal food supply in the laboratory. However, in double-mating trials using the sterile-male technique to measure paternity of aggressive versus nonaggressive males, we found that sons of aggressive parents fathered relatively more offspring. We conclude that assortative mating by aggressiveness type might maintain between-individual differences in aggressiveness in L. sclopetarius.
... Further, males that had recently copulated took over females in a shorter period than noncopulated ones. Such enhancement of competitive performance after sexual experience has been observed in both vertebrates (Guevara-Fiore et al. 2012) and invertebrates (Chamorro-Florescano and Favila 2008;Kralj-Fišer et al. 2011;Kou and Hsu 2013). For example, in the vole Microtus ochrogaster, males with mating experience more aggressively respond to an intruder compared with males that cohabited with a female without mating or that were housed Fig. 1 Cumulative occurrences of takeover in females guarded by owner males during male-male contests of P. nigrofascia. ...
Article
Prior social experience often affects subsequent competitive interactions and their outcomes. Although the effects of prior contest experience have been widely examined, effects of mating experience remain less well examined. We examined, in males of the hermit crab Pagurus nigrofascia, whether males successively copulated with more than one female and whether males with copulation experience differed in their subsequent contest behaviors and probability of winning in male-male contests compared to males without copulation experience. The copulation experience of intruders was manipulated and the contest behaviors compared between mated and unmated groups. Males mated with several females regardless of the male body size. Compared with unmated intruders, intruders with mating experience succeeded more often in taking over females and did so within a shorter period particularly when the male-male contests occurred over females with a long time to molt. These results suggest that mated males of P. nigrofascia overestimate the female quality and/or enhance the competitive performance similar to the “winner effect” that is a positive feedback from prior winning experience to future contests.
... Sexual size dimorphism in araneoid spiders may predictably coevolve with behaviors such as emasculation, genital plugging and sexual cannibalism, judging from their convergent co-occurrence in the families Theridiidae, Nephilidae and Araneidae . The first species level phylogeny of Caerostris represents a new clade to complement ongoing work on the evolutionary patterns, causes and consequences of SSD in the spider family Nephilidae (Kralj-Fišer et al. 2011;Zhang et al. 2011;Danielson-Francois et al. 2012;Kuntner et al. 2012;Li et al. 2012;Kuntner & Elgar 2014), the araneid Argiope (Nessler et al. 2007;Foellmer 2008;Cheng & Kuntner 2014) Diagnosis.-Caerostris of both sexes differ from other araneids by the following combination of somatic features: prosoma and opisthosoma wider than long, head region wide and elevated from thoracic region, two pairs of median prosomal projections (none or one pair in males), the sternal tubercule adjacent to coxae IV, the median and lateral eyes grouped on separate tubercules, a frontal rostrum, cheliceral furrow smooth rather than denticulated, the abdominal sigillae, the flattened and hairy patellae, tibiae and metatarsi of legs I, II and IV, the spatulate setae on femur IV, and the ventro-lateral abdominal sclerotization in several rather than one line of small dots (Grasshoff 1984;Kuntner et al. 2008;. Caerostris differ from other araneids by the following genital features: female epigynum with paired epigynal hooks (Figs. ...
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Bark spiders (genus Caerostris Thorell 1868) are important models in biomaterial research due to the remarkable biomechanical properties of the silk of C. darwini Kuntner & Agnarsson 2010 and its gigantic web. They also exhibit female gigantism and are promising candidates for coevolutionary research on sexual dimorphism. However, Caerostris spiders are taxonomically understudied and the lack of a phylogeny impedes evolutionary research. Using a combination of one mitochondrial and one nuclear marker, we provide the first species-level phylogeny of Caerostris including half of its species diversity but dense terminal sampling focusing on new lineages. Our phylogenetic and morphological results provide the evidence for six previously undescribed species: C. almae n. Sp., C. bojani n. Sp., C. pero n. Sp. and C. wallacei n. Sp., all from Madagascar, C. linnaeus n. Sp. from Mozambique and C. tinamaze n. Sp. from the Republic of South Africa.
... Gregorič, Zhang, Li, & Kuntner, 2011;Kralj-Fišer & Schneider, 2012). We defined "approach" as a movement by one spider toward the other individual, "web-shaking" as sudden and large amplitude shaking of the web, which spiders usually exhibit when approaching other individuals, "attacking" as a sudden move in the direction of the other individual resulting in a body contact with the opponent, and "chasing" as a running after the (escaping) opponent resulting in a successful attack or escape of the opponent(Kralj-Fišer et al., 2017). ...
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Abstract Sex differences in the genetic architecture of behavioral traits can offer critical insight into the processes of sex‐specific selection and sexual conflict dynamics. Here, we assess genetic variances and cross‐sex genetic correlations of two personality traits, aggression and activity, in a sexually size‐dimorphic spider, Nuctenea umbratica. Using a quantitative genetic approach, we show that both traits are heritable. Males have higher heritability estimates for aggressiveness compared to females, whereas the coefficient of additive genetic variation and evolvability did not differ between the sexes. Furthermore, we found sex differences in the coefficient of residual variance in aggressiveness with females exhibiting higher estimates. In contrast, the quantitative genetic estimates for activity suggest no significant differentiation between males and females. We interpret these results with caution as the estimates of additive genetic variances may be inflated by nonadditive genetic effects. The mean cross‐sex genetic correlations for aggression and activity were 0.5 and 0.6, respectively. Nonetheless, credible intervals of both estimates were broad, implying high uncertainty for these estimates. Future work using larger sample sizes would be needed to draw firmer conclusions on how sexual selection shapes sex differences in the genetic architecture of behavioral traits.
... Sterile eunuch males then remain with females and guard them against rival males. In another nephilid, Nephilengys malabarensis (Walckenaer, 1841), eunuch males have an advantage in direct male-male contests (Kralj-Fišer et al. 2011) and show enhanced stamina (Lee et al. 2012). Eunuch males might benefit from lower energy costs, i.e. having lighter bodies (Lee et al. 2012) and access to prey in the female's web, which may explain their longer lifespans. ...
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Adult body size, development time, and growth rates are components of organismal life histories, which crucially influence fitness and are subject to trade-offs. If selection is sex-specific, male and female developments can eventually lead to different optimal sizes. This can be achieved through developmental plasticity and sex-specific developmental trajectories. Spiders present suitable animals to study differences in developmental plasticity and life history trade-offs between the sexes, because of their pronounced sexual dimorphism. Here, we examine variation in life histories in the extremely sexually size dimorphic African hermit spider (Nephilingis cruentata) reared under standardized laboratory conditions. Females average 70 times greater body mass (and greater body size) at maturity than males, which they achieve by developing longer and growing faster. We find a small to moderate amount of variability in life history traits to be caused by family effects, comprising genetic, maternal, and early common environmental effects, suggesting considerable plasticity in life histories. Remarkably, family effects explain a higher variance in male compared to female life histories, implying that female developmental trajectories may be more responsive to environment. We also find sex differences in life history trade-offs and show that males with longer development times grow larger but exhibit shorter adult longevity. Female developmental time also correlates positively with adult body mass, but the trade-offs between female adult mass, reproduction, and longevity are less clear. We discuss the implications of these findings in the light of evolutionary trade-offs between life history traits.
... Male Nephilengys malabarensis also detach their entire pedipalp, which continues sending sperm into a female. Such an emasculated and, thus, lightened male can guard the female from other males more efficiently [15][16][17]. Other males sacrifice themselves as food to females in copula, to send more sperm while being eaten [18]. ...
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Some male spiders exhibit female genital mutilation behaviour (FGM) by removing the female genital appendage (scape) to control the mating frequency of females. Female spiders have two, i.e. right and left, genital openings connected with separate spermathecae into which males transfer sperm successively using one pedipalp (secondary genitalia) at a time. Thus, males must complete at least two palpal insertions to fill both spermathecae, before FGM. The present study examined whether (i) scape removal is only associated with the second palpal insertion (one-action hypothesis) or (ii) two contralateral palpal insertions facilitate FGM, with each insertion cutting the basal part of the scape halfway (two-actions hypothesis). Experiments in which females were replaced after a male had made the first insertion did not support the one-action hypothesis, because scapes remained intact after the newly introduced virgin females received their first palpal insertion, which was the second insertion by the males. In comparison, mating experiments using two half-eunuchs (i.e. one of the palps of each male had been manually removed, forcing them to fill female spermatheca on one side only) supported the twoactions hypothesis. FGM was more frequent in females that received two contralateral palpal insertions than in females that received ipsilateral insertions.
... Environmental and social characteristics can generate or alter sex-specific selection that might enhance, mitigate, or even reverse differences dictated by anisogamy in the POL between the sexes , topical collection on Pace-of-life syndromes). Breeding biology, such as different mating systems and breeding strategies (semelparity and iteroparity), can affect the intensity of sexual selection (Andersson 1994;Bonnet 2011;Kralj-Fišer et al. 2011;Fisher et al. 2013;Janicke et al. 2016), and thus, the existence of sex-specific POL and POLS. For example, we might expect fast males in polygynous systems, fast females in polyandrous systems, and little differences between the sexes in monogamous systems since the intensity of the sex-specific selection varies across these different mating systems. ...
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The pace-of-life syndrome (POLS) hypothesis predicts that behavior and physiology covary with life history. Evidence for such covariation is contradictory, possibly because systematic sources of variation (e.g. sex) have been neglected. Sexes often experience different selection pressures leading to sex-specific allocation between reproduction and self-maintenance, facilitating divergence in life-history. Sex-specific differences in means and possibly variances may therefore play a key role in the POLS framework. We investigate whether sexes differ in means and variances along the fast-slow pace-of-life continuum for life history and physiological and behavioral traits. In addition, we test whether social and environmental characteristics such as breeding strategy, mating system, and study environment explain heterogeneity between the sexes. Using meta-analytic methods, we found that populations with a polygynous mating system or for studies conducted on wild populations, males had a faster pace-of-life for developmental life-history traits (e.g., growth rate), behavior, and physiology. In contrast, adult life-history traits (e.g., lifespan) were shifted towards faster pace-of-life in females, deviating from the other trait categories. Phenotypic variances were similar between the sexes across trait categories and were not affected by mating system or study environment. Breeding strategy did not influence sex differences in variances or means. We discuss our results in the light of sex-specific selection that might drive sex-specific differences in pace-of-life and ultimately POLS. Electronic supplementary material The online version of this article (10.1007/s00265-018-2534-2) contains supplementary material, which is available to authorized users.
... Spiders also show a variety of strategies for dispersal (Blandenier, 2009;Coyle, 1983), foraging (Jackson, 1992; and mating (Jackson, 1992). Importantly, personality in spiders can also be studied in the context of behaviors that are common to these species, but are absent in vertebrates, such as precopulatory cannibalism (Arnqvist & Henriksson, 1997;Kralj-Fišer et al., 2013;Rabaneda-Bueno et al., 2008), and male emasculation during mating (Kralj-Fišer et al., 2011). However, what makes spiders an excellent model system for testing ecological and evolutionary hypotheses related to personality is that spiders have the unique physiological traits of both venom (Cooper et al., 2015; Zobel-Thropp ...
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Spiders are useful models for testing different hypotheses and methodologies relating to animal personality and behavioral syndromes because they show a range of behavioral types and unique physiological traits (e.g., silk and venom) that are not observed in many other animals. These characteristics allow for a unique understanding of how physiology, behavioral plasticity, and personality interact across different contexts to affect spider's individual fitness and survival. However, the relative effect of extrinsic factors on physiological traits (silk, venom, and neurohormones) that play an important role in spider survival, and which may impact personality, has received less attention. The goal of this review is to explore how the environment, experience, ontogeny, and physiology interact to affect spider personality types across different contexts. We highlight physiological traits, such as neurohormones, and unique spider biochemical weapons, namely silks and venoms, to explore how the use of these traits might, or might not, be constrained or limited by particular behavioral types. We argue that, to develop a comprehensive understanding of the flexibility and persistence of specific behavioral types in spiders, it is necessary to incorporate these underlying mechanisms into a synthesized whole, alongside other extrinsic and intrinsic factors. Few studies have explored the mechanisms driving the expression of personality in spiders, and what effects extrinsic and intrinsic factors (and their interactions) have on the expression of personalities. Physiological traits, particularly venom and silk, may play an important role in the expression of personalities and/or behavioral flexibility in spiders
... Indeed, genital mating plugs can reduce remating probability of females considerably [5,[71][72][73]. In some species sterile males survive and guard the female, in others they die during copulating with or without female intervention [66,74,75]. ...
Article
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’.
... Aggressiveness was measured as a score based on the frequency of what we deem to be Baggressive^behavior: approaching (score = 1), web-shaking (score = 1), attacking (score = 2), and chasing (score = 3) (e.g., Kralj-Fišer et al. 2011;. Aggressive behaviors were similar for all three species. ...
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Behavioral characteristics importantly shape an animals’ ability to adapt to changing conditions. The notion that behavioral flexibility facilitates exploitation of urban environments has received mixed support, but recent studies propose that between-individual differences are important. We leverage existing knowledge on three species of orb-web spider (Araneidae, Araneae) whose abundances differ along an urban–rural gradient to test predictions about between- and within-species/individual behavioral variation. We sampled Larinioides sclopetarius from their urban environment, and two species from suburban environments, Zygiella x-notata and Nuctenea umbratica. For each species, we quantified activity in a novel environment and within-species aggression. We analyzed between- and within-individual variation in behavior as well as their repeatability and correlations. As predicted, L. sclopetarius exhibited the highest activity in a novel environment and N. umbratica the lowest. Across all species, males were more aggressive than females and Z. x-notata was the most aggressive, followed by L. sclopetarius and N. umbratica. For all species, between-individual differences in activity and aggressiveness were repeatable; but the two behaviors were not correlated for any species. We next tested how group composition in relation to aggressiveness affects survival in high density conditions. Groups of Z. x-notata consisting of aggressive and tolerant spiders had higher survival rates than groups composed of only aggressive or tolerant individuals. Ultimately, we uncovered a complex pattern of behavioral variation between species as well as between and within individuals and we discuss the relative roles of this variation with respect to adapting to urban environments. Significance statement Urbanization has drastically changed biodiversity patterns. While the majority of species cope poorly with urban habitats, some species flourish in cities. Our understanding of behavioral characteristics that facilitate this exploitation, however, remains poor. We explored between and within species and individual variation in behaviors in ecologically similar orb-weaving spider species whose abundances differ along the urban–rural gradient. We detect both consistent individual differences and plasticity, in individuals’ response to a novel environment, suggesting that some degree of flexibility in reaction to novelty may be crucial in an urbanized environment. We also found that variation in aggressiveness type enables survival in high density conditions, conditions typical for urban populations. Urban populations thus exhibit a complex pattern of behavioral flexibility and behavioral stability.
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Sexual cannibalism by females and associated male behaviours may be driven by sexual conflict. One such male behaviour is the eunuch phenomenon in spiders, caused by total genital emasculation, which is a seemingly maladaptive behaviour. Here, we provide the first empirical testing of an adaptive hypothesis to explain this behaviour, the remote copulation, in a highly sexually cannibalistic orb-web spider Nephilengys malabarensis. We demonstrate that sperm transfer continues from the severed male organ into female genitals after the male has been detached from copula. Remote copulation increases the total amount of sperm transferred, and thus probably enhances paternity. We conclude that the mechanism may have evolved in response to sexual cannibalism and female-controlled short copulation duration.
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Males of sexually cannibalistic spiders commonly mutilate parts of their paired genitals (palps) during copulation, which may result in complete emasculation or the 'eunuch phenomenon'. In an orb-web nephilid spider, Nephilengys malabarensis, about 75 per cent of males fall victim to sexual cannibalism, and the surviving males become half-eunuchs (one palp emasculated) or full-eunuchs (both palps emasculated). While it has been shown that surviving eunuchs are better fighters compared with intact males when guarding the females with which they have mated, mechanisms behind eunuchs' superior fighting abilities are unknown. The previously proposed 'gloves-off' hypothesis, attributing eunuchs' enhanced locomotor endurance to the reduction in total body weight caused by genital mutilation, is plausible but has remained untested. Here, we tested the gloves-off hypothesis in N. malabarensis by comparing the time until exhaustion (i.e. endurance) of intact males with half- and full-eunuchs created experimentally. We found that by reducing body weight up to 4 per cent in half-eunuchs and 9 per cent in full-eunuchs through emasculation, endurance increases significantly in half-eunuchs (32%) and particularly strongly in full-eunuchs (80%). Our results corroborate the gloves-off hypothesis and further point towards the adaptive significance of male emasculation.
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Abstract Spiders of the tropical American colonial orb weaver Parawixia bistriata form a communal bivouac in daytime. At sunset, they leave the bivouac and construct individual, defended webs within a large, communally built scaffolding of permanent, thick silk lines between trees and bushes. Once spiders started building a web, they repelled other spiders walking on nearby scaffolding with a "bounce" behavior. In nearly all cases (93%), this resulted in the intruder leaving without a fight, akin to the "bourgeois strategy," in which residents win and intruders retreat without escalated contests. However, a few spiders (6.5%) did not build a web due to lack of available space. Webless spiders were less likely to leave when bounced (only 42% left) and instead attempted to "freeload," awaiting the capture of prey items in nearby webs. Our simple model shows that webless spiders should change their strategy from bourgeois to freeloading satellite as potential web sites become increasingly occupied.
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Immune defense is a key feature in the life history of organisms, expensive to maintain, highly regulated by individuals and exposed to physiological and evolutionary trade-offs. In chelicerates, relatively scarce are the studies that relate postcopulatory mechanisms and immune response parameters. This work makes an approximation to the female’s immunological consequences produced after the placement of a foreign body in the genitalia of three scorpions species, two species that normally receive genital plugs during mating (Urophonius brachycentrus and U. achalensis) and one that does not (Zabius fuscus). Here we performed the first morphological description of the natural plugs of the two Urophonius species. We described complex three zoned structure anchored to the female genital atrium and based on this information we placed implants in the genitalia (for eliciting the local immune response) of virgin females of the three species and measured the immune encapsulation response to this foreign body. We found a greater and heterogeneous response in different zones of the implants in the plug producing species. To corroborate the specificity of this immune response, we compared the local genital reaction with the triggered response at a systemic level by inserting implants into the female body cavity of U. brachycentrus and Zabius fuscus. We found that the systemic response did not differ between species and that only in the plug producing species the local response in the genitalia was higher than the systemic one. We also compared the total hemocyte load before and after the genital implantation to see if this parameter was compromised by the immunological challenge. We confirmed that in Urophonius species the presence of a strange body in the genitalia caused a decrease in the hemocyte load. Besides, we find correlations between the body weight and the immunological parameters, as well as between different immunological parameters with each other. Complementarily, we characterized the hemocytes of the three scorpion species for the first time. This comparative study can help to provide a wider framework of the immunological characteristics of the species, their differences and their relationship with the particular postcopulatory mechanism such as the genital plugs.
Article
The pantropical orb web spider family Nephilidae is known for the most extreme sexual size dimorphism among terrestrial animals. Numerous studies have made Nephilidae, particularly Nephila, a model lineage in evolutionary research. However, a poorly understood phylogeny of this lineage, relying only on morphology, has prevented thorough evolutionary syntheses of nephilid biology. We here use three nuclear and five mitochondrial genes for 28 out of 40 nephilid species to provide a more robust nephilid phylogeny and infer clade ages in a fossil-calibrated Bayesian framework. We complement the molecular analyses with total evidence analysis including morphology. All analyses find strong support for nephilid monophyly and exclusivity and the monophyly of the genera Herennia and Clitaetra. The inferred phylogenetic structure within Nephilidae is novel and conflicts with morphological phylogeny and traditional taxonomy. Nephilengys species fall into two clades, one with Australasian species (true Nephilengys) as sister to Herennia, and another with Afrotropical species (Nephilingis Kuntner new genus) as sister to a clade containing Clitaetra plus most currently described Nephila. Surprisingly, Nephila is also diphyletic, with true Nephila containing N. pilipes + N. constricta, and the second clade with all other species sister to Clitaetra; this "Nephila" clade is further split into an Australasian clade that also contains the South American N. sexpunctata and the Eurasian N. clavata, and an African clade that also contains the Panamerican N. clavipes. An approximately unbiased test constraining the monophyly of Nephilengys, Nephila, and Nephilinae (Nephila, Nephilengys, Herennia), respectively, rejected Nephilengys monophyly, but not that of Nephila and Nephilinae. Further data are therefore necessary to robustly test these two new, but inconclusive findings, and also to further test the precise placement of Nephilidae within the Araneoidea. For divergence date estimation we set the minimum bound for the stems of Nephilidae at 40 Ma and of Nephila at 16 Ma to accommodate Palaeonephila from Baltic amber and Dominican Nephila species, respectively. We also calibrated and dated the phylogeny under three different interpretations of the enigmatic 165 Ma fossil Nephila jurassica, which we suspected based on morphology to be misplaced. We found that by treating N. jurassica as stem Nephila or nephilid the inferred clade ages were vastly older, and the mitochondrial substitution rates much slower than expected from other empirical spider data. This suggests that N. jurassica is not a Nephila nor a nephilid, but possibly a stem orbicularian. The estimated nephilid ancestral age (40-60 Ma) rejects a Gondwanan origin of the family as most of the southern continents were already split at that time. The origin of the family is equally likely to be African, Asian, or Australasian, with a global biogeographic history dominated by dispersal events. A reinterpretation of web architecture evolution suggests that a partially arboricolous, asymmetric orb web with a retreat, as exemplified by both groups of "Nephilengys", is plesiomorphic in Nephilidae, that this architecture was modified into specialized arboricolous webs in Herennia and independently in Clitaetra, and that the web became aerial, gigantic, and golden independently in both "Nephila" groups. The new topology questions previously hypothesized gradual evolution of female size from small to large, and rather suggests a more mosaic evolutionary pattern with independent female size increases from medium to giant in both "Nephila" clades, and two reversals back to medium and small; combined with male size evolution, this pattern will help detect gross evolutionary events leading to extreme sexual size dimorphism, and its morphological and behavioral correlates.
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Within arachnids, genital plugs are morphologically diverse, and they can be formed by male, female or be a contribution of both sexes. Although several species of scorpions with genital plugs are known, the physiological effects on the female after being plugged have not been well studied yet. This work compares three scorpion species, two with genital plugs and one without. We first describe the genital plugs morphology of two Urophonius species. Second, through the placement of artificial genital plugs in the female genital atrium, we tested 1) whether there are interspecific differences in the immune encapsulation response on the artificial genital plug, 2) if there are an effect in the hemocyte load in the hemolymph, and 3) if individual’s immunological parameters and body weight are correlated. Additionally, we describe and quantify the hemocytes in these species. In both species of Urophonius , genital plugs were found covering the female genital aperture and blocking the genital atrium. The plugs consist of three zones that are distinct in morphology and coloration. We found different patterns of encapsulation and melanization on the artificial plug according to the species, with a greater and more specific response in females of plug producing species. Also, these species showed a decrease in the hemocyte load one month after the placement of the artificial plug, possibly due to the recirculation of the hemocytes into the genital area. In addition, correlations were found between the body weight and the immunological parameters, as well as between different immunological parameters. Our results suggest that females contribute to the formation of genital plugs by adding material and generating the darkening of the genital plugs in certain zones. This comparative study can help to provide a wider framework of different physiological consequences related to a particular postcopulatory mechanism such as the genital plugs.
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We investigated the mating biology of the previously unstudied central European spider Leviellus thorelli (Ausserer 1871) by staging laboratory mating trials using males and females of varying mating histories. Our aim was to seek common themes in sexual behaviors of the sexually size-monomorphic ''zygiellid'' spiders with their putatively close relatives, araneids and nephilids, which are relatively well studied with respect to sexual biology. We found L. thorelli mating biology to more closely resemble that of sexually size-monomorphic araneids than that of dimorphic nephilids. Unlike in nephilids with sexually conflicted adaptations, we found no evidence for genital damage or plugging in Leviellus Wunderlich 2004, although we found rare cases of half-eunuchs. We suggest that the mating system of L. thorelli spiders is determined by short female sexual attractiveness, reduced receptivity after mating and/or intensive mate guarding.
Chapter
In this chapter, the authors reflect on their development of a team-taught interdisciplinary course on “A Cultural and Evolutionary History of Sexuality.” Their respective areas of expertise are history of sexuality (Hellwarth) and evolutionary biology and animal behavior (Mumme). The authors encountered numerous challenges in teaching a course of this nature, including integrating multidisciplinary materials within the classroom, and helping students “make meaning” of interdisciplinary investigation. They also address institutional challenges, provide course materials (syllabus, examinations, and writing assignments), and reflect on some possible “best practices” in teaching such a course.
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In spiders, sperm transfer from the male to the female is indirect via secondary copulatory structures, the pedipalps. At the time of transfer the sperm are not mobile and the ejaculate needs to move through narrow male and female ducts to the female sperm storage organ. In addition, copulation duration can be very short, often limited to just a few seconds. Finally, sexual cannibalism and genital damage limits male life-time mating opportunities. These features of the reproductive biology in spiders are likely to result in sperm transfer constraints. Here we review the intrinsic and extrinsic sperm transfer limitations and conduct a meta-analysis on sperm transfer data from published data. Most of the information available relates to orb-web spiders, but our meta-analysis also includes non-orb-web spiders. Our review identifies some of the behavioural factors that have been shown to influence sperm transfer, and lists several morphological and physiological traits where we do not yet know how they might affect sperm transfer.
Book
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One hundred years after Darwin considered how sexual selection shapes the behavioral and morphological characteristics of males for acquiring mates, Parker realized that sexual selection continues after mating through sperm competition. Because females often mate with multiple males before producing offspring, selection favors adaptations that allow males to preempt sperm from previous males and to prevent their own sperm from preemption by future males. Since the 1970s, this area of research has seen exponential growth, and biologists now recognize sperm competition as an evolutionary force that drives such adaptations as mate guarding, genital morphology, and ejaculate chemistry across all animal taxa. The insects have been critical to this research, and they still offer the greatest potential to reveal fully the evolutionary consequences of sperm competition. This book analyzes and extends thirty years of theoretical and empirical work on insect sperm competition. It considers both male and female interests in sperm utilization and the sexual conflict that can arise when these differ. It covers the mechanics of sperm transfer and utilization, morphology, physiology, and behavior. Sperm competition is shown to have dramatic effects on adaptation in the context of reproduction as well as far-reaching ramifications on life-history evolution and speciation.
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The nephilid 'coin spiders' (Herennia Thorell) are known for their arboricolous ladder webs, extreme sexual size dimorphism and peculiar sexual biology. This paper revises Herennia taxonomy, systematics, biology and biogeography. The widespread Asian Herennia multipuncta (Doleschall) (= H. sampitana Karsch, new synonymy; = H. mollis Thorell, new synonymy) is synanthropic and invasive, whereas the other 10 species are narrowly distributed Australasian island endemics: H. agnarssoni, sp. nov. is known from Solomon Islands; H. deelemanae, sp. nov. from northern Borneo; H. etruscilla, sp. nov. from Java; H. gagamba, sp. nov. from the Philippines; H. jernej, sp. nov. from Sumatra; H. milleri, sp. nov. from New Britain; H. oz, sp. nov. from Australia; H. papuana Thorell from New Guinea; H. sonja, sp. nov. from Kalimantan and Sulawesi; and H. tone, sp. nov. from the Philippines. A phylogenetic analysis of seven species of Herennia, six nephilid species and 15 outgroup taxa scored for 190 morphological and behavioural characters resulted in 10 equally parsimonious trees supporting the monophyly of Nephilidae, Herennia, Nephila, Nephilengys and Clitaetra, but the sister-clade to the nephilids is ambiguous. Coin spiders do not fit well established biogeographic lines (Wallace, Huxley) dividing Asian and Australian biotas, but the newly drawn 'Herennia line' suggests an all-Australasian speciation in Herennia. To explain the peculiar male sexual behaviour (palpal mutilation and severance) known in Herennia and Nephilengys, three specific hypotheses based on morphological and behavioural data are proposed: (1) broken embolic conductors function as mating plugs; (2) bulb severance following mutilation is advantageous for the male to avoid hemolymph leakage; and (3) the eunuch protects his parental investment by fighting off rival males.
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Plugging of female genitals via male sexual mutilation is a common sexual repertoire in some nephilid spiders (Herennia, Nephila, Nephilengys), but the behavioral pathways leading to emasculation are poorly understood. Recent work suggests that copulating Herennia males damage their reproductive organs during copulation and then voluntarily, and stereotypically, remove their pedipalps to become eunuchs. Presumably, such emasculation increases agility allowing the male to better fend off rival males. However, through our observation of male antagonism in Nephilengys borbonica (Vinson 1863) in La Reunion (Indian Ocean), we discovered that genital severance involving the entire male palp is induced by a rival eunuch. Additionally, laboratory matings of the same species from Mayotte provide the first observations of female sexual cannibalism in this species, one such forceful copulation termination leading to emasculation of the entire palp. These novel behaviors suggest that mate plugging and the eunuch phenomenon are more plastic repertoires than hitherto thought, and thus our observations add to possible pathways leading to them. Based on our examination of 791 samples of Nephilengys spp. from museum collections and of a freshly collected representative sample of N. borbonica, we conclude that i) palpal severance is common (50% of males from the wild were eunuchs lacking both palps), but ii) the females (or perhaps subsequent males) must possess a mechanism for removing severed palps from the epigyna (none had a whole palpal bulb), leaving behind only partial, embolic plugs, and iii) the disparity between male palpal damage (50%) and visible mating plugs in females (21%) merits further research as the relative numbers of severed males and plugged females can offer insight into which sex may have the upper hand in an evolutionary arms race.
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The normal pattern of egg production in female dung flies consists of laying several successive egg batches of approximately equal numbers of eggs; although the number of eggs per batch is directly proportional to female size, the egg size remains constant.After a single insemination, a female can lay at least four batches without any drop in fertility. After a double mating in which the sperm from one male is labelled by exposure to 10 krad irradiation dose, the second male fertilizes 81·4 per cent of the eggs provided no further mating intervenes. After a double mating in which the second is interrupted, the competitiveness of the second mating can be shown to increase most steeply during the first half of copula. When females are mated immediately before laying (as in nature), matings labelled in various positions indicate that sperm from a given male can fertilize eggs in up to six successive batches, but that the percentage fertilization falls sharply as the number of batches (and hence number of subsequent matings) increases. With mated females, the last male to mate before oviposition fertilizes about 80 per cent of the succeeding batch irrespective of the number of previous matings.A model, which assumes that sperm from matings previous to the one before oviposition will compete for the remaining 20 per cent of the batch in the same proportionate relationship as they did for the previous batch, fits well with the experimental observations. Two patterns are therefore distinguishable for calculating the total egg gain of a male, depending on whether he mates with a virgin or non-virgin female. By assessing the chances of take-overs (where a second male ousts the male originally paired to a female) from field data, their effect is included in the model and the maximum, minimum, and probable average egg gains are calculated for males mating with females in different stages of their reproductive cycle. Egg gains with mated females could be increased by an increase in copula duration, but this would decrease the rate of capture of new females and also increase the probability of take-over. By using the model to assess the fertilization rate (eggs/min) achieved by males with varying copula durations in the present population and theoretical populations where the duration is both greater and smaller than at present, it can be predicted that selection would favour a value close to that observed. When the effect of virgin females is included, the fit is even better. Matings with post-oviposition females are much shorter than normal and the predicted optimum duration is very close to that observed.
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During copulation, male redback spiders (Latrodectus hasselti: Theridiidae) position themselves above the female's jaws. This apparent male complicity in sexual cannibalism is favored by sexual selection because cannibalized spiders receive two paternity advantages. First, cannibalized males copulated longer and fertilized more eggs than those that survived copulation. Second, females were more likely to reject subsequent suitors after consuming their first mate. These results represent empirical evidence for male copulatory suicide as an adaptive behavior.
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The remarkable bark spiders (genus Caerostris: Araneidae) are poorly known Old World tropical orb-weavers, whose diversity, currently at 11 species, is grossly underestimated. Most species build large webs at forest edges, clearings, and gardens, but in Madagascar, probably the hot spot of Caerostris diversity, at least one species occupies a unique ecological niche: casting its web across streams, rivers and lakes, so that the orb is suspended above water and attached to substrate on each riverbank via bridgelines up to 25 m. Here, we summarize current knowledge on Caerostris natural history, and specifically focus on the remarkable web architecture and biology of the newly described Caerostris darwini n. sp. Darwin's bark spider builds its web, a regular orb suspended above water, and maintains it with daily reinforcing of bridgelines and renewal of orb for many days. Web size ranged from 900–28,000 cm2, with the largest measured web of about 2.8 m2 being the largest orb ever measured, to our knowledge. With anchor lines capable of bridging over 25 m, it also builds the longest webs among all spiders—a unique form of web gigantism. We report on mass capture of ephemeropteran prey items in C. darwini n. sp. webs during a single day. Webs contained up to 32 mayflies that were subsequently wrapped en masse before the spider fed on them. We also provide the first evidence of kleptoparasitism in these webs both by other spiders (Argyrodinae) and by newly documented, undescribed symbiotic flies. Caerostris display extreme sexual size dimorphism with large females and small males, which is manifested in enigmatic sexual behaviors such as mate guarding, male-male aggressiveness, genital mutilation, mate plugging, and self castration. Caerostris is thus a promising candidate for evolutionary studies, and its diversity, biology, and phylogenetic relationships all deserve a closer scrutiny.
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Two to five days before sexual maturation, female sierra dome spiders (Linyphia litigiosa: Linyphiidae) undergo a transformation in their behavior toward males that visit their webs. During this latter part of their penultimate instar, females change from consistently positioning themselves far away from males to actively maintaining close proximity, reactions I call avoidant and associative behavior, respectively. Consistent associative behavior ceases after the female's first mating and thus is limited to soon-to-mature penultimate females. When a mate-seeking male fords an associative female, he attempts to guard her until she matures; this is often a multi-day affair. In contrast, males guard immature avoidant and mature mated females for only a single day. This dichotomy in male guarding times can be understood by the fact that associative behavior signals that the female will soon develop peak reproductive value. Upon completion of their final molt, 98% of females immediately mate with the current guarding male. Secondary suitors are not as likely to achieve mating. Moreover, first mates father 1.8 times more offspring, on average, than secondary mates. Whenever they meet on any female's web, males fight until one of the contestants withdraws. Fights typically are intensive, occasionally deadly, and often result in usurpation of the web by the newly arriving male. Larger males win more fights, but other qualities (e.g., vigor and persistence) appear to be important when contestants differ by less than 10–20% in body weight. Prolonged (i.e., multi-day) guarding of associative females enhances the intrasexual selection process by ensuring that every male that arrives at the web finds it already guarded. Therefore every male that finds the web becomes a participant in a series of male-male conflicts and web usurpations which span the period between the resident female's commencement of associative behavior and her sexual maturation. Since unforced male departures from the webs of associative females are rare, victors are retained on the web until they themselves lose a fight. This facilitates a steady increase in the fighting ability of sequential guards throughout the associative period, up until female maturation and mating. On my study site, first mates represented the final winners in a combative sorting process based on a minimum average of 2 fights; they were heavier and larger than secondary mates and randomly sampled males. The combination of (1) associative behavior by nearly mature females, (2) high mating propensity of newly mature females, and (3) first male sperm priority, constitutes a system whereby females enhance male-male competition and boost the expected fighting prowess of the principal sire of their progeny. Since males appear to make no material contribution toward progeny, the female's behavior probably functions to improve the genetic constitution of the offspring. In addition, the timing of associative behavior may limit prolonged guarding by food-stealing males to a period (1) encompassing the female's pre-molt fast and (2) before the heavy yolking of eggs, thereby ameliorating the nutritional costs of intrasexual selection.
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Sperm competition is a potent driving force in evolution leading to a remarkable variety of male adaptations that prevent or reduce fertilization by rivals. An extraordinary defensive strategy against sperm competition has evolved in a number of web spiders where males break off parts of their paired genitalia in order to obstruct the copulatory openings of females (mating plug). A recent comparative analysis on the family level reports that genital damage is most frequent in species with sexual cannibalism although, as yet, a functional association between sexual cannibalism and genital damage has not been found. Using the moderately sexually cannibalistic orb-web spider Argiope lobata, we show for the first time that males cannibalized during their first copulation damaged their pedipalps with significantly higher probability (74%) than males that escaped (15%). Of all males that damaged their genitalia, 44% were able to place a genital fragment inside the copulatory opening of the female, resulting in a relatively low total plugging rate of 14%. Successful obstruction of the female copulatory opening reduced the share of paternity of subsequent males (P 2 = 0.06%), thus, indicating that genital damage may have evolved as a response to sperm competition in this species as well. However, the low incidence of successful plugging and the strong relationship between sexual cannibalism and genital damage suggest that apart from paternity protection, the nature of genital damage in A. lobata is further shaped by sexual conflict or cryptic female choice.
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To understand the evolution of mating systems, we need to consider why reproductive strategies differ between species in the way they do. For example, males in most mammals appear entirely specialised on mating with many females, whereas males in many birds also invest in offspring quality by providing paternal care. Alternatively or additionally, males may invest in enhancing their paternity share in any mating they get. Taken to the extreme, this may result in males investing maximally in gaining paternity with one or two females only, in the absence of paternal care. Mating systems with monogynous (or bigynous) males and polyandrous females are taxonomically widespread but relatively rare overall. In spiders, however, low male mating frequencies have evolved several times independently and are associated with remarkable adaptations that include sexual cannibalism and genital damage. In the first part of this chapter, we describe the mating strategies, and the associated costs and benefits of sexual cannibalism and genital damage, of selected spider species that represent independent evolutionary origins of these traits. We then introduce models that investigate the evolution of mating systems with low male mating frequencies. The models predict that a male-biased sex ratio is required for monogyny to evolve. We outline how such a sex ratio bias may have arisen in concert with female-biased sexual size dimorphism. Finally, we discuss monogyny in the light of sexual conflict theory.
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The morphologically specialized queen caste has been lost in various ponerine ants, and mated workers (‘gamergates’) reproduce instead of queens. Unlike previous reports in the literature, we found only one gamergate in each colony ofDinoponera quadriceps. We documented monogyny by dissecting ovaries and spermathecae in 914 workers from 15 colonies, and by observing mating in the laboratory. In colonies without a gamergate, aggressive interactions among some of the unmated nestmates led to the behavioural differentiation of a top-ranking worker (‘alpha’), which laid almost all the eggs. Only the alpha went outside the nest at night, and mated if foreign males were present (N=11 tests), thus becoming a gamergate. The alpha was sexually attractive even when her ovaries were not yet active. After intromission, the male remained linked to the alpha while she severed the end of his abdomen. Pieces of the male genitalia remained attached to her genital tract, and she removed them after 30±18 min (X±sdN=9). We interpret this to be a mating plug, preventing other males from fathering her offspring. None of these newly inseminated gamergates continued to go outside the nest, and, when tested, they never re-mated (N=4). Thus, gamergates ofD. quadricepsprobably mate only once. In queenless ant species, comparative evidence indicates that worker mating is often regulated in monogynous species, while unrestricted mating of young individuals is typical of polygynous species (oviposition is regulated subsequently). Furthermore, the occurrence of either monogyny or polygyny influences the mating strategies of males, and mating plugs have been reported only in some monogynous species.
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Once thought to be energetically cheap and easy to produce, empirical work has shown that sperm is a costly and limited resource for males. In some spider species, there is behavioral evidence that sperm are permanently depleted after a single mating. This extreme degree of mating investment appears to co-occur with other reproductive strategies common to spiders, e.g. genital mutilation and sexual cannibalism. Here we corroborate that sperm depletion in the golden orb-web spider Nephila clavipes is permanent by uncovering its mechanistic basis using light and electron microscopy. In addition, we use a phylogeny-based statistical analysis to test the evolutionary relationships between permanent sperm depletion (PSD) and other reproductive strategies in spiders. Male testes do not produce sperm during adulthood, which is unusual in spiders. Instead, spermatogenesis is nearly synchronous and ends before the maturation molt. Testis size decreases as males approach their maturation molt and reaches its lowest point after sperm is transferred into the male copulatory organs (pedipalps). As a consequence, the amount of sperm available to males for mating is limited to the sperm contained in the pedipalps, and once it is used, males lose their ability to fertilize eggs. Our data suggest that PSD has evolved independently at least three times within web-building spiders and is significantly correlated with the evolution of other mating strategies that limit males to monogamy, including genital mutilation and sexual cannibalism. We conclude that PSD may be an energy-saving adaptation in species where males are limited to monogamy. This could be particularly important in web-building spiders where extreme sexual size dimorphism results in large, sedentary females and small, searching males who rarely feed as adults and are vulnerable to starvation. Future work will explore possible energetic benefits and the evolutionary lability of PSD relative to other mate-limiting reproductive behaviors.
Article
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The morphology of male genitalia often suggests functions besides sperm transfer that may have evolved under natural or sexual selection. In several species of sexually cannibalistic spiders, males damage their paired genitalia during mating, limiting them to one copulation per pedipalp. Using a triple-mating experiment, we tested if genital damage in the orb-web spider Argiope bruennichi increases male fitness either through facilitating his escape from an aggressive female or by obstructing the female's insemination ducts against future copulation attempts from other males. We found no survival advantage for males damaging their pedipalps; however, copulations into a previously used insemination duct were significantly shorter when the previous male had left parts of his genitalia inside the insemination duct. Because copulation duration determines paternity in this species, our result suggests that male genital damage in A. bruennichi is sexually selected. By breaking off parts of their intromittent organs inside a virgin female, males can reduce sperm competition and thereby increase their paternity success. Copyright 2007.
Article
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Female multiple mating selects for male adaptations that maximize fertilization success in a context of sperm competition. While male mating strategies usually reflect a trade-off between present and future reproduction, this trade-off is largely removed in systems where the maximum number of matings for males is very small. Selection may then favor extreme mechanisms of paternity protection that amount to a maximal investment in a single mating. Males in several arthropod taxa break off parts of their copulatory organs during mating, and it has frequently been suggested that mutilated males can thus secure their paternity. Nevertheless, such a mechanism has rarely been confirmed directly. Here we study the golden orb spider Nephila fenestrata, which has a mating system with potentially cannibalistic, polyandrous females, and males that are often functionally sterile after mating with one female only. We show that males in this species can indeed protect their paternity by obstructing the female's genital openings with fragments of their copulatory organs.
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Mating strategies are to a large degree shaped by conflicts between the sexes, causing a rapid antagonistic coevolution of traits involved in reproduction. The view that sexual cannibalism represents a form of sexual conflict leads to the prediction of male traits that facilitate escape from cannibalistic females. A variety of traits have been suggested to serve this function in spiders, where sexual cannibalism is comparatively common. Empirical evidence, however, is virtually absent. Here we show experimentally that opportunistic mating with feeding females, which has been reported from several species of orb-weaving spiders, greatly reduces the risk of cannibalism and injury for males in the spider Nephila fenestrata. This has direct consequences for a male's fertilization success because surviving males can reduce the female's remating probability by guarding her against rivals. Although copulation with previously mated females sometimes appears to be mechanically impossible, second males that do copulate can expect to fertilize on average 64% of a female's eggs. Our results support the view that opportunistic mating may have evolved as a male tactic in a context of sexual conflict over sexual cannibalism. Copyright 2005.
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More than 41,000 spider species are known with about 400-500 added each year, but for some well-known groups, such as the giant golden orbweavers, Nephila, the last valid described species dates from the 19(th) century. Nephila are renowned for being the largest web-spinning spiders, making the largest orb webs, and are model organisms for the study of extreme sexual size dimorphism (SSD) and sexual biology. Here, we report on the discovery of a new, giant Nephila species from Africa and Madagascar, and review size evolution and SSD in Nephilidae. We formally describe N. komaci sp. nov., the largest web spinning species known, and place the species in phylogenetic context to reconstruct the evolution of mean size (via squared change parsimony). We then test female and male mean size correlation using phylogenetically independent contrasts, and simulate nephilid body size evolution using Monte Carlo statistics. Nephila females increased in size almost monotonically to establish a mostly African clade of true giants. In contrast, Nephila male size is effectively decoupled and hovers around values roughly one fifth of female size. Although N. komaci females are the largest Nephila yet discovered, the males are also large and thus their SSD is not exceptional.
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Low female mating frequencies often appear to be cases of direct male induction that can oppose female interests. Mating plugs are most obvious means leading to low degrees of multiple mating in females. In spiders, mating plugs are formed by a variety of amorphous materials, by the breakage of the male sperm transferring organ, or by the whole male that functions as a mating barrier. Our compilation of the available information on the presence of the various types of mating plugs suggests that plugs predominantly occur in entelegyne spiders. In this group, plugs do not interfere with oviposition since separate openings for insemination and oviposition are present. In contrast, mating plugs seem to be rare in haplogyne spiders that do not possess separate openings. The available experimental studies on the function of the different types of plugs suggest that plugs can be considered as male adaptations to avoid sperm competition. However, females in some cases were shown to have evolved means to prevent or control male manipulation or may selectively favour plug production in specific males, an aspect which has largely been neglected. In order to understand plug evolution and function we need to explore the morphological, behavioural and biochemical aspects involved and extend our approach to interactions between the sexes.
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Genital morphology is informative phylogenetically and strongly selected sexually. We use a recent species-level phylogeny of nephilid spiders to synthesize phylogenetic patterns in nephilid genital evolution that document generalized conflict between male and female interests. Specifically, we test the intersexual coevolution hypothesis by defining gender-specific indices of genital complexity that summarize all relevant and phylogenetically informative traits. We then use independent contrasts to show that male and female genital complexity indices correlate significantly and positively across the phylogeny rather than among sympatric sister species, as predicted by reproductive character displacement. In effect, as females respond to selection for fecundity-driven fitness via giantism and polyandry (perhaps responding to male-biased effective sex ratios), male mechanisms evolve to monopolize females (male monogamy) via opportunistic mating, pre- and postcopulatory mate guarding, and/or plugging of female genitalia to exclude subsequent suitors. In males morphological symptoms of these phenomena range from self-mutilated genitalia to total castration. Although the results are compatible with both recently favored sexual selection hypotheses, sexually antagonistic coevolution, and cryptic female choice, the evidence of strong intersexual conflict and genitalic damage in both sexes is more easily explained as sexually antagonistic coevolution due to an evolutionary arms race.
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Sexual conflict theory predicts an antagonistic coevolution, with each sex evolving adaptations and counter-adaptations to overcome a temporary dominance of the other sex over the control of paternity. Polyandry allows sexual selection to operate after mating has commenced, with male and female interests competing for control of fertilization. There are numerous examples of male control of paternity, but few studies have unambiguously revealed female control. Attributing variance in paternity to females is often difficult since male and female influences cannot be separated unambiguously. However, we show that polyandrous female orb-web spiders Argiope keserlingi (Arancidae) control the paternity of their offspring by adjusting the timing of sexual cannibalism. Our experiments reveal that females copulating with relatively smaller males delay sexual cannibalism, thereby prolonging the duration of copulation, and that these males consequently fertilize relatively more eggs.
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Males of some cannibalistic species of spiders and insects appear to sacrifice themselves by allowing the female to eat them, and the adaptive significance of such drastic terminal reproductive investment has recently been demonstrated for a spider. Typically, the female has to kill the male, but it has been suggested that males of some species in the cannibalistic orb-weaving spider genus Argiope may die in copula without female 'collaboration'. Here, we provide the first experimental evidence to our knowledge of programmed sudden death after onset of copulation in males of the spider Argiope aurantia. Our observations reveal that males invariably die during the insertion of their second pedipalp, regardless of whether they mate with newly moulted, defenceless females or with older mature females that often attack them. We determined experimentally that the death of males is triggered immediately upon insertion of the second palp, when males become unresponsive, and heartbeat ceases within minutes of insertion. We discuss the possible adaptive significance of programmed death during copulation, and argue that male death has evolved in a context other than sexual cannibalism.
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One potential consequence of sexual size dimorphism is conflict among characters. For example, a structure evolved for reproduction can impair performance during other activities (e.g., locomotion). Here we provide quantitative evidence for an animal overcoming an evolutionary conflict generated by differential scaling and sexual size dimorphism by obligatorily removing an undamaged reproductive organ, and thus dramatically enhancing its locomotor performance. The spider genus Tidarren (Araneae, Theridiidae) is interesting because, within several species presenting extreme sexual size dimorphism (males representing approximately 1% of the total mass of the female), males voluntarily remove one of their two disproportionately large pedipalps (modified copulatory organs; a single one represents approximately 10% of the body mass in an adult) before achieving sexual maturity. Whether the left or right pedipalp is removed appears to be random. Previous researchers have hypothesized that pedipalp removal might enhance locomotor performance, a prediction that has remained untested. We found that, for male Tidarren sisyphoides, maximum speed increased (44%) significantly and endurance increased (63%) significantly after pedipalp removal. Furthermore, spiders with one pedipalp moved approximately 300% greater distances before exhaustion and had a higher survival after exertion than those with two pedipalps. Removal of the pedipalp may have evolved in male Tidarren because of enhanced abilities to search for females (higher endurance and survival after exertion) and to out-compete rival males on the female's web (higher maximum speed). Our data also highlight how the evolution of conflicts can result in the evolution of a novel behavior.
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Pair formation in social insects mostly happens early in adult life and away from the social colony context, which precludes promiscuity in the usual sense. Termite males have continuous sperm production, but males of social Hymenoptera have fixed complements of sperm, except for a few species that mate before female dispersal and show male-fighting and lifelong sperm production. We develop an evolutionary framework for testing sexual selection and sperm competition theory across the advanced eusocial insects (ants, wasps, bees, termites) and highlight two areas related to premating sexual selection (sexual dimorphism and male mate number) that have remained understudied and in which considerable progress can be achieved with relatively simple approaches. We also infer that mating plugs may be relatively common, and we review further possibilities for postmating sexual selection, which gradually become less likely in termite evolution, but for which eusocial Hymenoptera provide unusual opportunities because they have clonal ejaculates and store viable sperm for up to several decades.
Chapter
The chapter focuses on Polyandry, which sets the stage for sperm competition, and may provide female spiders with both material and genetic benefits. The material benefits include a reduction in the costs of male harassment and, perhaps, an increase in fecundity through the provision of nuptial gifts, including the body of the male. The genetic benefits, which are modified by the patterns of sperm precedence, are less apparent in females among species with a predominantly first-male sperm priority. However, for male spiders, most of the opportunities for securing paternity appear to be related to the timing of mating, physically guarding females from rival males and blocking the genital region of the female with a plug, or increasing the duration of copulation. Moreover, the latter reduces female receptivity and increases fertilization success in competition with other males, although the mechanisms remain unknown. Therefore, the studies of sperm competition also benefit by examining precedence patterns involving more than two males. The clear sexual dimorphism and often elaborate courtship behavior of many cursorial spiders provide a rich seam of model systems to investigate the evolutionary significance of both overt and cryptic female choice.
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Male bowl and doily spiders (Frontinella pyramitela: Linyphiidae) engage in dangerous fights over access to females. Relatively smaller individuals are more at risk of fatal injury than their larger opponents. Males assess relative fighting ability during contests: smaller individuals tend to give up quickly. Fights occur between a male with information about the value of the contested female (number of fertilizable eggs) and an intruding male with less information. In this paper, a sequential assessment game (a game theory model of fighting behavior) is adapted to male combat in the bowl and doily spider to attempt a quantitative test. The model makes predictions about fight duration, probability of winning, and the occurrence of fatalities as a function of resource value and size asymmetry. Comparison with empirical data from staged contests yields a generally good quantitative agreement with the predictions. A few deviations are also noted.
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Uniquely among spiders, males of two cobweb spider (Theridiidae) genera, Tidarren Chamberlin & Ivie, 1934 and Echinotheridion Levi, 1963, voluntarily amputate one of their secondary sexual organs ( the pedipalpi, modified as sperm transfer organs) before their last molt and thus have only one palp as adults. This is the first step in a fascinating sexual biology observed in both genera, which is marked by sexual dimorphism males are tiny compared with females - and usually involves both emasculation and sexual cannibalism. To study the evolution of these striking traits it is essential to understand the phylogenetic relationship of these genera. Both morphological and molecular data place Tidarren in the subfamily Theridiinae. However, Echinotheridion has not been placed phylogenetically to date owing to rarity of specimens, and difficulty of interpreting the highly autapomorphic palpal organ, the main source of morphological characters. Here, the phylogenetic position of Echinotheridion is inferred using fragments of three nuclear (Histone 3, 18S rDNA, and 28S rDNA) and two mitochondrial (16S rDNA and COI) loci. Each matrix separately, and a combined matrix, were analysed using parsimony with gaps either treated as missing data, or as 5th state, and with Bayesian methods. Although all genes agree that Tidarren and Echinotheridion are closely related, perhaps surprisingly, none of the analyses supported their sister relationship. The sister relationship was ambiguously supported in a preliminary morphological analysis, whereas combined molecular and morphological data refuted it. This implies a more complex evolutionary history of male sexual organ removal and other bizarre sexual biology of Tidarren and Echinotheridion than previously envisioned. Many of the analyses are equally consistent with two hypotheses: a single origin, followed by a secondary loss; or independent evolution of this behaviour in the two genera. However, based on the combined molecular Bayesian phylogeny, and some of the preliminary 'total evidence' analyses, the latter hypothesis is better supported.
Article
Male (Fontinella pyramitela Linyphiidae) engage in dangerous fights over access to females. Males assess relative fighting ability during contests: smaller individuals tend to give up quickly. Fights occur between a male with information about the value of the contested female (number of fertilizable eggs) and an intruding male with less information. A sequential assessment game (a game theory model of fighting behavior) is adapted to male combat to attempt a quantitative test. The model makes predictions about fight duration, probability of winning, and the occurrence of fatalities as a function of resource value and size asymmetry. -from Authors
Article
Males of Tidarren cuneolatum (Tullgren, 1910) amputate one of their palps a few hours after the penultimate moult, like T. sisyphoides (Walckenaer, 1841) from the USA (Branch, 1942). Hence adult males, which are minute, have only one palp, either left or right randomly. This palpal organ is not oversized, when compared with other small spiders. During courtship females are unusually active, signalling receptivity by continuous twanging with legs II. Males construct a mating thread. Copulation involves one insertion, which lasts ca 4 min. Thus, only one receptaculum is inseminated during copulation. With the advance of insertion the male's prosoma becomes shrunken. Copulation regularly ends in mate consumption. In copulation with a virgin female the palp was inserted contralaterally. Females taken in the field had both receptacula filled with sperm and therefore were polyandrous. Re-mating was also observed in the laboratory. Remarkably the second male performed an ipsilateral insertion, if it possessed the same palp as the previous male. Probably the virgin receptaculum was recognized. Postembryonic development is rapid in males, which moult three times and mature ca 41 days after hatching from the cocoon. Females need four or five moults and ca 69 days to reach maturity and then survive ca 2-4 months.
Article
Tidarren argo sp. nov. is described from Yemen. As in its congeners, the male amputates one of his palps before maturation and enters his adult life with one palp only. The new species is shown to adopt exceptional copulatory behaviour. As soon as the male achieves genitalia coupling with his palp, the palp is torn off by the female. The separated gonopod remains attached to the female's epigynum for c. 4 h and apparently continues to function independently. Furthermore, it serves as a mating plug. In the meantime the female feeds on the palpless male. Emasculation synchronizes sexual cannibalism and sperm transfer, and may lengthen the interval between copulations. This unique mating behaviour probably allows continuation of insemination by the dismembered palp and is reported for the first time.
Article
I . Intrasexual seiection may have played a large part in insects in the evolution of copulation with internal fertilization from indirect spermatophore-transferring acts. 2. ‘Sperm competition’ may be defined as the competition within a single female between the sperm from two or more males over the fertilization of the ova. 3. There is considerable evidence from sperm-marking experiments that sperm competition is very common in insects as a result of multiple matings. Insects so far examined show that sperm from all inseminations can be used (to a varying extent) in the fertilization of subsequent offspring, but mating does not always result in successful insemination. In most cases (so far examined), the last male to mate tends to predominate in fertilizing the offspring. 4.Insects are preadapted to sustaining a very high level of sperm competition, compared with several other animal groups. The main preadaptations may be sum- marized as follows: (a)Females often mate several times within the duration of effec- tiveness of a given ejaculate. There may be several reasons for this. Though most usually females are unreceptive for some time after mating, some species appear ‘promiscuous’. Unreceptive females are also sometimes raped. Male persistence is sometimes prolonged, so that full female receptivity is advantageous. It is advan- tageous for a female to become receptive again when fertility first begins to decline; this is not when all the first ejaculate is used up. (b) Female insects typically possess specialized sperm storage organs in which sperm can be maintained in a viable condi- tion for a very long time, often until the death of the female. (c) Extremely efficient utilization of stored sperm at the time of fertilization appears to be an insect charac- teristic. In Drosophila the number of stored sperm virtually equals the possible number of fertilizations. Overlapping of effective ejaculates is therefore high. Second insemina- tions almost invariably reduce the fertility which would have been experienced by the first male to mate. 5. It is argued that this preadaptation to a very high level of sperm competition has led to intense intrasexual selective pressures on the male. In response to these pressures, two main lines of sexually selected adaptation are predicted: (a) towards mechanisms by which a male inseminates a female in such a way as to achieve pre- cedence over previously stored sperm and (b) accentuated by the above adaptation, mechanisms will evolve by which a male which mates with a given female will reduce the occurrence or success of subsequent inseminations with that female. These two forms of adaptation are diametrically opposed ; a high selective advantage would be gained by a male which superseded previous sperm and prevented any subsequent successful inseminations. 6. Several adaptations in male insects can be interpreted in the light of the above predictions, though many of these may also have other adaptive values through natural selection. The adaptation which evolves is not necessarily that which yields the maxi- mum possible egg gain to a given male (i.e. total sperm precedence), but that which results in the highest fertilization rate. 7. Sperm precedence is achieved in Drosophila by sperm displacement, where sperm from a second male predominate over previously stored sperm by directly displacing them from the sperm stores. Sperm displacement may occur in many insects. 8. Several behavioural and physiological adaptations of male insects may help to reduce the effectiveness, or occurrence of second inseminations of the same female by other males. These include : ( a ) Mating plugs (sphragis, spermat0phragmata)-male accessory gland secretions, usually transferred after insemination, which coagulate and form plugs within the female genital tract. Plugs may often serve to ‘guard’ the female until unreceptivity is initiated. In many insects, agents in the seminal fluid or male accessory gland secretions induce unreceptivity in the female. (b)Prolonged copu- lation-sometimes copulation takes much longer than seems necessary merely to transfer the sperm. This may have the same functions as that of a mating plug, but renders the male unfree to search for further females. (c) Passive phases (amplexus, tandem behaviour)-stages of the male’s reproductive behaviour during which he remains mounted on or otherwise attached to the female but without true genital contact between the two sexes. Postcopulatory passive phases sometimes serve to guard the female during oviposition where high densities of searching males are pre- valent. The postcopulatory passive phase of Scatophaga has an extremely high intra- sexual selective advantage which exceeds any apparent natural selective advantage by two orders of magnitude. (d)Non-contact guarding phases-reproductive behaviour phases during which the male remains close but not in contact with the female, guard- ing her from other males. Postcopulatory non-contact guarding phases appear to have the same selective advantage as postcopulatory passive phases. 9. Mechanisms to avoid ‘take-over ’ during copulation, passive, and non-contact guarding phases also serve to reduce sperm competition. These include increased efficiency of grasping apparatus, specialized rejection reactions which serve to dispel or ‘trick’ the recognition mechanism of the attacker, and emigrations from the site of highest probability of ‘take-over ’. There is quantitative evidence in Scatophaga that the emigration threshold of copulating males is determined by this form of intrasexual selective pressure. 10.Precopulatory passive phases may serve mainly to keep the sexes together until the female becomes receptive, but share several features in common with postcopula- tory passive phases. Territoriality of male insects may have arisen primarily through sexual selection as a mechanism by which a male guards an area into which a female is most likely to enter.
Article
The Pantropical spider clade Nephilidae is famous for its extreme sexual size dimorphism, for constructing the largest orb-webs known, and for unusual sexual behaviors, which include emasculation and extreme polygamy. We synthesize the available data for the genera Nephila, Nephilengys, Herennia and Clitaetra to produce the first species level phylogeny of the family. We score 231 characters (197 morphological, 34 behavioral) for 61 taxa: 32 of the 37 known nephilid species plus two Phonognatha and one Deliochus species, 10 tetragnathid outgroups, nine araneids, and one genus each of Nesticidae, Theridiidae, Theridiosomatidae, Linyphiidae, Pimoidae, Uloboridae and Deinopidae. Four most parsimonious trees resulted, among which successive weighting preferred one ingroup topology. Neither an analysis of an alternative data set based on different morphological interpretations, nor separate analyses of morphology and behavior are superior to the total evidence analysis, which we therefore propose as the working hypothesis of nephilid relationships, and the basis for classification. Ingroup generic relationships are (Clitaetra (Herennia (Nephila, Nephilengys))). Deliochus and Phonognatha group with Araneidae rather than Nephilidae. Nephilidae is sister to all other araneoids (contra most recent literature). Ethological data, although difficult to obtain and thus frequently missing for rare taxa, are phylogenetically informative. We explore the evolution of selected morphological and behavioral characters, discuss and redefine the homology of palpal sclerites, disprove semientelegyny in spiders, trace the newly interpreted evolution of the orb web, and show that nephilid genital morphologies coevolve with sexual behaviors and extreme sexual size dimorphism. Phylogenetic interpretations of behavior suggest new insights into spider biology and avenues for future research.© The Willi Hennig Society 2007.
Article
Mating systems are frequently shaped by conflicts over reproductive interests between males and females. Sexual cannibalism can be an especially dramatic manifestation of such conflicts. However, the resolutions of this conflict differ among sexually cannibalistic spider species. Cannibalism may be in the interest of both sexes when females consume males as a foraging decision to improve fecundity and/or males sacrifice their bodies to increase fertilization success. In other species, females exert se- quential choice of partner by selectively terminating copulation through cannibalism while males fail to obtain a paternity advantage. Here, we investigate the adaptive value of cannibalism in the orb-web spider Nephila plumipes where 60% of males do not survive copulation. Virgin females in poor condition are more frequently cannibalistic and more likely to kill large males, but the frequency of cannibalism among mated females is not influenced by these factors. Instead, males that mate with mated females increase their fertilization success by being cannibalized. Cannibalized males generally mate for longer, but longer copulations correspond with increased paternity only in mated females. The amount of sperm from particular males that a female stored was not influenced by any of the measured variables. The number of sperm stored was not related to paternity, nor was there any detectable reduction in sperm number after females had reproduced. Our data suggest that the conflict between the sexes differs between virgin and mated females. Females should always cannibalize a male, but males only gain from cannibalism when mating with mated females, not when mating with virgin females. Interestingly, the frequencies of cannibalism are not different in matings with virgin or mated females. Key words: cannibalism, foraging, mating, paternity advantage. (Behav Ecol 12:547-552 (2001))
Article
Theory predicts that the outcome and escalation level of animal contests will reflect the contestants' expected payoffs as well as their relative fighting ability. Although an individual's future prospects of reproduction are expected to be critical for the risk of injury that it should accept when contesting a given resource, previous empirical work has ignored the possibility that this factor may differ between individuals. We studied male–male contests in the golden orb spider Nephila fenestrata, where the potential for future reproduction is much lower in mated than virgin males. Males typically mate with only one female in their lifetime, and are subsequently functionally sterile because of damage to their mating organs. Nevertheless, they guard their mate against rival males. This leads to a situation where mated males, having nothing to lose, are predicted to fight with maximal force when facing an intruder. In line with this prediction, mated males usually won contests against virgin males, even when the latter were physically superior. Staged contests between mated males resulted in high frequencies of injury. Our results show that constraints on future reproduction can be critical for understanding a species' contest behaviour.
Article
The evolution of sexual cannibalism has been modelled as both an adaptive and nonadaptive female strategy. Recent evidence from several species suggests a connection between female foraging and sexual cannibalism, but the precise benefits for females have remained obscure. Here, we investigate the difference between cannibalistic and noncannibalistic female Nephila plumipes by removing the potential nutritional benefit of cannibalism. Courting and mating males that were killed by a female were immediately removed so that the female could not consume them. Nevertheless, cannibalistic females gained more mass from maturation to oviposition and produced larger first clutches than noncannibalistic females, although cannibalistic females matured at a smaller size and mass than noncannibalistic females. In juvenile instars, mass gain was generally smaller in females that moulted in a good condition but intermoult intervals were shorter. However, the time from maturity to oviposition was not shorter in females that matured in a good condition. Male behaviour did not differ according to the risk of cannibalism. We suggest that sexual cannibalism in N. plumipes is a side-effect of an increased foraging vigour of females that matured at a smaller size and body mass. Selection pressure on males to avoid cannibalism may be weak because of limited mating opportunities.
Article
Abstract The nephilid genus Nephilengys, known for its synanthropic habits, large webs with a retreat and the extreme sexual size dimorphism, is revised. Of the twenty-three available names, only four species with a globally allopatric distribution are recognized, illustrated and described from both sexes: N. cruentata (Fabricius, 1775) inhabits tropical Africa and South America, where it has probably been introduced; N. borbonica (Vinson, 1863) is found on Madagascar, Comoros, Seychelles and the Mascarene Islands; N. malabarensis (Walckenaer, 1842) ranges from India and Sri Lanka to China, Japan and eastern Indonesia; N. papuana Thorell, 1881 stat.n. is known from New Guinea and tropical Australia. Nephila instigans Butler, 1876 is the proposed syn.n. of N. borbonica; N. borbonica livida Vinson, 1863 is syn.n. of N. borbonica; N. niahensis Deeleman-Reinhold, 1989 is syn.n. of N. malabarensis; N. rainbowi Hogg, 1899 is syn.n. of N. papuana. N. kenmorei Barrion & Litsinger, 1995, here proposed as a nomen dubium, is an araneid. Nephilengys biology is reviewed and its anatomy summarized for use in a phylogenetic analysis of 197 characters scored for all Nephilengys, selected nephilid species and non-nephilid outgroups. Two new clades are circumscribed, the ‘cruentata species group’ (with N. cruentata and N. borbonica) and the ‘malabarensis species group’ (with N. malabarensis and N. papuana).
Article
In some spiders, a discrete portion of the male's copulatory organ (the apical sclerite) breaks off during copulation and remains in the female's reproductive tract. Apical sclerites may prevent insemination by rivals (sperm competition), stimulate females to favourably bias paternity (cryptic choice) or breakage may reflect sexual conflict over copulation duration with little direct effect on paternity. It has been assumed that any benefits of organ breakage are balanced by a large cost (male sterility) in species where males could otherwise mate multiply, but this has never been experimentally tested. We examined these ideas in the Australian redback spider (Latrodectus hasselti Thorell 1870, Araneae: Theridiidae), a species where males are functionally sterile after one normal mating. We experimentally removed sclerites and found males were able to mate, had similar copulation durations and transferred similar numbers of sperm as males with intact sclerites. Benefits of organ breakage were examined by forcing intact, rival males to inseminate the same or opposite reproductive tracts (female have paired, independent tracts in this taxon) and assessing paternity as a function of sclerite location. As predicted, apical sclerites were typically deposited at the entrance to the female's sperm storage organ, where they could physically block insemination by rivals. First male precedence was common when males inseminated the same tract and deposited sclerites at the entrance to the spermatheca, but not when sclerites were found elsewhere in the tract, or when rivals inseminated opposite tracts (where physically blocking rivals was impossible). Our data show that, in redbacks, copulatory organ breakage is not a side-effect of sexual conflict, is unlikely to be a cue for cryptic female choice, but allows males to avoid sperm competition. Moreover, copulatory organ damage can have minimal reproductive cost for males, so assumptions of sterility after organ breakage are unjustified without supporting data.
Article
Sexual selection, through female choice and/or male–male competition, has influenced the nature and direction of sexual size dimorphism in numerous species. However, few studies have examined the influence of sperm competition on size dimorphism. The orb-web spider Nephila edulis has a polygamous mating system and extreme size dimorphism. Additionally, the frequency distribution of male body size is extremely skewed with most males being small and few large. The duration of copulation, male size and sexual cannibalism have been identified as the significant factors determining patterns of sperm precedence in spiders. In double mating trials, females were assigned to three treatments: either they mated once with both males or the first or the second male was allowed to mate twice. Paternity was strongly associated with the duration of copulation, independent of mating order. Males that were allowed to mate twice not only doubled the duration of copulation but also their paternity. Small males had a clear mating advantage, they copulated longer than large males and fertilized more eggs. Males of different sizes used different tactics to mate. Large males were more likely to mate through a hole they cut into the web, whereas small males approached the female directly. Furthermore, small males usually mated at their first attempt but large males required several attempts before mating took place. There was no obvious female reaction towards males of different sizes.
Article
1. The reproductive benefits and predatory costs of male-male competition were studied in the orb weaver, Nephila clavipes. During the breeding season adult males search for females, and congregate on their orbs. 2. Males compete for hub position proximal to the female, with the largest male assuming hub status. Smaller males move about the periphery of the orb. 3. Hub males gained the advantage of almost exclusive mating, and a potential advantage of feeding on prey captured by the female. Peripheral males pursued various alternatives, but rarely mated. 4. Females, the larger sex, occasionally preyed on males. The cost to males from female predation was no greater for hub than peripheral males.
Article
In natural populations, courting males of Araneus diadematus are often consumed by females before they have successfully copulated. Despite the possible nutritional benefits of sexual cannibalism for females, the male can derive no benefit by being consumed before copulation. In this study, females that consumed a single male significantly increased their body mass, regardless of the quality of their diet. The implication is that, for A. diadematus, sexual cannibalism increases female fecundity. In experimentally controlled courtship sequences, larger males were less likely to be cannibalized than smaller males, but female size had no effect on male mating success. The mating success of males was not influenced by the age of the male, indicating that cannibalism is not the results of male senility.
Article
Sexual selection theory predicts that signals reflecting the relative quality of individuals should be used in mate choice. Females could base their choice of copulation partners on male secondary sexual traits that honestly signal male age, as predicted by the age-based indicator mechanism. Studies have shown that female blue tits prefer older males and that aspects of dawn song reflect male quality, but it remains unknown whether dawn song characteristics correlate with male age. We compared dawn song characteristics of second-year (SY) and older (ASY) male blue tits (cross-sectional analysis), and tested for age-related changes within individuals (longitudinal analysis) and differential overwinter survival of SY males. We further investigated the relation between dawn song and paternity gain and loss. We found that ASY male blue tits began to sing earlier relative to sunrise than did SY males. This difference in the onset of dawn singing was due to age-related changes in individual performance rather than differential survival of individuals with varying expression of the trait. Males that began to sing earlier at dawn had more mating partners, and were more likely to gain extrapair paternity. Our findings suggest that the onset of dawn song can provide a simple mechanism for females to assess the relative quality of their mate and of neighbouring males. We propose that females use the onset of singing as a cue for their choice of extrapair partners.
Article
Male bowl and doily spiders (Frontinella pyramitela: Linyphiidae) fight over access to adult females. The probability of disablement or fatal injury in these contests is a linear function of their duration. Thus the fights fit closely the assumptions of a version of the game theory ‘war of attrition’. Because the details of sperm competition are known, female value (expected number of eggs fertilized) to either a copulating male or an intruder can be quantified for any stage of copulation. Using this information, the predictions of the war of attrition model were critically examined by experimental manipulation of fighting ability and female value for both web residents and intruders. When female value was equal for both combatants, the ability to win fights was correlated with body size and the duration of contests was inversely correlated with size difference. The winning percentage of males of specific size differences varied directly with female value. The treatments with the highest percentage of injuries and fatalities were those in which a smaller resident was defending a female of great value to him. In two treatments in which larger web residents were contesting for females of low value, the predictions of the model were seemingly not supported. However, a quantitative analysis of the treatments shows that these apparently anomalous results are in accord with the model.
Article
Nephilid spiders are known for gigantic females and tiny males. Such extreme sexual dimorphism and male-biased sex ratios result in fierce male-male competi- tion for mates. Intense sperm competition may be responsible for behaviors such as mate guarding, mate binding, opportunistic mating, genital mutilation, mating plugs and male castration (eunuchs). We studied the mating biology of two phylogenetically, behaviorally and morphologically distinct south-east Asian nephilid spider species (Herennia multipuncta, Nephila pilipes) in nature and in the laboratory. Specifically, we established the frequencies and effectiveness of plug- ging (a plug is part of the male copulatory organ), and tested for male and female copulatory organ reuse. Both in nature and in the laboratory, plug frequencies were higher in H. multipuncta (75-80% females plugged) compared with N. pilipes (45-47.4%), but the differences were not significant. Plugs were single and effective (no remating) in H. multipuncta but multiple and ineffective (remating possible) in N. pilipes .I nHerennia, the males plugged when the female was aggressive and in Nephila plugging was more likely when mating with previously mated and larger females. Further differences in sexual biology are complete palpal removal and higher sexual aggressiveness in Herennia (sexual cannibalism recorded for the first time), and mate binding in Nephila. Thus, we propose the following evolutionary hypothesis: nephilid plugging was ancestrally successful and enabled males to monopolize females, but plugging became ineffective in the phylogenetically derived Nephila. If the evolution of nephilid sexual mechanisms is driven by sexual conflict, then the male mechanism to monopolize females prevailed in a part of the phylogeny, but the female resistance to evade monopolization ultimately won the arms race.
Article
Reproductive strategies of males and females usually differ and as a consequence, may impose asymmetric costs of reproduction on the two sexes and result in conflict between the sexes. In spiders, males do not provide parental care and females store sufficient sperm for several clutches. These characteristics define the stage for a conflict between males and females that occur mainly over the frequency of mating. Factors such as sexual size dimorphism, operational sex ratio, mating system and life history strategies are likely to influence the degree of conflict and its outcome for different species. Male spiders may suffer large costs of mating due to mate search, assessment of female condition, courtship and cannibalistic tendencies of their mates. Courtship may reduce cannibalism, although in some cases, males 'benefit' from being cannibalised by having an increased fertilisation rate or greater offspring fitness. In some species, limited mating capacities will increase the value of the current mating relative to future reproduction. Apart from a possible benefit of genetic variability within a clutch, females might not benefit from multiple mating and multiple mating may even be costly. Exceptions occur if additional resources are provided by males or when offspring fitness increases with additional mating. Forced copulation, prey theft, loss of web and reduction of foraging time can all result in reduced reproductive success for females. We discuss the interacting influences of life-history traits (especially patterns of growth and maturation and sexual size dimorphism) and the reproductive strategies of males and females, using semelparous spider, Stegodyphus lineatus(Eresidae), as an example of a species in which males and females can have strongly conflicting interests
Article
The details of sperm transfer and usage in the multiply-mating bowl and doily spider (F. pyramitela) were investigated. Interrupted copulation experiments revealed that males transfer no sperm during the initial phase of copulation, but thereafter sperm transfer is very rapid. Using sterile and fertile males the consequences of double mating were examined. If intruders displace a copulating male, the first male still fertilizes all the eggs he would have after copulating for that particular duration. If the first copulation has been completed, a second male may gain a few fertilizations in a female's third egg sac, although females in the field almost never survive long enough to deposit three sacs. If any significant interval has passed since the initial copulation, a second male fertilizes no eggs. First male sperm priority seems especially common in spiders though it is rare in insects. This is hypothesized to be because the lengthy interval between mating and first oviposition in spiders has selected against other methods of paternity assurance. The female reproductive morphology of the entelegyne spiders may also be conducive to first male sperm priority.