Sexual Paradox: Complementarity, Reproductive Conflict and Human Emergence

Golden Silk (Banana or Calico) Spider Nephila clavipes male and female.

In the popular mind, mating of spiders is as far from sexual paradox as one could imagine, a naked lunch for the femme fatale, in which the often much smaller, male becomes a delicacy even in the throes of fertilization. However this is true only for some well-known species, such as the Black Widow. Neither is it clear this is a one-sided love affair. The Australian redback male literally dances in front of the female's jaws to entice her into biting him, giving him longer to fertilize her more completely (Andrade R16).

The sexual stakes in spiders are made higher, both by the female's predatory nature and the fact that some species mate only once or at most a few times and the females can store sperm for up to two years, making a single sexual feat by the male the progential act of a lifetime. Despite the apparent imbalances, spider courtship poses intriguing and diverse examples of sexually-antagonistic coevolution, with all manner of subtleties and variations.

It is never easy to tell which sex the given act serves to greater degree. An Australian redback male is well-served if his death dance into the female's jaws gives him a lion's share of the male genes in her several batches of eggs. At an even greater extreme is the male orb-weaving spider Argiope aurantia. Male spiders transfer their sperm to palps in their legs which they insert into the female. In aurantia the male places both palps in the female and dies on the spot, making it difficult for another male to fertilize her (Foellmer R215).

Argiope keyserlingi

The much smaller size of many male spiders is another paradoxical issue. Male competition would select for larger, dominant males, but the female St. Andrews Cross Argiope keyserlingi tends to favour smaller males (Elgar et. al. R186), suggesting female selection drives this process. The females wrap their prospective mates in a silky cocoon as a way to give them more choice over which male's sperm to favour the most. Unlike the redback, these males struggle to escape and some do, often missing a leg. In the polyandrous orb-web spider Nephila edulis, males are much smaller and have a very skewed size distribution. Smaller males approach the female directly and mate more successfully and more often than larger ones, who have to cut a hole in the web (Schneider et. al. R618-R621).

Nephila plumipes

In Nephila plumipes, about 60% of males are cannibalized. However not all females are sexual cannibals, but only those in leaner condition. Males cautiously wait until the female catches a fly, thus avoiding pre-mating homicide. Despite expiring, males which are eaten have an advantage in mating for longer, if the female mates with more than one male and sperm competition is thus a real factor. Female cannibalism seems to be a function of predatory acuity generally and does not appear to be a specific sexually homicidal adaption.

Often it is not the desired male, but a rejected one who ends up becoming lunch. Tarantulas who are well-matched in size and live for up to 20 years, as well as Thomisidae and Clubionidae simply 'say hello' with a brief interplay of their front legs. Then if the female is into the idea of mating, and doesn't attack the male, copulation follows. Neither does familiarity bred contempt. Wolf spider males come in a variety of phenotypes with varying appearances. Females prefer, and are less likely to eat, males with whom they have already become familiar during an adolescence in which they remain unable to mate before their last molt . Other species of web building spider exploit this social situation by seeking a child bride, setting up home beside the web of an adolescent female so they can become familiar before she reaches maturity.

In various species of Dictyna, a male seeks out a female in her web and then moves in. He will walk around on her web vibrating his legs on the web and giving brief vibratory touches to her with his legs when they meet. He may build a special canopy in a corner of her web. Some time and a number of meetings occur before she allows him to mate. He may stay for weeks.

Dictyna civica male and female

Male dancing serves both as web music and a visual display. A male needs to announce his presence with a special dance quite different from the struggling of a trapped fly and the female will generally acknowledge this with responsive jiggling, warning irritation or a frightening silence depending on the circumstances. Salticidae males have colourful palps and front legs. Typically the male raises and lowers his front legs, vibrates his palps and runs to and fro in front of the female in order to excite her. The dancing is often energetic and prolonged, ten or twenty minutes is not unusual.

Phintella vittata (Daiqin Li)

A study in Current Biology shedding new light on spider mating found that male jumping spiders (Phintella vittata) are using ultraviolet B (UVB) rays to communicate with females, by reflecting the rays from their bodies. The researchers discovered that females were more likely to mate with males that could "talk" to them with UVB compared with spiders sitting in chambers where UVB light had been blocked with filters.

Some spider species offer a captured feast in a 'meat for sex' exchange. The male hunting spider Pisaura mirabilis can detect a female by smell or crossing a dragline she has left behind. He then hunts for a fly, which he wraps in a swathe of silk, postures in front of her and when her fangs are safely embedded in the fly he mates with her.

Tetragnatha male

Tetragnatha males rely on strength and good design. They have large mandibles and the male has two large spines on his. When he meets a mature female he moves straight towards her with his jaws open wide. The female opens hers wide as well. As they get close enough for their legs to touch and their jaws meet, the male locks his around the female's, the spines and his longer fangs allow him to trap her jaws completely. Now that it is impossible for her to bite him, they descend on a strand of web and mate hanging face to face. Afterwards he makes a quick release escape dropping rapidly to the ground.

Xysticus cristatus

Xysticus cristatus mixes bravado with caution. On meeting a female he (left) rushes up and grabs her (right) by the leg. When she stops complaining he climbs around on her back, fondling her with his legs, gently ties her down with strands of silk. When she is anchored, he climbs off her back and pushes underneath her from behind to copulate. Having finished mating he departs leaving her tied up. It takes her a little while to escape.

Latrodectus hasselti

A female redback (Latrodectus hasselti) has two spermathecae, for storing sperm., one on each side. A male can only insert one of his palps at a time and breaks it off inside her as a contraceptive plug, to avoid the next male using the same side having any more than a 20% chance of insemination. Having two spermathecae means the female generally has the choice of sperm from two males and the strongest sperm gets most of the offspring. But a strong male can recover from being partly digested dangling in front of the female's jaws and return to claim both spermathecae and thus 100% of the queen's potential (R652).

Dolomedes triton

One shouldn't underestimate the cannibalistic voracity of female spiders however. Female Dolomedes triton the fishing spider which also catches small fish, can become so aggressive that she would prefer to eat male spiders before they even mate with her. The most voracious of these females however are also the most daring with predators, so other forms of selection are contributing to a diversity of personality types (Johnson and Sih R342).

Harvestman

The harvestmen, of which the daddy long legs is a member, are a non-poisonous group closely related to spiders. The males of these species harvest the eggs of the females with which they copulate, so sexual paradox provides for an intriguing situation in which the male's egg garden becomes his sexual advertisement, and the more eggs a male can guard in his nest, the more attractive he will be to females. Here the ‘peacock's tail' has become the very eggs he cares for. A female, instead of copulating and leaving a single egg with him may try to eat the egg of another female competitor on the sly.

These varieties of mating teach us that the relations between the sexes are an endless struggle of Machiavellian manoeuvre and counter-strike in which neither sex ultimately has the upper hand, no matter how gruesome the appearances. In the centre of the cyclone lies the state of sexual paradox with each sex running while standing still to try to keep their end of the game alive. This variety amid genuine sexual paradoxes of coevolution is a lesson for human sexual dominion, where there has been an attempt to assert a unilateral dominance in an attempt to overthrow the natural order of sexually antagonistic coevolution.