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Abstract

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.

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... 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 . ...
... Examples of behavioural strategies that augment male reproductive success and paternity in spite of cannibalism seem to be more numerous. These include mate guarding, mate binding, opportunistic mating, sacrificial death during copulation, and genital mutilation, even emasculation 12,[14][15][16]18,19,22,24,25 . ...
... This means that, despite being cannibalised, male eunuchs can benefit from selecting the better charged palp thereby maximising sperm transfer. Although the other four species studied here do not engage in full emasculation, lesser genital mutilation may facultatively occur in A. versicolor, H. multipuncta and N. pilipes 14,15,19,35,36 . Since damaged organs may malfunction as sperm transferring devices after their first use, partially damaged males may likewise benefit from preferential use of the better charged palp, analogous to eunuchs. ...
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.
... The suggested evolutionary link between male genital complexity and its impact on female mating rates has not been tested in a phylogenetic framework. Relatively small nephilid males of certain species engage in extreme mating strategies, including severing terminal parts of their pedipalps (sperm transferring appendages), which are used to plug female copulatory openings [39,40]. Experimental studies on selected species found that plugs from males with complex genitals commonly prevent female polyandry, whereas plugs from simple genitals do not [39,41]. ...
... Relatively small nephilid males of certain species engage in extreme mating strategies, including severing terminal parts of their pedipalps (sperm transferring appendages), which are used to plug female copulatory openings [39,40]. Experimental studies on selected species found that plugs from males with complex genitals commonly prevent female polyandry, whereas plugs from simple genitals do not [39,41]. Assuming that male strategies to monopolize paternity with a single female via genital plugging are not in the interest of the female [20], females ought to evolve counter-adaptations. ...
... 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]. ...
Article
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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 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 mutilation[32][33][34][35][36][44][45][46][47][48], 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. ...
... We are thus facing a largely unknown origin of amorphous mating plugs in spiders, with the correspondingly spurious understanding of spider mating plug biology. Spiders are highly suitable organisms for sexual biology research[53,54], and the family Nephilidae contains particularly good taxonomic models for studying mating plug biology and its implications for sexual selection[45,55,56]. Within nephilids, male and female genitalia apparently coevolved from simple to complex and back to simple in a unique display of evolutionary arms race[57], where more complex male genital plugs enforce female monandry (e.g. ...
... Herennia, Nephilengys). Through simplification of female and male genitals, however, the male produced mating plugs became ineffective, and thus the females of phylogenetically derived Nephila were able to reassert polyandry[45]. The most dramatic case of the documented polyandry comes from the giant wood spider Nephila pilipes, a highly sexually dimorphic species (Fig. 1A), where females commonly sport multiple embolic plugs[45]. ...
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.
... Only males with intact palps (i.e. without any damage, see Kuntner et al. 2009b) were used in the experiments. In the laboratory, we kept females individually in plastic frames (50 Â 50 cm and 10 cm high) with bamboo sticks attached to their inner sides to allow them to build complete orb-webs on which all mating trials were conducted. ...
... All interactions between the male and female were filmed by HD video cameras. Nephila pilipes males often mate opportunistically when the female is engaged in wrapping or consuming prey (Robinson & Robinson 1980; Kuntner et al. 2009b); therefore, no prey were provided to the females during the mating trials to control for the possibility of opportunistic mating, which would have reduced the occurrence and frequency of female cannibalism (Fromhage & Schneider 2005). Only trials in which males successfully mated (i.e. ...
... Therefore, it may be seen as a counteradaptation to female resistance to repeated mating rather than to mating per se. Moreover, the percentage of males being cannibalized by females decreased through mate binding from 71.4% to 17.4%, suggesting that mate binding may reduce sexual cannibalism (Kuntner et al. 2009b). More importantly, our study revealed the mechanisms of mate binding by which males reduce female aggressiveness; that is, both tactile and chemical cues together play crucial roles in rendering females more prone to repeated mating and in reducing the risk of sexual cannibalism. ...
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.
... We macerated all palps in concentrated KOH overnight in order to make them transparent and expandable in distilled water. We excised and examined all epigyna externally, then macerated each epigynal preparation in concentrated KOH overnight, and carefully cleaned it with needles in distilled water (e.g., Kuntner et al. 2009b). This technique exposes the dorsal epigynal anatomy and renders spermathecae translucent, which allows any embolic leftovers lodged inside spermathecae to be seen under a stereomicroscope. ...
... Genital damage.-Two mated males (n 5 17) emasculated one palp to become half-eunuchs ( Kuntner et al. 2009b) after separating from the females they had copulated with. We found the damaged palps in the males' vials, implying that they were not stuck in the female genitalia during copulation but were rather self-removed after mating. ...
... Our results show no evidence for genital plugging, but we recorded two cases of male L. thorelli becoming eunuchs by severing their palps subsequent to mating. This resembles the eunuch behavior of Herennia Thorell 1877 (Kuntner 2005;Kuntner et al. 2009b), but not that of other nephilids where males leave a palp in the female genital tract ( Kuntner et al. 2009c;Kralj-Fišer et al. 2011;Li et al. 2012), nor that of Tidarren Chamberlin & Ivie 1934 where the single-palped male spontaneously dies while copulating and thus functions as a whole-body mating plug (Knoflach & van Harten 2001). Although the eunuch's behavior in Leviellus is clearly not obligate, it may nevertheless be suggestive of some level of post-mating sterility in males. ...
Article
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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.
... The plugging hypothesis (Kuntner, 2005) sees emasculation as an extension of lesser genital damage where terminal ends of palps (emboli/embolic conductors; Fig. 1E, F) function as genital plugs (Robinson, 1982;Uhl et al., 2010), and the mutilated palp is thus permanently disfigured, and cannot be used for further mating (Kuntner et al., 2009c). Therefore, males may remove it entirely using predetermined weak points. ...
... Trials with Nephilingis livida produced similar results, although the plugging effectiveness was slightly lower at 64% (Kralj-Fišer & Kuntner, 2012), a difference that the authors attributed to significantly different genital anatomy between Nephilengys (as malabarensis) and Nephilingis (as livida). In Herennia multipuncta, known for eunuchs, the extensive male plugs were fully successful in preventing female remating, while in Nephila pilipes, a species with no eunuchs, the plugs were ineffective (Kuntner et al., 2009c). This available evidence in nephilids suggests that eunuchs who plug, also more successfully enforce female monandry, while in Nephila spp. the females are highly polyandrous. ...
... Therefore, those males that drop one or both palps may be able to achieve higher agility (Ramos et al., 2004;Kuntner et al., 2009a), and the edge in male-male contests. Thus, a proximate explanation for the better fighting abilities is the 'gloves-off' hypothesis (Kuntner et al., 2009c) predicting enhanced physical stamina in emasculated eunuchs (Ramos et al., 2004;Kralj-Fišer et al., 2011;Lee et al., 2012). ...
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.
... The plugging hypothesis (Kuntner, 2005) where terminal ends of palps (emboli/embolic conductors; Fig. 1E, F) function as genital plugs (Robinson, 1982;Uhl et al., 2010), and the mutilated palp is thus permanently disfigured, and cannot be used for further mating (Kuntner et al., 2009c). Therefore, males may remove it entirely using predetermined weak points. ...
... Trials with Nephilingis livida produced similar results, although the plugging effectiveness was slightly lower at 64% (Kralj-Fišer & Kuntner, 2012), a difference that the authors attributed to significantly different genital anatomy between Nephilengys (as malabarensis) and Nephilingis (as livida). In Herennia multipuncta, known for eunuchs, the extensive male plugs were fully successful in preventing female remating, while in Nephila pilipes, a species with no eunuchs, the plugs were ineffective (Kuntner et al., 2009c). This available evidence in nephilids suggests that eunuchs who plug, also more successfully enforce female monandry, while in Nephila spp. the females are highly polyandrous. ...
... Therefore, those males that drop one or both palps may be able to achieve higher agility (Ramos et al., 2004;Kuntner et al., 2009a), and the edge in male-male contests. Thus, a proximate explanation for the better fighting abilities is the 'gloves-off' hypothesis (Kuntner et al., 2009c) predicting enhanced physical stamina in emasculated eunuchs (Ramos et al., 2004;Kralj-Fišer et al., 2011;Lee et al., 2012). ...
... Relatively recently, however, studies investigating reproductive strategies such as sperm competition, genital damage and plugging, male terminal investment, sexual cannibalism, female polyandry, male monogyny, and sexual conflict triggered a shift in focus among researchers of spider biology (Andrade 1996;Elgar and Fahey 1996;Schneider and Lubin 1998;Schneider et al. 2000;Elgar et al. 2003a, b;Andrade and Kasumovic 2005;Fromhage and Schneider 2006;Miller 2007;Fromhage et al. 2008;Kuntner et al. 2009b, c;Uhl et al. 2010;Fromhage and Schneider 2012;Herberstein et al. 2012). These studies solidified the view that most sexual strategies, including those that relate to genital and body sacrifice pose certain fitness advantages such as securing paternity and monopolizing partners (Austad 1984;Andrade 1996;Kuntner et al. 2009c;Uhl and Busch 2009;Welke and Schneider 2010). ...
... Various hypotheses have been proposed to explain male emasculating behaviors (reviewed in Kuntner et al. 2014). The plugging hypothesis predicts that the broken male genital parts lodged in female copulatory organs must effectively prevent female remating, thereby reducing sperm competition and increasing paternity share (Kuntner 2005;Kuntner et al. 2009c;Uhl et al. 2010). However, as genital plugs are a widespread phenomenon in spiders, this hypothesis may apply to any genital damage and is not strictly restricted to emasculating eunuchs. ...
... In this case, the possession of the disproportionally heavy palp should be more costly than its removal. In fact, the proximate cause of eunuch superior fighting abilities has been explained by the gloves-off hypothesis, which predicts the male endurance and stamina to increase with each severance of the heavy palp (Ramos et al. 2004;Kuntner et al. 2009c;Lee et al. 2012). Accordingly, Tidarren males remove one of their palps before mating rendering them more agile and thereby likely allowing them to win contests against rival males (Ramos et al. 2004). ...
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.
... been shown to function as effective mating plugs (Monnin & Peeters 1998; Fromhage & Schneider 2006; Snow et al. 2006; Nessler et al. 2007; Kuntner et al. 2009c). In some of these species, males spontaneously die after the first or second copulation , whereas they may survive copulation in others but subsequently lack their genital organs (palps). ...
... In staged experimental trials in the laboratory, we first tested the plugging hypothesis. We predicted that broken palps would prevent a female remating by forming a physical barrier inside her genital tract, as in N. fenestrata (Fromhage & Schneider 2006) and H. multipuncta (Kuntner et al. 2009c). We estimated the importance of male palp amputation for his paternity with respect to the number of insertions by two subsequent suitors. ...
... The remaining 12.5% of males retrieved their damaged palps from copula, but then subsequently chewed them off to become voluntary eunuchs. A similar behavioural pattern has been documented in H. multipuncta, in which males first damaged their palps during copulation by breaking the embolic conductor, which became a mating plug, then subsequently chewed off the damaged palp (Kuntner et al. 2009c). Full genital amputation is also known in the theridiid spiders Echinotheridion and Tidarren (Knoflach & van Harten 2000, 2001 Agnarsson 2006). ...
Article
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.
... Male N. fenestrata, N. plumipes, and N. pilipes frequently damage their genitalia during mating, but not N. clavipes, N. edulis, nor N. senegalensis . While plugs in N. fenestrata are effective as plugs against rivals , they are apparently an exception, as broken palps in other Nephila spiders are ineffective (e.g., Nephila plumipes, reviewed in , and it is common to find multiple "plugs" in the same genital tract (Kuntner, Kralj-Fiser, Schneider, & Li, 2009). The question of how genital mutilation evolved despite ineffective plugging is fascinating, but beyond the scope of this chapter (see Kuntner, Kralj-Fiser, et al., 2009;. ...
... While plugs in N. fenestrata are effective as plugs against rivals , they are apparently an exception, as broken palps in other Nephila spiders are ineffective (e.g., Nephila plumipes, reviewed in , and it is common to find multiple "plugs" in the same genital tract (Kuntner, Kralj-Fiser, Schneider, & Li, 2009). The question of how genital mutilation evolved despite ineffective plugging is fascinating, but beyond the scope of this chapter (see Kuntner, Kralj-Fiser, et al., 2009;. ...
... Since not all species of Nephila and Argiope experience palp damage , there is some interesting potential to ask how this variation affects links between plasticity and local social context (see Kuntner, Kralj-Fiser, et al., 2009;Schneider et al., 2015). ...
Chapter
Phenotypic plasticity refers to the ability of individuals with a given genotype to show variation in phenotypes under different conditions (e.g., Kelly, Panhuis, & Stoehr, 2012; Pigliucci, 2001; West-Eberhard, 2003), an ability that may be adaptive ifplastic phenotypes have higher fitness than those that are inflexible in the face of environmental variation (Nettle & Bateson, 2015). Understanding the evolution, nature, and optimization of adaptive phenotypic plasticity is a major goal of modern research in evolutionary ecology, behavior, and conservation. Adaptive plasticity encompasses a wide range ofresponses that differ in the time-scale ofintegration ofenvironmental variation with phenotypic changes, and whether those changes are permanent or transient (Beaman, White, & Seebacher, 2016; Charmantier et al., 2008; Fawcett & Frankenhuis, 2015; Groothuis & Taborsky, 2015; Guerrero-Bosagna et al., 2018; Kasumovic, 2013; Nyman, Fischer, Aubin-Horth, & Taborsky, 2017; Snell-Rood, 2013; Taborsky, 2017). Most relevant to this review is the considerable effort aimed at understanding how trait expression is affected by information acquired during ontogeny (developmental plasticity, Kasumovic, 2013; Pigliucci, 2001; WestEberhard, 2003) or during adult life stages (activational plasticity, SnellRood, 2013). The evolution of these forms of adaptive plasticity is most likely when environmental conditions vary on a scale that ensures the phenotypes and life histories that confer high fitness for adults are different from those that were advantageous in the previous generation, but are detectable by juveniles (developmental plasticity), or that these conditions change throughout the lifetime of the adult (activational plasticity, Nettle & Bateson, 2015). Even under these conditions, however, plasticity is only expected if reliable information is available to the individual regarding the changing state of the environment on a time-scale that allows phenotype-environment matching (Dore et al., 2018; Nettle & Bateson, 2015; Pigliucci, 2001). Here I provide an overview of adaptive plasticity, particularly how links between changing social context and sexual selection can shape the evolution ofplasticity (Section 2). I then discuss the utility of testing hypotheses for such socially-linked adaptive plasticity in taxa with extreme mating behaviors (Section 3). I conclude with empirical examples of plasticity in web-building spiders in which severe limits on male mating frequency arise from high rates of sexual cannibalism, male genital
... Consistent behaviors support the inference that nephilid males do not benefit from being eaten after mating. They evade attacks (80), always place their bodies far from female jaws (unlike many other spiders), and flee if the female becomes aggressive (88). These behaviors may evade or depress female aggression and/or ameliorate decreases in male fitness (if not survival). ...
... Male N. pilipes stereotypically lay silk threads on the female body and legs in between mating bouts (Figure 4g), called mate binding (88). Mate binding lowers female aggression. ...
... 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). ...
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.
... Male N. fenestrata, N. plumipes, and N. pilipes frequently damage their genitalia during mating, but not N. clavipes, N. edulis, nor N. senegalensis . While plugs in N. fenestrata are effective as plugs against rivals , they are apparently an exception, as broken palps in other Nephila spiders are ineffective (e.g., Nephila plumipes, reviewed in , and it is common to find multiple "plugs" in the same genital tract (Kuntner, Kralj-Fiser, Schneider, & Li, 2009). The question of how genital mutilation evolved despite ineffective plugging is fascinating, but beyond the scope of this chapter (see Kuntner, Kralj-Fiser, et al., 2009;. ...
... While plugs in N. fenestrata are effective as plugs against rivals , they are apparently an exception, as broken palps in other Nephila spiders are ineffective (e.g., Nephila plumipes, reviewed in , and it is common to find multiple "plugs" in the same genital tract (Kuntner, Kralj-Fiser, Schneider, & Li, 2009). The question of how genital mutilation evolved despite ineffective plugging is fascinating, but beyond the scope of this chapter (see Kuntner, Kralj-Fiser, et al., 2009;. ...
... Since not all species of Nephila and Argiope experience palp damage , there is some interesting potential to ask how this variation affects links between plasticity and local social context (see Kuntner, Kralj-Fiser, et al., 2009;Schneider et al., 2015). ...
Chapter
Full chapter is available for free download until May 11, 2019 at https://authors.elsevier.com/b/1YmApEsvgWKow. Phenotypic plasticity is the ability of organisms with a given genotype to develop varied phenotypes under fluctuating environmental conditions. This chapter provides an overview of the conditions under which adaptive phenotypic plasticity is expected to evolve, and the challenge of conducting rigorous tests of hypotheses for such plasticity. It is argued that advances in the field may be facilitated by focusing on species in which some of the complexity of plastic responses is naturally simplified. Here, the focus is on assessing adaptive plasticity of male spiders in response to spatio-temporal heterogeneity in demographic variables that cause changes in the mode and intensity of sexual selection. For web-building spiders in the genera Argiope, Nephila, and Latrodectus, males rarely mate more than once due to sexual cannibalism, male genital mutilation, and arduous, risky mate searching, simplifying predictions about adaptive phenotypes. Population density, the proximity of mates and competitors, and the operational sex ratio may all be linked to variation in the importance of traits that confer advantages in the different episodes of selection that determine male fitness. These links are reviewed in the context of the biology of representative species in each genus. Experimental studies of adaptive plasticity demonstrate that there are robust associations between pheromone-mediated assessment of social context and male development and behavior. The utility of continued study of these spiders with an eye to comparative studies is emphasized.
... Sexual cannibalism caused by female choice may be particularly adaptive in species where females are monopolized by males. 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). ...
... Thus, males are monogamous or bigamous (two palps) by default. In nephilids where males emasculate their palps during mating, the plugs prevent remating into the used female CO by the rival males in approximately 70% of the cases (Kuntner et al. 2009b;Kralj-Fišer et al. 2011). Mate plugging will thus limit female mating to a single male if both of her genital openings get plugged. ...
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.
... Sexual cannibalism caused by female choice may be particularly adaptive in species where females are monopolized by males. 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). ...
... Thus, males are monogamous or bigamous (two palps) by default. In nephilids where males emasculate their palps during mating, the plugs prevent remating into the used female CO by the rival males in approximately 70% of the cases (Kuntner et al. 2009b; KraljFišer et al. 2011). Mate plugging will thus limit female mating to a single male if both of her genital openings get plugged. ...
Data
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 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.
... Phylogenies, particularly at the species level, may thus be utilised as predictors, which may include, among others, biogeographic events (Schuh 2000; Hubert et al. 2007), evolutionary pressures and outcomes (Kiontke et al. 2004; Kuntner et al. 2009a), niche conservatism (Warren et al. 2008), and gene and protein qualities (van der Heijden et al. 2007; Ye et al. 2008). More specifically, topology and character optimisation may predict biology of unknown species, be it ecology (Cranston 2008), behaviour (Agnarsson and Kuntner 2005; Coddington and Agnarsson 2006) or functional morphology (Kuntner et al. 2009b). Despite the obvious predictive power of phylogenies, they are rarely used by non-systematists to predict, and guide studies of, behaviour in as yet unobserved species. ...
... Because nephilids are model organisms in behavioural, ecological, morphological and developmental research (e.g. Vollrath and Parker 1992; Coddington et al. 1997; Uhl and Vollrath 2000; Schneider and Elgar 2001, 2002, 2005 Higgins 2002; Fromhage and Schneider 2005a, 2005b Miyashita 2005; Harvey et al. 2007; Kuntner et al. 2009a Kuntner et al. , 2009b), discovering and describing the natural history of previously unstudied taxa is a priority. Here we test phylogenetically generated predictions of behaviour in previously unstudied Clitaetra species. ...
Article
Full-text available
Phylogenies are underutilised, powerful predictors of traits in unstudied species. We tested phylogenetic predictions of web-related behaviour in Clitaetra Simon, 1889, an Afro-Indian spider genus of the family Nephilidae. Clitaetra is phylogenetically sister to all other nephilids and thus important for understanding ancestral traits. Behavioural information on Clitaetra has been limited to only C. irenae Kuntner, 2006 from South Africa which constructs ladder webs. A resolved species-level phylogeny unambiguously optimised Clitaetra behavioural biology and predicted web traits in five unstudied species and a uniform intrageneric nephilid web biology. We tested these predictions by studying the ecology and web biology of C. perroti Simon, 1894 on Madagascar and C. episinoides Simon, 1889 on Mayotte. We confirm predicted arboricolous web architecture in these species. The expected ontogenetic allometric transition from orbs in juveniles to elongate ladder webs in adults was statistically significant in C. perroti, whereas marginally not significant in C. episinoides. We demonstrate the persistence of the temporary spiral in finished Clitaetra webs. A morphological and behavioural phylogenetic analysis resulted in unchanged topology and persisting unambiguous behavioural synapomorphies. Our results support the homology of Clitaetra hub reinforcement with the nephilid hub-cup. In Clitaetra, behaviour was highly predictable and remained consistent with new observations. Our results confirm that nephilid web biology is evolutionarily conserved within genera.
... In many spiders , males seal the female genital opening after copulation , in order to avoid sperm concurrence and secure their paternity . One type of such sealing mechanism is the controlled breakage of the embolus tip (Schneider et al. 2001 ;Kuntner et al. 2009 ) or the autotomy of the whole pedipalp (Knofl ach and Van Harten 2001 ), which then stays attached to the epigyne. The embolus tip 2.3 Other Interlocking Devices might stay attached, because it is pressed and locked in the narrow duct, due to the elasticity of both embolus and duct wall material. ...
... Another strategy of males in securing paternity is the production of mating plugs , which seal the female genital opening (Parker 1970 ;Kuntner et al. 2009 ;. In contrast to insects, in arachnids this is much more common than mate guarding. ...
Book
This book surveys attachment structures and adhesive secretions occurring in this class of animals and discusses the relationships between structure, properties, and function in the context of evolutionary trends, and biomimetic potential. Topics comprise mechanical attachment devices, such as clamps, claws, hooks, spines and wraps, as well as hairy and smooth adhesive pads, nano-fibrils, suction cups, and viscid and solidifying adhesives. Attachment is one of the major types of interactions between an organism and its environment. There are numerous studies that deal with this phenomenon in lizards, frogs, insects, barnacles, mussels and echinoderms, but the second largest class of animals, the Arachnida, was highly neglected so far. The authors demonstrated that most arachnid adhesive structures are highly analogous to those of insects and vertebrates, but there are also numerous unique developments with some intriguing working principles. Because arachnid attachment organs have a very strong potential of technological ideas for the development of new materials and systems, inspirations from biology could also be interesting for a broad range of topics in materials and surface engineering.
... Males in several spider and some insect species obligatorily break their genital organs within female genitals during copulation in order to produce mate plugs which avoid/reduce sperm competition with subsequent mates (Uhl, Nessler, & Schneider, 2010). 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). ...
Article
Full-text available
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.
... Spider sexual biology has been intensively studied in recent years under different research approaches (Eberhard, 2004a;Huber et al., 2007;Eberhard and Huber, 2010;Uhl et al., 2010;Michalik and Rittschof, 2011) although investigation in this area goes back a long time (e.g., Gerhardt, 1911). Detailed morphological analysis of male and female genital structures (Huber, 2004a;Burger and Kropf, 2007;Dimitrov et al., 2007;Burger et al., 2010;Izquierdo and Labarque, 2010;Burger, 2011Burger, , 2013 and the appropriate documentation of sexual behavior (van Helsdingen, 1965;Eberhard, 2004aEberhard, , 2011 have been important data sources for testing hypotheses on sexual selection (Uhl, 2000a;Greven, 2002, 2005;Eberhard, 2004a;Huber, 2005aHuber, , 2006Aisenberg and Eberhard, 2009;Kuntner et al., 2009a) and male-female coevolution (Eberhard, 2004b,c;Huber, 2005b;Ramos et al., 2005;Kuntner et al., 2009b). In addition, genital characters usually dominate morphological data matrices in current phylogenetic studies and support the monophyly of several clades at different hierarchical levels (Arnedo et al., 2009; Alvarez-Padilla and Benjamin, 2011;Huber, 2011;Lopardo et al., 2011;Frick and Scharff, 2013). ...
Article
Full-text available
Female genital morphology of secondarily haplogyne spiders has been poorly studied, hampering the analysis of its possible phylogenetic significance. We conduct a comparative morphological study of 12 species of the secondarily haplogyne spider genus Glenognatha Simon, 1887 using scanning electron microscopy. Representatives of the closely related genera Pachygnatha Sundevall, 1823 and Dyschiriognatha Simon, 1893 were also examined. The female genitalia of Glenognatha, Dyschiriognatha, and Pachygnatha species examined are composed of a spiracle-shape gonopore, a membranous chamber, a pair of copulatory ducts (CD) leading to spermathecae and a large uterus externus (UE). The most significant variation among Glenognatha species, previously unregistered within Araneoidea, is related with the absence or presence of CD and spermathecae. In addition, several characters as the form and distribution of long stem gland ductules and compartmentalization of the UE may be important for phylogenetic inference at species and generic level. Our results corroborate the close relationship between Dyshiriognatha and Glenognatha. A table with potentially informative female genitalic characters for phylogenetic inference within Glenognatha is provided. Understanding the general structure of the female genitalia in secondarily haplogyne taxa is a crucial step in order to propose characters for phylogenetic inference and to understand its possible functional significance. J. Morphol., 2014. © 2014 Wiley Periodicals, Inc.
... Furthermore, a previously unstudied developmental mechanism of additional adult growth through molting exists, in addition to a plethora of behavioral adaptations arising through sexual selection that we believe are connected with, if not determined by, extreme SSD (Kuntner et al. 2009a). Notable examples of such behaviors are extreme polygamy, mating plugs, genital mutilation, mate binding (Kuntner et al. 2009b(Kuntner et al. , 2012Zhang et al. 2011) and the construction of giant asymmetrical webs . ...
Article
Full-text available
Nephila are known for the greatest degrees of sexual size dimorphism among orb weaving spiders (Araneoidea) and thus among terrestrial animals. However, a meaningful quantification of the dimorphism is lacking and the proximate developmental mechanisms of female gigantism are poorly understood, being attributed solely to female delayed maturation. Here we show that females in the giant wood spider Nephila pilipes (Fabricius 1793) become giants through facultative post-maturity molting, a phenomenon resulting in female carapaces on average 4.27 times longer than males' (ranging from 3 to 6.4 times), and female mass averaging 125 times the male's (ranging from 28 to 502 times). Although the small males follow a typical developmental pathway and reach maturity with their final molt, the females mature at varying sizes and instars and then continue to grow by molting the entire exoskeleton except their genitals. The newly discovered phenomenon of additional, single-sex, adult, non-genital molting may represent a critical developmental adaptation that facilitates female gigantism in Nephila as a response to fecundity selection.
... However, polyandry is common in the majority of the animals (Arnqvist and Nilsson 2000; Boulton and Shuker 2013;Taylor et al. 2014), and spiders are no exception. Indeed, polyandry seems to be the most 1 3 frequent mating system in Araneae (Huber 2005), although some cases of monandry and monogyny have been reported (Pérez-Miles et al. 2007), principally associated with the occurrence of mating plugs and sexual cannibalism (Hosken et al. 2009;Kuntner et al. 2009;Nakata 2016). Among the benefits of polyandry for females are ensuring sufficient sperm to fertilize all of their eggs, receiving direct benefits such as nuptial gifts or, more indirectly, avoiding inbreeding and increasing the genetic diversity of the offspring (Eberhard 1996;Maklakov and Lubin 2006;Peretti and Aisenberg 2015). ...
Article
Populations of a species may show variation in mating systems, especially when the species is widely distributed. Aglaoctenus lagotis is a funnel-web wolf spider distributed in South America and with a ‘central Argentina form’ (CA) and a ‘southern Uruguay form’ (SU). Both forms differ in sexual behaviour, population density and copulatory season. This study evaluates the potential level of polyandry of both forms, sequentially exposing females to different males of their form under laboratory conditions. The number of copulations each female accepted and the characteristics of these sexual encounters were registered. CA females accepted more re-copulations than SU females and seemed to maintain more sexual attractiveness after the first copulation. In neither form was female re-copulation influenced by body characteristics, duration of the first copulation, ejaculation frequency or copulatory body shaking of females. Additionally, the PCA showed that both forms could be separated by their copulation behaviours. The higher level of polyandry in the CA form compared to the SU form suggested in our results adds another difference between these forms, currently under study to determine whether they are different species. This study is the first on mating systems in funnel-web wolf spiders, adding knowledge to the discussion about the evolution of sexual strategies in this group.
... Veiling took place in about 33% of courtship observations in Latrodectus revivensis Shulov, 1948(Anava & Lubin 1993, in 50% of Steatoda bipunctata (Linnaeus, 1758) pairings (Knoflach 2004), and only occasionally in Steatoda grossa (Scott et al. 2017). Intriguingly, application of a bridal veil appears to be an obligate behavior in Nephila pilipes (Fabricius, 1793), as well as in Pisaurina mira (Bruce & Carico 1988;Kuntner et al. 2009;Anderson & Hebets 2016). Conversely, Cupiennius coccineus F.O. Pickard-Cambridge, 1901 (Ctenidae) males normally do not use veils in laboratory trials, but in an inter-species mating experiment, some male C. coccineus deposited silk on C. salei females, which are larger than conspecific females (Schmitt 1992). ...
Article
Spiders are well known for using chemical, vibratory, tactile, and visual signals within mating contexts. All spiders produce silk, and even in non-web building spiders, silk is intimately tied to courtship and mating. Silk produced by females provides a transmission channel for male vibratory courtship signals, while webs and draglines provide a substrate for female sex pheromones. Observations of male spiders producing silk during sexual interactions are also common across phylogenetically widespread taxa. However, the function of male-produced silk in mating has received very little study. Exploring the function of male silk use during mating will provide a deeper understanding of the complex mating systems of spiders and allow tests of hypotheses about the evolution of male and female traits under sexual selection and/or conflict. In this review, we outline functional hypotheses that may explain each of the following three main categories of silk deposition males exhibit during courtship and mating: (1) silk deposition on females' webs or other silk structures, (2) silk deposition on females ('bridal veils') and (3) silk associated with nuptial gifts. We then summarize the current knowledge of silk use by male spiders within these three categories and the types of mechanisms that may lead to functional effects, and discuss areas where future work can be targeted. © 2018 American Museum of Natural History. All rights reserved.
... During courtship, the tiny male surrounds the female body by repeatedly laying down silk, although the silk cannot truly restrain the female (Robinson and Robinson 1973). This behavior is called "mate binding" and was interpreted as a counter adaptation to the threat of sexual cannibalism (Kuntner et al. 2009b). Suggestive evidence for this comes from staged matings showing that mate binding mostly occurs after the female has aggressively terminated the first copulation. ...
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.
... Some MASC may reduce either the risk or intensity of sperm competition (Parker 1998). For example, mate guarding or mating plugs made from ejaculate components (e.g., Fenton 1984) or detached male genitals (e.g., Nessler et al. 2007;Kuntner et al. 2009) can prevent or delay female remating, and a similar function has been suggested for copulatory stimulation (Stockley 2002). Indeed, any male trait that reduces female remating rates may have evolved, in part at least, through selection arising from the risk of sperm competition. ...
Article
Traits that increase a male's fertilization success during sperm competition can be harmful to females and therefore represent a source of sexual conflict. In this review, we consider the variety of male adaptations to sperm competition (MASC) that may give rise to sexual conflict-including mate guarding, prolonged copulations, the transfer of large numbers of sperm, and the manipulation of females through nonsperm components of the ejaculate. We then reflect on the fitness economics influencing the escalation of these sexual conflicts, considering the likelihood of females evolving traits to offset the negative effects of MASC when compared with the strong selection on males that lead to MASC. We conclude by discussing the potential evolutionary outcomes of sexual conflict arising from MASC, including the opportunities for females to mitigate conflict costs and the prospects for conflict resolution.
... Only males with intact palps (i.e. without any damage, see Kuntner et al. 2009) were used in the experiments. ...
Article
Full-text available
Sexual conflict is common in animals, and female sexual cannibalism represents an extreme form of sexual conflict. Males in many species have evolved a variety of strategies to circumvent or decrease the risk of female sexual cannibalism. Opportunistic mating, by which a male mates with a female when she is disturbed or when she is feeding or undertaking moulting, is one of such kinds of strategies, and widely occurs in many animals, especially in spiders. However, whether the occurrence of male opportunistic mating depends on the intensity of female sexual cannibalism remains largely unexplored. We predicted a positive correlation between them. In this study, we tested this prediction by performing a series of mating trials in the laboratory using three species of web-building spiders with different intensities of female sexual cannibalism: Nephila pilipes, Nephilengys malabarensis, and Parasteatoda tepidariorum. We found that the occurrence of male opportunistic mating was positively, though not statistically significantly, correlated with the intensity of female sexual cannibalism, thus supporting our hypothesis. All together, we provide evidence that male opportunistic mating may have evolved to respond to the selection pressure posed by female sexual cannibalism.
... On the bases of their relative size, location of deposition, and physical composition, several terms i.e., copulatory plugs, sperm plugs, vaginal plugs, and spermatocleutrum, have been used to refer to mating plugs in different groups of animals. Mating plugs have been observed in nematodes (Hodgkin & Doniach 1997), in- sects (Danielsson 1998;Polak et al. 1998Polak et al. , 2001Mikheyev 2003;de Mello 2007), crustaceans (Oh & Hankin 2004;Rodgers et al. 2011), arachnids ( Kunter et al. 2009;Althaus et al. 2010;Ramirez et al. 2010;Uhl et al. 2010;Sentensk a et al. 2015), and vertebrates, such as snakes (Shine et al. 2000), lizards (Moreira & Birkhead 2003Moreira et al. 2007), primates (Eberle and Kappeler 2007) and rodents (Hartung & Dewsbury 1978;Voss 1979;Ramm et al. 2005). In arachnids, mating plugs have been investigated in several species of spiders and scorpions. ...
Article
In many species of scorpions (Order Scorpiones) and spiders (Order Araneae), mating plugs (gel-like or sclerotized) are deposited in the female reproductive tract, minimizing the possibilities of further matings. Although harvestmen (Order Opiliones) have direct sperm transfer via copulatory organs (penis or spermatopositor in the male and ovipositor in the female), prior studies of the reproductive anatomy of these arachnids have not reported the occurrence of these structures. With the aid of scanning electron microscopy, we observed distinct masses of amorphous, gel-like material in the distal openings of the ovipositors of six different specimens including representatives of the families Cosmetidae (Cynorta marginalis and Flirtea picta), Gonyleptidae (Discocyrtulus bresslaui and Geraeocormobius sylvarum), Kimulidae (Kimula sp.) and Metasarcidae (Metasarcus clavifemur). Dissection of one of these structures from a specimen of the cosmetid harvestman C. marginalis revealed a detailed endocast of the internal surfaces of the female reproductive tract. Considerable interspecific variation in the relative sizes and shapes (smooth and rough) of the amorphous gel-like structures were observed, but evidence of sclerotized components (i.e., parts of the male genitalia) was not found. The location and morphology of the gel-like structures are consistent with observations of mating plugs in other arachnids. The composition, source (male, female or both) and function of these amorphous gel-like structures (i.e. effective matting plug) requires additional study.
... Such genital plugs, which leave the palpal organ functionally sterile (but see [19]), were shown to prevent or reduce future inseminations in most species that have been investigated so far (e.g. [20][21][22][23][24][25];). In some species, even the whole male body may serve as a short term mating plug [26]. ...
Article
Full-text available
Sperm competition imposes a strong selective pressure on males, leading to the evolution of various physiological, morphological and behavioral traits. Sperm competition can be prevented by blocking or impeding the access to female genitalia by means of a mating plug. We investigated the factors responsible for plug production and function in the promiscuous female-cannibalistic spider Micaria sociabilis (Gnaphosidae). We performed mating trials using females with and without a plug that consists of an amorphous mass. The mating trials demonstrated that the probability of male plugging increased non-linearly with the duration of copulation. Copulation duration and plug production seem to be controlled by the female. We found that females terminated matings later if males were fast at genital coupling. Whereas incomplete plugs had disappeared on the day following copulation, complete plugs persisted (40%). In matings with females with complete plugs, only a small proportion of males (7%) were able to remove the plug, indicating the high effectiveness of plugging. Moreover, males ceased attempts to copulate with plugged females with higher probability. 3D X-ray microscopy of the female and male genitalia showed that the plug material can extend far into the female genital tract and that the plug material is produced by a massive gland inside the palpal organ of the modified male pedipalps. Our study demonstrates that the mating plug in M. sociabilis constitutes an effective male strategy to avoid sperm competition that seems to be under female control.
... without any damage) were used in the experiments. During the mating season, there are up to eight males waiting in a sub-adult female's web, and mating usually results in male pedipalp damage in this species (Kuntner et al., 2012b;Kuntner et al., 2009). Therefore, we assumed that the males with intact pedipalps we used were unmated. ...
Article
Full-text available
While molting occurs in the development of many animals especially in arthropods, post-maturity molting (PMM, organisms continue to molt after sexual maturity) has received little attention. Mechanism of molting has been studied intensively, however, the mechanism of PMM remains unknown although it is suggested to be crucial for the development of body size. In this study, we investigated factors that potentially induce PMM in the golden orb-web spider Nephila pilipes, which has the greatest degree of sexual dimorphism among terrestrial animals. We manipulated the mating history and the nutrient consumption of the females to examine whether they can affect PMM. The results showed that female spiders under low nutrition were more likely to molt as adults, and mating had no significant influence to the occurrence rate of PMM. Moreover, spiders that experienced PMM lived longer than those without and their body sizes were significantly increased. Therefore, we concluded that it is the nutritional condition rather than the mating history that has affected PMM.
... Plugs are often formed by males adding secretory substances into or over the female's genital opening after sperm transfer (Parker, 1998), but can also be devised by males leaving copulatory organs that break off partly or completely during copulation in the genital duct of the female. Plugging this duct with part of the copulatory organ is common among widow spiders, for example Latrodectus curacaviensis (Bhatnagar & Rempel, 1962), Latrodectus mactans (Abalos & Baez, 1963) and Latrodectus revivensis (Berendonck & Greven, 2002), and occurs also in other spider genera, for example A. bruennichi (Nessler, Uhl, & Schneider, 2006) and the nephilid spider Herennia multipuncta (Kuntner, Kralj-Fi ser, Schneider, & Li, 2008). ...
Article
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Males of the brown widow spider, Latrodectus geometricus (Theridiidae), invest energy in courtship displays and are often cannibalized after mating; accordingly, partial sex role reversal is expected. In this species, subadult females are able to mate and produce viable offspring. In contrast to mature females, these subadult females do not cannibalize their mates after copulation. Nevertheless, when given a choice, males preferred mature over subadult females and older over young mature females. We found no benefit for males in mating with the females of their choice. Older females were significantly less fecund than young mature females, and were not more fecund than subadult females. We tested possible advantages in mating with cannibalistic (mature) females, such as an increased probability of plugging the female's genital duct or longer copulations, or disadvantages in mating with subadult females, such as higher remating risk. None of these explanations was supported. Thus, we lack an adaptive explanation for male preference for mature older females. We suggest that older females produce more pheromone to attract males and that males are thus misled into mating with older, more aggressive and less fecund females.
... In the genus Argiope genital damage occurs in a number of species and prevalence as well as effectiveness at plugging varies , Sasaki and Iwahashi, 1995. Interestingly, mating plugs consisting of parts of male genitalia appear common in species with low male mating rates and sexual cannibalism (Foellmer, 2008, Kuntner et al., 2009b, Miller, 2007, Snow et al., 2006 a pattern which has been confirmed in a comparative study (Miller, 2007). ...
Article
Spider mating behaviour is varied and often surprising. In the past few decades, there has been a shift from descriptive natural history approaches to a more manipulative, theory-based dissection of the behavioural and evolutionary ecology of mating. This approach has yielded evidence in support of important underlying themes of sexual selection. In this chapter, we summarise patterns of mating behaviour in spiders, and the conditions that underlie variation in this behaviour, with an emphasis on how sexual selection theory relates to observed patterns. We end by suggesting spiders may prove particularly tractable models for testing hypotheses regarding mechanisms of sexual selection, sex-specific mating tactics, and reciprocal links between these, and ecology, demography and life history. Introduction. There are a number of traits common to the true spiders (Order Araneae) that lend unusual dimensions to their mating behaviour (e.g. Uhl and Elias, Chapter 5). Almost all spiders are predacious (for an exception see Meehan et al., 2009), and have sensory systems exquisitely tuned to vibrational and pheromonal signals. Males transfer sperm via specialised intromittent organs (males' palps), not directly connected to the gonads, into females' sperm storage organs of variable number (spermathecae), often via independent insemination tubules (Foelix, 1996). In addition, although the mating season holds risks similar to those for all sexual species (e.g. mate rejection, competitive injury, predation), male spiders (and rarely, females; Aisenberg et al., 2009, Cross et al. 2007b, Jackson and Pollard, 1990, Schutz and Taborsky, 2005) also face the additional risk of mortality through their predacious potential mate.
... Female monopolization avoidance mechanisms in spiders include mate choice through precopulatory sexual aggression and cannibalism 24 , post-copulatory cryptic female choice 25 , and genital morphologies that decrease male plug effectiveness 26 . Male genital plugs in C. darwini are deemed inefficient because females readily remate and genital plugs can be removed by subsequent males. ...
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Several clades of spiders whose females evolved giant sizes are known for extreme sexual behaviors such as sexual cannibalism, opportunistic mating, mate-binding, genital mutilation, plugging, and emasculation. However, these behaviors have only been tested in a handful of size dimorphic spiders. Here, we bring another lineage into the picture by reporting on sexual behavior of Darwinâ €™ s bark spider, Caerostris darwini. This sexually size dimorphic Madagascan species is known for extreme web gigantism and for producing the worldâ €™ s toughest biomaterial. Our field and laboratory study uncovers a rich sexual repertoire that predictably involves cannibalism, genital mutilation, male preference for teneral females, and emasculation. Surprisingly, C. darwini males engage in oral sexual encounters, rarely reported outside mammals. Irrespective of femaleâ €™ s age or mating status males salivate onto female genitalia pre-, during, and post-copulation. While its adaptive significance is elusive, oral sexual contact in spiders may signal male quality or reduce sperm competition.
... If somatic sizes evolve mismatches (SSD), then the smaller sex (males) may be expected to compensate in genital size. Furthermore, the effectiveness of male genital plugs, as known in nephilid spiders, would be compromised in the case of considerable genital size mismatch between the sexes [33,67] because male genital plugs could be bypassed by emboli of rivals. The picture is complicated because both intromittent and non-intromittent palpal parts may be seen as contributors to SGD, but it seems evident that the intromittent parts compensate in size evolution in order to avoid genital size mismatches. ...
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Background In most animal groups, it is unclear how body size variation relates to genital size differences between the sexes. While most morphological features tend to scale with total somatic size, this does not necessarily hold for genitalia because divergent evolution in somatic size between the sexes would cause genital size mismatches. Theory predicts that the interplay of female-biased sexual size dimorphism (SSD) and sexual genital size dimorphism (SGD) should adhere to the ‘positive genital divergence’, the ‘constant genital divergence’, or the ‘negative genital divergence’ model, but these models remain largely untested. We test their validity in the spider family Nephilidae known for the highest degrees of SSD among terrestrial animals. ResultsThrough comparative analyses of sex-specific somatic and genital sizes, we first demonstrate that 99 of the 351 pairs of traits are phylogenetically correlated. Through factor analyses we then group these traits for MCMCglmm analyses that test broader correlation patterns, and these reveal significant correlations in 10 out of the 36 pairwise comparisons. Both types of analyses agree that female somatic and internal genital sizes evolve independently. While sizes of non-intromittent male genital parts coevolve with male body size, the size of the intromittent male genital parts is independent of the male somatic size. Instead, male intromittent genital size coevolves with female (external and, in part, internal) genital size. All analyses also agree that SGD and SSD evolve independently. Conclusions Internal dimensions of female genitalia evolve independently of female body size in nephilid spiders, and similarly, male intromittent genital size evolves independently of the male body size. The size of the male intromittent organ (the embolus) and the sizes of female internal and external genital components thus seem to respond to selection against genital size mismatches. In accord with these interpretations, we reject the validity of the existing theoretical models of genital and somatic size dimorphism in spiders.
... In many spiders , males seal the female genital opening after copulation , in order to avoid sperm concurrence and secure their paternity (Uhl et al. 2010 ). One type of such sealing mechanism is the controlled breakage of the embolus tip (Schneider et al. 2001 ;Kuntner et al. 2009 ) or the autotomy of the whole pedipalp (Knofl ach and Van Harten 2001 ), which then stays attached to the epigyne. The embolus tip 2.3 Other Interlocking Devices might stay attached, because it is pressed and locked in the narrow duct, due to the elasticity of both embolus and duct wall material. ...
Chapter
Rigid cuticular structures that generate high friction by mechanical interlocking with substrate protuberances are the most abundant attachment devices in arthropods. Here we review the different types of such structures in arachnids. The claws of appendages are primarily to increase foothold on walking and climbing substrates, but may also be important means of prey capture, which often comes with structural modifications. Claws are often supported by spines and microtrichia, all of which have different tip diameters. Such a set of differently sized interlocking devices may generate friction on a broad range of substrate roughness from very fine to rather coarse. Other examples of interlocking mechanisms are hooks and platelets on different body parts, some types of genital sealing (mating plugs), and silk threads interlocking with protuberances of substrate surfaces. Clamps and pincers are muscle-driven attachment devices, which are abundant means of prey capture and food handling: the chelicerae, the pedipalpal chelae of scorpions and pseudoscorpions, the raptorial legs (spinated legs or pedipalps for prey capture), and the cucullus (‘hood’) of Ricinulei. Other mechanical attachment devices are expansion anchors that are first pierced into a substrate, such as prey cuticle, plant epidermis or host skin, and interlocked there. They are represented by some specialized mouth parts. Lock-and-key is a system, in which two specific co-adapted structures interlock with each other. They can be found in some copulation organs. Wrapping around the substrate is an effective means of attachment, as it can highly enhance the action of friction. This mechanism is frequently used by long-legged harvestmen, when walking on thin cylindrical surfaces like grass or herb stems. It is further utilized by some spiders which tightly wrap their prey in silk.
... For instance, mate guarding might reduce the glycogen reserves of males in stream-dwelling isopods [12]. Some male spiders form mating plugs by breaking their pedipalps and leaving breakages in the copulatory openings of females [13,14]. Male Nephilengys malabarensis also detach their entire pedipalp, which continues sending sperm into a female. ...
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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.
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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.
Article
Intra‐specific variation pattern is informative to understanding the evolution of morphological traits, but has been rarely studied in jumping spiders. Here we investigate the intra‐specific variation of non‐genitalic and genitalic traits in two euophryine jumping spider species that show considerable difference in sexual dimorphism: Chapoda recondita (Peckham & Peckham, 1896) and Antillattus cambridgei (Bryant, 1943). The results show the pre‐copulatory sexually selected traits (e.g. male chelicerae) tend to have positive intra‐specific allometry, and thus may have evolved under strong directional selection. The genitalic traits and some non‐genitalic traits tend to show negative allometries. Unlike non‐genitalic traits, the genitalic traits usually have high size‐corrected intra‐specific variation (CV’). Factors that may account for the negative allometry and high size‐corrected intra‐specific variation in genitalic traits are discussed. Pre‐ and post‐copulatory sexual selection may coexist in species and whether there is a trade‐off between these two selection mechanisms remains to be investigated. We found that the genitalic and non‐genitalic traits show different intra‐specific variation patterns in two euophryine jumping spider species, Chapoda recondita and Antillattus cambridgei. The genitalic traits show negative intra‐specific allometry but high size‐corrected intra‐specific variation, whereas the pre‐copulatory sexually‐selected traits (e.g. male chelicerae) that may have evolved under strong directional selection show positive allometry.
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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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Although the diversity of spider orb web architectures is impressive, few lineages have evolved orb webs larger than 1m in diameter. Until recently, such web gigantism was reported only in a few nephilids and araneids. However, new studies on bark spiders (Caerostris) of Madagascar report a unique case of web gigantism: Darwin's bark spider (C. darwini) casts its webs over substantial water bodies, and these webs are made from silk whose toughness outperforms all other known spider silks. Here we investigate C. darwini web architecture and provide data to begin to answer two intriguing questions to explain these extraordinary web characteristics: 1) Are C. darwini webs specialized to subdue unusually large, perhaps even vertebrate, prey? 2) Do these large, riverine webs allow the spiders to capitalize on catching numerous small semi-aquatic insects? During fieldwork in Madagascar, we studied C. darwini web architecture and ecology, as well as interactions with prey. We characterize C. darwini webs as having relatively simple capture areas with very open sticky spirals and few radial lines. We also compare web features in several sympatric Caerostris species, among which C. darwini represents the most extreme case of web gigantism, with the largest orbs up to 2.76 m2 and longest bridge lines reaching 25.5 m. While preliminary, current data suggest that C. darwini webs are effective snares for semi-aquatic insects such as mayflies and dragonflies, while vertebrate prey were never observed. We suggest that mass emergence of aquatic insects may function analogously to the capture of rare, large prey that recent studies suggest are critical for reproduction in orb weaving spiders.
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Classic explanations of variation in mating systems critically depend on variation in demography. Here, we emphasize how understanding dynamic links between fluctuating population structure and mating tactics, life history, morphology, and sensory capabilities may be advanced using spiders as models. The impressively diverse range of mating systems and tactics among spiders, coupled with unique and manipulable aspects of their biology, may yield important insights into mating system evolution.
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Monogynous males in various species actively limit themselves to mating with a single female in their lifetime. Whereas previous models have considered monogyny as an obligate mating strategy, here we explore the potential of monogyny to evolve as a context-specific (conditional) behavior. Using a state-dependent dynamic game model based on the biology of the cannibalistic spider Argiope bruennichi, we confirm that conditional monogyny can evolve under broad conditions, including an even sex ratio. We predict that males should make a terminal investment when mating with large, virgin females, especially if population density is low and the encounter occurs late in the season. We encourage empirical tests for the existence of conditional monogyny in all species where monogyny occurs in the absence of strict morphological constraints that would make it obligatory.
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Spiders are the preeminent silk craftsmen among arthropods and are best known for producing aerial orb webs that snare flying insects. Orb web spiders are ubiquitous predators in terrestrial ecosystems and are popular models for behavioural and ecological research, in part due to the ease of characterizing the shapes of orb webs. Orb webs are composite structures built from multiple types of silks, each with its own unique molecular structure and mechanical function, such that orb webs also link together evolutionary research from the genes coding for silk proteins to whole web function in the environment. Yet, orb webs are only intermediate structures in the evolutionary diversification of silk use among spiders, acting as stepping stones facilitating the origin of new web types and increased spider diversification. Here, we review the current research on the form and function of spider orb webs. We provide a comprehensive introduction to all aspects of orb web biology, suitable for any new investigation into orb web biology. While other reviews exist individually for webs, silk, and spider evolution, we hope that the synthetic nature of this review will facilitate a more integrated approach by future investigators. Finally, we explore in more detail some of the most dynamic areas of orb web biology to suggest promising venues for the next decade of research on these fascinating creatures and their silken snares. In particular, we discuss how spider webs might drive speciation, the dramatic growth in our understanding of the molecular ecology of spider silk, and the importance of a greater role for spider biology per se in silk biomimicry.
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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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Morphology and its relevance for systematics is a promising field for the application of biosemiotic principles in scientific practice. Genital coupling in spiders involves very complex interactions between the male and female genital structures. As exemplified by two spider species, Nephila clavipes and Nephila pilipes ssp. fenestrata, from a biosemiotic point of view the microstructures of the male bulb’s embolus and the corresponding female epigynal and vulval parts form the morphological zone of an intraspecific communication and sign-interpreting process that is one of the prerequisites for sperm transfer. Hence these morphological elements are of high taxonomic value, as they play an essential role in mating and fertilization and consequently in establishing and preserving a reproductive community. Morphology clearly benefits from a biosemiotic approach, as biosemiotics helps to sort out species-specific morphological characters and to avoid problematic typological interpretations.
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Sexual selection research has always been a subject for debate. Much of the criticism has concerned the imposition of conventional sex roles based on an anthropomorphic view of animals imposed by the researcher. This conventional view may have hampered research, for example from acknowledging male mate choice. Sexual conflict theory is a fast-growing research field, which initially stems from sexual selection research. We investigated how the sexes are described in sexual conflict research and what characteristics they are assigned. We assessed these topics with literature studies of (1) the terminology used and (2) what parameters are incorporated in sexual conflict models. We found that males and females are consequently described with different words, which have different connotations regarding activity in the conflict. Furthermore, theoretical models mainly investigate conflict costs for females, although costs for both sexes are necessary for coevolutionary dynamics. We argue that sexual conflict research uses stereotypic characterizations of the sexes, where males are active and females reactive. Thus, previous discussions on the use of anthropomorphic terms in sexual selection seem not to have had any impact on sexual conflict research, which is why the topic of stereotyping the sexes is still of current importance. We suggest that scientific gains can be made by eliminating a sex-stereotyped perspective.
Chapter
This book demonstrates that there is an enormous diversity of attachment devices and adhesives among arachnids. This diversity is comparable to what has previously been found in insects. In this chapter, we discuss the evolutionary driving forces that might have been acted on both the occurrence and shaping of such structures and secretions, in relation to their biological functions. We discuss instances, where the evolution of such structures might have been driven by another precursor function. Examples for this are the locomotory attachment pads of spiders, in which the original function might have been prey capture, or those of amblypygids, where the original function was obviously attachment to the mother cuticle. We discuss the role of sexual selection, as well as herbivore-plant, predator-prey and parasite-host interactions in the evolution of attachment devices and adhesive secretions in arachnids. Further, we discuss the role of attachment devices in dispersal and microhabitat access.
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The male reproductive system and spermatozoa of spiders are known for their high structural diversity. Spider spermatozoa are flagellate and males transfer them to females in a coiled and encapsulated state using their modified pedipalps. Here, we provide a detailed overview of the present state of knowledge of the primary male reproductive system, sperm morphology and the structural diversity of seminal fluids with a focus on functional and evolutionary implications. We conceptualized characters for the male genital system, spermiogenesis and spermatozoa for the first time based on published and new data. In total, we scored 40 characters for 132 species from 56 families representing all main spider clades. We obtained synapomorphies for several taxa including Opisthothelae, Araneomorphae, Dysderoidea, Scytodoidea, Telemidae, Linyphioidea, Mimetidae, Synotaxidae and the Divided Cribellum Clade. Furthermore, we recovered synspermia as a synapomorphy for ecribellate Haplogynae and thus propose Synspermiata as new name for this clade. We hope that these data will not only contribute to future phylogenetic studies but will also stimulate much needed evolutionary studies of reproductive systems in spiders.
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Pre‐copulatory cannibalism – females devouring males during courtship – may bring no benefit to either sex. The ‘aggressive spillover hypothesis’ (ASH) posits that pre‐copulatory cannibalism represents a spillover of female aggressiveness from the juvenile foraging context, when aggressiveness is advantageous, to the adult mating context, when aggressiveness may be non‐adaptive or maladaptive. The ASH suggests that individuals exhibit limited plasticity in aggressive behaviours because they are genetically canalised for indiscriminate aggressiveness towards prey and conspecifics, including males. Hence, a tendency to employ pre‐copulatory cannibalism is a part of the female aggression syndrome, an assertion generally accepted in the personality field. We here re‐evaluate the previous findings in the light of personality criteria, which we propose for ASH validation: between‐individual differences, repeatability and heritability in tendency for pre‐copulatory attacks (and pre‐copulatory cannibalism) and voracity towards prey, and their correlation. To re‐evaluate ASH and to allow for additional or alternative explanations, we ask whether pre‐copulatory cannibalism depends on female hunger, mating status, size and/or male quality. Finally, we ask whether cannibalistic females have a reduced reproductive success as predicted by the ASH. While repeatability and heritability in voracity towards prey and its correlation with the tendency to engage in pre‐copulatory cannibalism were found in certain systems, we lack any evidence for repeatability and heritability in pre‐copulatory cannibalistic attempts and for its maladaptiveness. Rather than only resorting to the ASH, foraging and mate choice hypotheses may also explain pre‐copulatory cannibalism. We suggest clarifying the use of the terms sexual cannibalism (effect) and female aggressiveness or tendency to attack and devour males (cause), and argue that male strategies to avoid cannibalism should be considered. We propose testing the ASH as the explanation for pre‐copulatory cannibalism in those cases where female tendency to devour males correlates with actual pre‐copulatory cannibalism and when all the above criteria are fulfilled. Finally, we propose future directions for studying the ASH.
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Studies that investigate patterns of paternity in polyandrous species typically employ double-mating trials, in which the paternity share of each male is established by either the sterile male technique or using genetic markers. However, polyandrous females may mate with more than two males and, in some species, triple-mating trials produce different patterns of paternity from double-mating trials. We investigated patterns of paternity share in triple-mating trials of the sexually cannibalistic orb-web spider Nephila plumipes. These experiments reveal little quantitative changes to paternity share when more than two males mate with the female; the third male apparently diluted the fertilisation success of the second male but not of the first male. Sexual cannibalism had little impact on the fertilisation success of the first male, but greatly increased the fertilisation success of the third male. When offered a choice, males did not prefer to mate with virgin over mated females, but males that chose virgin females were significantly heavier than those that chose mated females.
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Rapid divergent evolution of male genitalia is one of the most general evolutionary trends in animals with internal fertilization; the shapes of genital traits often provide the only reliable characters for species identification. Yet the evolutionary processes responsible for this pattern remain obscure. The long-standing lock-and-key hypothesis, still popular among taxonomists, suggests that genitalia evolve by pre-insemination hybridization avoidance; that is, hybrid inferiority drives the evolution of male genitalia with a proper mechanical fit to female genitalia. The sexual selection hypothesis,, in contrast, proposes that divergent evolution of genitalia is the result of sexual selection, brought about by variation in postinsemination paternity success among males. Here, by comparing pairs of related clades of insects that differ in mating system, I assess how the opportunity for postmating sexual selection affects the rate of divergent evolution of male genitalia. Genital evolution is more than twice as divergent in groups in which females mate several times than in groups in which females mate only once. This pattern is not found for other morphological traits. These findings provide strong empirical evidence in favour of a postmating sexual selection mechanism of genital evolution.
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We examined the importance of size dependent sexual cannibalism as a selection pressure leading to extreme male size variablility in Nephila. A laboratory study on Australian Nephila edulis showed pre-copulalory cannibalism to be extremely low (1%); and post-copulatory cannibalism to be notable (12.2% per mating, 5.2% per insertion bout) but not correlated to male size. Females attacked large first males less often than small first males. Fewes large second males were killed but were more often injured than small second males. A field study on American Nephila clavipes confirmed this trend by showing respectable male residency in female webs with the larger males "surviving" longer than smaller ones. Thus small males (which have been shown to suffer from male-male competition) do not benefit from reduced sexual cannibalism. We conclude that the tremendous variability in male size distribution is coupled to size related opportunism and thus plays a major role in Nephila life history tactics.
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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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The past decade has seen a profound change in the scientific understanding of reproduction. The traditional view of reproduction as a joint venture undertaken by two individuals, aimed at replicating their common genome, is being challenged by a growing body of evidence showing that the evolutionary interests of interacting males and females diverge. This book demonstrates that, despite a shared genome, conflicts between interacting males and females are ubiquitous, and that selection in the two sexes is continuously pulling this genome in opposite directions. These conflicts drive the evolution of a great variety of those traits that distinguish the sexes and also contribute to the diversification of lineages. Göran Arnqvist and Locke Rowe present an array of evidence for sexual conflict throughout nature, and they set these conflicts into the well-established theoretical framework of sexual selection. The recognition of conflict between the sexes is transforming our theories for the evolution of mating systems and the sexes themselves. Written by two top researchers in the field, Sexual Conflict is the first book to describe this transformation. It is a must read for all scholars and students interested in the evolutionary biology of reproduction.
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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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SEXUAL dimorphism in body size is widespread in the animal kingdom. Whereas male giantism has been studied and explained extensively1,2, male dwarfism has not. Yet it is neither rare3–7 nor without theoretical interest8,9. Here we provide experimental and comparative data on spiders to support the theory that dwarf males are associated with high differential adult mortality, with males at much greater risk. Species with sedentary (low-risk) females have dwarf, roving (high-risk) males. Life-history theory could readily explain dwarfing if juvenile, but not adult, male mortality were large. We present a new model in which high mortality of searching mature males reduces the adult sex ratio (males: females), relaxing male–male competition and reducing the importance of male body size to favour dwarfing by early maturation. Early maturity also reduces male juvenile mortality and thus opposes adult mortality. This provides a mechanism that buffers skews in adult sex ratio and which is quite distinct from Fisher's principle10 and allied mechanisms9,11 for the primary sex ratio.
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The degree and direction of sexual dimorphism varies widely but in several taxa of orb-weaving spiders, including Nephila, males may be less than one-tenth the size of females. This difference is commonly attributed to selection through precopulation sexual cannibalism: females may either fail to detect very small males, or ignore them as potential prey items. However, there is often the potential for male-male competition in these species-because several males can be found on the web of a single female. We investigated experimentally the effects of sexual cannibalism and male-male competition on male body size and hence sexual dimorphism in the Australian golden orb-weaver (Nephila plumipes). Small males were less likely to be detected and cannibalized than larger males. However, larger males excluded small males from the central hub of the web, where mating takes place. The conflicting effects of sexual cannibalism and male-male competition may be responsible for the relatively large variation in male body size in this species.
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Abstract Sexual size dimorphism (SSD) can strongly influence the evolution of reproductive strategies and life history. If SSD is extreme, and other characters (e.g., genitalic size) also increase with size, then functional conflicts may arise between the sexes. Spiders offer an excellent opportunity to investigate this issue because of their wide range of SSD. By using modern phylogenetic methods with 16 species of orb-weaving spiders, we provide strong evidence for the “positive genitalic divergence” model, implying that sexual genitalic dimorphism (SGD) increases as SSD increases. This pattern is supported by an evolutionary mismatch between the absolute sizes of male and female genitalia across species. Indeed, our findings reveal a dramatic reversal from male genitalia that are up to 87X larger than female genitalia in size-monomorphic species to female genitalia that are up to 2.8X larger in extremely size-dimorphic species. We infer that divergence in SGD could limit SSD both in spiders, and potentially in other taxa as well. Further, male and female body size, as well as male and female genitalia size, are decoupled evolutionarily. Finally, we show a negative scaling (hypoallometry) of male and female genitalic morphology within sexes. Evolutionary forces specific to each sex, such as larger female size (increased fecundity) or smaller male size (enhanced mate-searching ability), may be balanced by stabilizing selection on relative genitalic size.
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A consequence of multiple mating by females can be that the sperm of two or more males directly compete for the fertilisation of ova inside the female reproductive tract. Selection through sperm-competition favours males that protect their sperm against that of rivals and strategically allocate their sperm, e.g., according to the mating status of the female and the morphology of the spermatheca. In the majority of spiders, we encounter the otherwise unusual situation that females possess two independent insemination ducts, both ending in their own sperm storage organ, the spermatheca. Males have paired mating organs, but generally can only fill one spermatheca at a time. We investigated whether males of the African golden orb-web spider Nephila madagascariensis can prevent rival males from mating into the same spermatheca and whether the mating status of the female and/or the spermatheca causes differences in male mating behaviour. There was no significant difference in the duration of copulations into unused spermathecae of virgin and mated females. We found that copulations into previously inseminated spermathecae were generally possible, but shorter than copulations into the unused side of mated females or with virgins. Thus, male N. madagascariensis may have an advantage when they mate with virgins, but cannot prevent future males from mating. However, in rare instances, parts of the male genitals can completely obstruct a female genital opening.
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Male genitalia may facilitate sperm protection by acting as a plug that prevents or hinders future matings. The pedipalps (intromittant organs) of males of the orb-web spider, Nephila plumipes, have a conductor with a peculiarly curved ending and a triangular process near the terminal end. The tip of the conductor, including the process, breaks during most matings and remains inside the female genital tract. We explored the possible function of the conductor as a mating plug using the double-mating sterile-male technique. Our data are not consistent with a plug function because males use only one pedipalp in each mating, thus leaving an unobstructed insemination duct available for future matings; conductors of males mating with virgin females are not more likely to break than those of males mating with mated females, and second males show no preference for used or unused spermathecae. In addition, males that inserted their palp in the insemination duct that contained a tip of the conductor from a previous male obtained a share in the paternity of the female's clutch of eggs. Interestingly, the conductor is more likely to break if it is inserted in an unused spermatheca. We argue that several lines of evidence suggest that the conductor breaks as a result of intersexual conflict over the duration of copulation.
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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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Extreme sexual body size dimorphism (SSD), in which males are only a small fraction of the size of the females, occurs only in a few, mostly marine, taxonomic groups. Spiders are the only terrestrial group in which small males are relatively common, particularly among orb-weavers (especially in the families Tetragnathidae and Araneidae) and crab spiders (Thomisidae). We used a taxonomic sample of 80 genera to study the phylogenetic patterns (origins and reversals) of SSD in orb-weaving spiders (Orbiculariae). We collected and compiled male and female size data (adult body length) for 536 species. Size data were treated as a continuous character, and ancestral sizes, for males and females separately, were reconstructed by using Wagner parsimony on a cladogram for the 80 genera used in this study. Of these 80 genera, 24 were female-biased dimorphic (twice or more the body length of the male); the remaining 56 genera were monomorphic. Under parsimony only four independent origins of dimorphism are required: in the theridiid genus Tidarren, in the distal nephilines, in the "argiopoid clade," and in the araneid genus Kaira. Dimorphism has reversed to monomorphism at least seven times, all of them within the large "argiopoid clade." The four independent origins of dimorphism represent two separate instances of an increase in female size coupled with a decrease of male size (involving only two genera), and two separate instances of an increase in female size with male size either remaining the same or increasing, but not as much as females (involving 30 genera). In orb-weaving spiders, far more taxa are sexually dimorphic as a result of female size increase (22 genera) than as a result of male size decrease (two genera). SSD in orb-weaving spiders encompasses several independent evolutionary histories that together suggest a variety of evolutionary pathways. This multiplicity strongly refutes all efforts thus far to find a general explanation for either the origin or maintenance (or both) of SSD, because the different pathways very likely will require distinctly different, possibly unique, explanations. Each pattern must be understood historically before its origin and maintenance can be explained in ecological and evolutionary terms. The most frequently cited example of male dwarfism in spiders, the golden orb-weaving spider genus Nephila (Tetragnathidae), is in fact a case of female giantism, not male dwarfism.
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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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The traditional paradigm of male polygamy and female monogamy has been replaced by the recognition that both sexes may typically mate with several partners. As a consequence, much attention has focused on the evolution of polyandry, while the evolutionary significance of monogyny (male monogamy) remains poorly understood. Monogyny, a taxonomically widespread mating system that includes dramatic examples of male self-sacrifice, is predicted when the benefits of paternal investment exceed those of searching for additional mates. However, monogyny also occurs in animals lacking paternal investment, instead representing a form of paternity protection. It has been suggested that such mating systems are expected where the costs of mate search for males are high. However, this argument fails to recognize that if there is a low probability of a male finding a mate, then there may be a high probability that he will not need to defend his paternity. Using a mathematical model, we show that monogyny as a means of increasing paternity is favored when the sex ratio is male biased, but not necessarily by high search costs. The importance of a male-biased sex ratio for the evolution of monogyny is supported by various empirical studies.
Article
Recent theoretical and empirical interest in postmating processes have generated a need for increasing our understanding of the sources of variance in fertilization success among males. Of particular importance is whether such postmating sexual selection merely reinforces the effects of premating sexual selection or whether other types of male traits are involved. In the current study, we document large intraspecific variation in last male sperm precedence in the water strider Gerris lateralis. Male relative paternity success was repeatable across replicate females, showing that males differ consistently in their ability to achieve fertilizations. By analyzing shape variation in male genital morphology, we were able to demonstrate that the shape of male intromittent genitalia was related to relative paternity success. This is the first direct experimental support for the suggestion that male genitalia evolve by postmating sexual selection. A detailed analysis revealed that different components of male genitalia had different effects, some affecting male ability to achieve sperm precedence and others affecting male ability to avoid sperm precedence by subsequent males. Further, the effects of the shape of the male genitalia on paternity success was in part dependent on female morphology, suggesting that selection on male genitalia will depend on the frequency distribution of female phenotypes. We failed to find any effects of other morphological traits, such as male body size or the degree of asymmetry in leg length, on fertilization success. Although males differed consistently in their copulatory behavior, copulation duration was the only behavioral trait that had any significant effect on paternity.
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 sequential 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
Recent theoretical and empirical interest in postmating processes have generated a need for increasing our understanding of the sources of variance in fertilization success among males. Of particular importance is whether such postmating sexual selection merely reinforces the effects of premating sexual selection or whether other types of male traits are involved. In the current study, we document large intraspecific variation in last male sperm precedence in the water strider Gerris lateralis. Male relative paternity success was repeatable across replicate females, showing that males differ consistently in their ability to achieve fertilizations. By analyzing shape variation in male genital morphology, we were able to demonstrate that the shape of male intromittent genitalia was related to relative paternity success. This is the first direct experimental support for the suggestion that male genitalia evolve by postmating sexual selection. A detailed analysis revealed that different components of male genitalia had different effects, some affecting male ability to achieve sperm precedence and others affecting male ability to avoid sperm precedence by subsequent males. Further, the effects of the shape of the male genitalia on paternity success was in part dependent on female morphology, suggesting that selection on male genitalia will depend on the frequency distribution of female phenotypes. We failed to find any effects of other morphological traits, such as male body size or the degree of asymmetry in leg length, on fertilization success. Although males differed consistently in their copulatory behavior, copulation duration was the only behavioral trait that had any significant effect on paternity.
Article
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
In the current resurgence of interest in the biological basis of animal behavior and social organization, the ideas and questions pursued by Charles Darwin remain fresh and insightful. This is especially true of The Descent of Man and Selection in Relation to Sex, Darwin's second most important work. This edition is a facsimile reprint of the first printing of the first edition (1871), not previously available in paperback. The work is divided into two parts. Part One marshals behavioral and morphological evidence to argue that humans evolved from other animals. Darwin shoes that human mental and emotional capacities, far from making human beings unique, are evidence of an animal origin and evolutionary development. Part Two is an extended discussion of the differences between the sexes of many species and how they arose as a result of selection. Here Darwin lays the foundation for much contemporary research by arguing that many characteristics of animals have evolved not in response to the selective pressures exerted by their physical and biological environment, but rather to confer an advantage in sexual competition. These two themes are drawn together in two final chapters on the role of sexual selection in humans. In their Introduction, Professors Bonner and May discuss the place of The Descent in its own time and relation to current work in biology and other disciplines.
Article
Mating behaviour is analysed and compared in six species of the Theridion varians-group: Theridion melanostictum O. P.-Cambridge, The petraeum L. Koch, T. pictum (Walckenaer), T. pinastri L. Koch, T. refugum Drensky and T. varians Hahn. Copulation consists of numerous sequences of palpal insertions (copulatory sequences). Each sequence is followed by a sperm induction, except the last one which is terminated by formation of the mating plug. Number and duration of copulatory sequences and palpal insertion pattern exhibit considerable differences between species, as well as the number of insertion attempts. The first sequence of insertions not preceded by sperm induction is a pseudocopulation, a sequence without sperm transfer. As evidence of lack of insemination, pseudocopulated females did not lay an egg-cocoon. The mating plug is produced by secretions of the male and female genital tract. The male secretion is transferred to the palps via a ‘sperm web’ and to the epigyne by palpal applications. It is responsible for hardening of the plug. Plugged females will not copulate with another mate. In contrast to other araneoid spiders, contralateral insertion (left embolus inserts into right introductory duct and vice versa) is the rule in these species.
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
Nephila edulis is a spider with large body size variability in males and females. Genital characters show negative allometric values compared to somatic characters. In males, the embolus (the most important structure for sperm transfer) had a significantly lower coefficient of variation than body size. This suggests that male genitalia are under stabilizing selection favouring intermediate size. Female N. edulis showed a trend similar to males regarding allometric values in genitalia. In females, however, the variation coefficient in a specific genital character crucial for successful copulation did not differ from that of indicators for overall body size. This suggests that in Nephila the genitalia of the females experience less stabilizing selection than those of the males. In male and female genitalia, the mode of selection seems to cause developmental instability not in degrees of fluctuating asymmetry but in the degree of data scatter which indicates a lower coefficient of determination.
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.