Matjaž Gregorič

Mate quality, not aggressive spillover, explains sexual cannibalism in a size dimorphic spider

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.

Eunuchs are better fighters

Male–male competition for females can significantly affect a male’s reproductive success and hence his fitness. Game theory predicts that an individual should avoid fighting when its future reproductive potential is high, but should fight forcefully when its future reproductive potential is insignificant. When mates are scarce, extreme competition and fatal fighting is expected. We recently showed that Nephilengys malabarensis eunuchs, i.e. sterile spider males that lost their genitals during copulation, become more aggressive during male–male contests. Here, we add crucial comparative data by exploring eunuch fighting behaviour in Nephilengys livida from Madagascar, specifically by testing the ‘better fighter hypotheses’ in a laboratory setting. Similar to N. malabarensis, N. livida copulations resulted in total male castration with the severed palp plugging the female genitals in 70.83% cases, which mostly (63.63%) prevented subsequent copulations. Unexpectedly, however, N. livida eunuchs exhibited lower aggressiveness than virgin males. We interpret these results in the light of different mating biology between the so far studied species known for the eunuch phenomenon, which might reflect differing plug effectiveness due to variation in genital anatomy in N. livida, N. malabarensis and Herennia multipuncta. However, detected differences in aggressive behaviour of N. livida versus N. malabarensis eunuchs might also be explained by the species’ ecology, with lower population densities resulting in a relaxed male–male competition making excessive aggression and mate guarding redundant. This study thus questions the generality of overt aggressiveness in mated males with no reproductive value, and highlights the importance of understanding the natural history of species in the question.

Mass predicts web asymmetry in Nephila spiders

The architecture of vertical aerial orb webs may be affected by spider size and gravity or by the available web space, in addition to phylogenetic and/or developmental factors. Vertical orb web asymmetry measured by hub displacement has been shown to increase in bigger and heavier spiders; however, previous studies have mostly focused on adult and subadult spiders or on several size classes with measured size parameters but no mass. Both estimations are suboptimal because (1) adult orb web spiders may not invest heavily in optimal web construction, whereas juveniles do; (2) size class/developmental stage is difficult to estimate in the field and is thus subjective, and (3) mass scales differently to size and is therefore more important in predicting aerial foraging success due to gravity. We studied vertical web asymmetry in a giant orb web spider, Nephila pilipes, across a wide range of size classes/developmental stages and tested the hypothesis that vertical web asymmetry (measured as hub displacement) is affected by gravity. On a sample of 100 webs, we found that hubs were more displaced in heavier and larger juveniles and that spider mass explained vertical web asymmetry better than other measures of spider size (carapace and leg lengths, developmental stage). Quantifying web shape via the ladder index suggested that, unlike in other nephilid taxa, growing Nephila orbs do not become vertically elongated. We conclude that the ontogenetic pattern of progressive vertical web asymmetry in Nephila can be explained by optimal foraging due to gravity, to which the opposing selective force may be high web-building costs in the lower orb. Recent literature finds little support for alternative explanations of ontogenetic orb web allometry such as the size limitation hypothesis and the biogenetic law.

Mating Plugs in Polyandrous Giants: Which Sex Produces Them, When, How and Why?

Background 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. Methodology 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. Conclusions 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.

Nephilid spider eunuch phenomenon induced by female or rival male aggressiveness

Abstract Plugging of female genitals via male sexual mutilation is a common sexual repertoire in some nephilid spiders (Herennia, Nephila, Nephilengys), but the behavioral pathways leading to emasculation are poorly understood. Recent work suggests that copulating Herennia males damage their reproductive organs during copulation and then voluntarily, and stereotypically, remove their pedipalps to become eunuchs. Presumably, such emasculation increases agility allowing the male to better fend off rival males. However, through our observation of male antagonism in Nephilengys borbonica (Vinson 1863) in La Reunion (Indian Ocean), we discovered that genital severance involving the entire male palp is induced by a rival eunuch. Additionally, laboratory matings of the same species from Mayotte provide the first observations of female sexual cannibalism in this species, one such forceful copulation termination leading to emasculation of the entire palp. These novel behaviors suggest that mate plugging and the eunuch phenomenon are more plastic repertoires than hitherto thought, and thus our observations add to possible pathways leading to them. Based on our examination of 791 samples of Nephilengys spp. from museum collections and of a freshly collected representative sample of N. borbonica, we conclude that i) palpal severance is common (50% of males from the wild were eunuchs lacking both palps), but ii) the females (or perhaps subsequent males) must possess a mechanism for removing severed palps from the epigyna (none had a whole palpal bulb), leaving behind only partial, embolic plugs, and iii) the disparity between male palpal damage (50%) and visible mating plugs in females (21%) merits further research as the relative numbers of severed males and plugged females can offer insight into which sex may have the upper hand in an evolutionary arms race.

Darwin's bark spider: giant prey in giant orb webs (Caerostris darwini, Araneae: Araneidae)?

Abstract 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: Darwins 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.

Orb web features as taxonomic characters in Zygiella s.l. (Araneae: Araneidae)

Abstract The species classically grouped in the genus Zygiella F.O. Pickard-Cambridge 1902 are thought to all possess a characteristic orb web feature – a spiral-free sector in the upper part of the orb. Zygiella s.l. has recently been split into four genera, Zygiella s.s., Leviellus Wunderlich 2004, Parazygiella Wunderlich 2004 and Stroemiellus Wunderlich 2004, and proposed to belong to family Zygiellidae, rather than the classical Araneidae. To find orb web features that could potentially diagnose these species and/or genera, we investigated female web architectures of L. thorelli, P. montana, S. stroemi, Z. keyserlingi and Z. x-notata. We investigated a total of 278 female webs and compared 16 characters emphasizing web size, web and hub asymmetry, as well as radial and spiral counts. The free sector may be present in all species but its prevalence in female webs varied from 41% in Z. keyserlingi to 94% in P. montana. Various combinations of web architecture characters may diagnose those species that in our sample represented all four genera: Zygiella s.s. may be diagnosed by the median number of non-circulating sticky spirals below hub, Stroemiellus by the small web size with small mesh width and the non-circulating spirals above hub, Parazygiella by few primary radii and sticky spirals, and Leviellus by a pronounced vertical hub displacement. This suite of diagnostic features may provide preliminary support for the current taxonomy of Zygiella s.l., although the ultimate test, i.e., a phylogeny, is needed to test the validity of the genera. Seven out of 16 web characters are potentially phylogenetically informative because they show a statistically significant shared variation among species. Our study, which pioneers the quantification of web data to distinguish species, implies that the interspecific variation in webs may turn out to reflect phylogenetic relationships among Zygiella s.l.

Targeting a portion of central European spider diversity for permanent preservation

Abstract Given the limited success of past and current conservation efforts, an alternative approach is to preserve tissues and genomes of targeted organisms in cryobanks to make them accessible for future generations. Our pilot preservation project aimed to obtain, expertly identify, and permanently preserve a quarter of the known spider species diversity shared between Slovenia and Switzerland, estimated at 275 species. We here report on the faunistic part of this project, which resulted in 324 species (227 in Slovenia, 143 in Switzerland) for which identification was reasonably established. This material is now preserved in cryobanks, is being processed for DNA barcoding, and is available for genomic studies.

DNA barcode data accurately assign higher spider taxa

The use of unique DNA sequences as a method for taxonomic identification is no longer fundamentally controversial, even though debate continues on the best markers, methods, and technology to use. Although both existing databanks such as GenBank and BOLD, as well as reference taxonomies, are imperfect, in best case scenarios “barcodes” (whether single or multiple, organelle or nuclear, loci) clearly are an increasingly fast and inexpensive method of identification, especially as compared to manual identification of unknowns by increasingly rare expert taxonomists. Because most species on Earth are undescribed, a complete reference database at the species level is impractical in the near term. The question therefore arises whether unidentified species can, using DNA barcodes, be accurately assigned to more inclusive groups such as genera and families—taxonomic ranks of putatively monophyletic groups for which the global inventory is more complete and stable. We used a carefully chosen test library of CO1 sequences from 49 families, 313 genera, and 816 species of spiders to assess the accuracy of genus and family-level assignment. We used BLAST queries of each sequence against the entire library and got the top ten hits. The percent sequence identity was reported from these hits (PIdent, range 75–100%). Accurate assignment of higher taxa (PIdent above which errors totaled less than 5%) occurred for genera at PIdent values >95 and families at PIdent values ≥ 91, suggesting these as heuristic thresholds for accurate generic and familial identifications in spiders. Accuracy of identification increases with numbers of species/genus and genera/family in the library; above five genera per family and fifteen species per genus all higher taxon assignments were correct. We propose that using percent sequence identity between conventional barcode sequences may be a feasible and reasonably accurate method to identify animals to family/genus. However, the quality of the underlying database impacts accuracy of results; many outliers in our dataset could be attributed to taxonomic and/or sequencing errors in BOLD and GenBank. It seems that an accurate and complete reference library of families and genera of life could provide accurate higher level taxonomic identifications cheaply and accessibly, within years rather than decades.

Corrigendum: Targeting a portion of central European spider diversity for permanent preservation

[This corrects the article DOI: 10.3897/BDJ.1.e980.].