This Is Why Spider Monogamy Is TerrifyingS

In certain species of spiders and insects, females kill and eat their mates after sex. But the dark fishing spider experiences a very odd twist on this gruesome tale.

Rather than being killed by his mate, a male of this species (Dolomedes tenebrosus) spontaneously dies after sex — while still hanging from the bulbous body of his much larger bride. His death seems linked to the genital disfigurement he experiences from sex, and his dangling body becomes a healthy snack for his mate.

Lead researcher Steven Schwartz, a behavioral ecologist at the University of Nebraska–Lincoln, stumbled upon the spiders' strange behavior by chance. Initially, he says, he was interested in monogyny (male monogamy) and sexual cannibalism. When he checked out the mating behavior of D. tenebrosus, he saw males die after sex, but it didn't appear that the females had anything to do with the deaths. "I initially thought the female would kill the male like in other species," Schwartz tells io9.

Whatever the case, if a male dies after only mating with a single female, it's an example of monogyny, which is relatively rare, having been found in a few other spiders, insects and fish (such as the anglerfish). In the animal kingdom, males will typically mate with as many females as possible; females will also mate with multiple partners, but they are pickier with their mates. In other cases, males will mate less frequently than expected because they instead invest more energy into child rearing.

These different strategies carry their own reproductive benefits to the male, whether that is more offspring or healthier offspring. However, evolutionary biologists have struggled to find similar benefits to monogyny, where males will not only mate with a single female, but also forgo any child rearing, Schwartz says.

According to theory, male monogamy is most likely to develop in species with a male-biased effective sex ratio — the ratio between adult males and females that mate at least once. In these cases, where there are a lot more sexually mature males than females, males should want to focus their energy on a single, virgin female and fertilize all of her eggs, instead of trying to fertilize the eggs of multiple other females. The model also predicts that this male-biased sex ratio is more likely to occur in species with a female-biased sexual dimorphism (females are larger than males) because smaller animals have a better chance at surviving to breeding age.

Given that female D. tenebrosus are cannibalistic and weigh about 14 times as much as males, the species seemed perfect to learn more about monogyny. So Schwartz and his colleagues conducted a series of experiments.

To start, they went into the field (Lancaster County near Lincoln, Nebraska) and looked at the sex ratio and maturation times of dark fishing spiders, which only live for a couple of years. They found that males outnumbered females by almost 3:1 at the beginning of the breeding season — the species has a male-biased sex ratio. They then collected a couple dozen specimens and studied their mating behavior in the lab.

This Is Why Spider Monogamy Is TerrifyingS

As is common among spiders, male dark fishing spiders begin by ejaculating onto a "sperm-web." They then suck up the sperm with their two pedipalps (sperm-transfer appendages). To mate, the male will insert one of his pedipalps into a female's genital opening, and the hematodochal bulb inside the appendage will expand to push sperm into the female. The researchers saw that the males' legs curled up underneath their bodies and they hung motionlessly from the female's genital opening after the bulb expanded.

Tests showed that the males' heartbeats stopped within a few hours — even if the females didn't cannibalize their mates while they hung inert, the males would die anyway.

Schwartz says that the bulb inflation likely has something to do with the males' spontaneous deaths. "We have a number of different, weird observations," he says. In other spider species, the males' pedipalps contract after transferring sperm. But the bulbs of each and every one of the male D. tenebrosus remained swelled, representing a form of genital mutilation. What's more, "every single male that has mated died in the same way," Schwartz adds.

In fact, even males that did not actually have sex died after their pedipalps expanded. Schwartz recalls several males whose bulbs swelled and died just from him handling them. In another case, a male expanded onto a female's leg and subsequently died. Given that males always die after sex, this means that they only mate with a single female — they're monogamous.

This Is Why Spider Monogamy Is TerrifyingS

Interestingly, tests showed that both of the males' pedipalps were "charged" with sperm, suggesting that they die before realizing their full reproductive potential. "In this species, they are only using half their sperm," Schwartz says. Other experiments showed that males prefer the silk of virgin females, as predicted by the theoretical model of monogyny.

In a previous study that was part of his dissertation, Schwartz also found that females consistently ate their mates after they died, and experiments suggested that being cannibalized actually benefited the males reproductively. Females that were allowed to eat their partners produced offspring that were larger, more numerous and better able to survive than the offspring of non-cannibalistic mothers. Schwartz is now following up by running more experiments with larger sample sizes.

So it seems that even though male dark fishing spiders abruptly die after sex, experience genital mutilation and get eaten, they may, at the very least, still be reproductive winners.

You can check out the study in the journal Biology Letters.

Images and video courtesy of Steven Schwartz.