Microbes Can Change How Spiders Mate

(Inside Science) -- Spider sex is full of elaborate dances, danger, uncertainty and -- researchers now know -- microbes.

Funnel-web spiders (Agelenopsis pennsylvanica) hide in the hollows of their distinctive funnel-shaped webs, which are often built in urban hedgerows. They are mostly loners, so their interaction with other spiders is practically restricted to mating. It can be quite a show.

When a male spider wants to mate, he drums on a female’s web and sways his abdomen in a courting dance. If a female is receptive, the male then approaches her and inserts his sperm into her reproductive organs with specialized leglike appendages called pedipalps. But it’s a risky business -- sometimes, the female eats the male after mating. More aggressive females are more likely to eat a male, so he has to be strategic to get in and out fast.

But this mating process is even more complex than scientists thought. As it turns out, bacteria are also involved. “Microbes are so ubiquitous,” said behavioral disease ecologist Nick Keiser from the University of Florida in Gainesville. “They're on everything.”

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In a first-of-its-kind study, published in the journal Ethology, Keiser, then at the University of Pittsburgh, and his colleagues identified the bacteria lurking in the reproductive organs of funnel-web spiders. They collected spiders around the nearby neighborhood of Oakland and brought them to the lab. There, they swabbed the pedipalps of two male spiders and the abdomen of two female spiders and found six different strains of microbes.

But what really interested the researches was whether the bacteria had any effect on the spiders’ sexual behavior. “It was kind of an exploratory study,” said co-author Michelle Spicer, an ecologist at the University of Pittsburgh. They wanted to see “what happens when you modify the bacterial load on these spiders in the context of a super important behavior, which is courtship and mating,” she said.

The researchers coated the pedipalps of 20 males and the abdomen of 10 females with a cocktail of the bacterial strains. For comparison, they also coated the same organs of 15 male spiders and 11 female spiders with antibiotics, thus reducing the number of microbes in that area. Then, they paired the bacteria-coated or antibiotic-treated spiders with untouched spiders to see if they did something different in their mating ritual.

To their surprise, untouched males took about 10 minutes to start courting a female if she had been exposed to the bacterial cocktail. That’s 4.6 times longer, on average, than the rest of the pairings, which took around 2 minutes.

Why does the male take longer to start courtship when the female has been exposed to the bacterial cocktail? And most importantly, how does the male know a female has more bacteria? The scientists are not sure. Although they didn’t perform any molecular analysis, “we know that spiders in general do use a lot of chemical cues,” such as pheromones, said Spicer. Mechanical or vibrational cues could also signal a higher bacterial load. “It's got to be some weird, circuitous route that we don’t know about,” Keiser said.

There was an exception to the tendency for males to approach bacteria-smeared females more slowly. If a smeared female behaved aggressively, males began their courtship a bit earlier than the 10-minute average despite the presence of the bacteria. In spiders from other species, it's been shown that females with aggressive personalities are more likely to eat males. While the reasons for the male funnel-web spiders' haste are not yet clear, the researchers suspect that the threat of being eaten may override the threat of infection, prompting males to act fast.

The researchers did not stop their observations there. Because some bacteria can be harmful, they also tracked the lifespan of the spiders after they mated. After 40 days, most females remained alive, except for the untouched females that had mated with bacteria-loaded males -- about half of them died. Because this didn’t happen to the females that were smeared with bacteria, the researchers think that the males infected the untouched females with bacteria while introducing their seminal fluid -- a sort of sexually transmitted infection, which has been reported before in spiders. 

“That was one of the things that was most surprising to me,” said Spicer.

Some studies have previously looked into how bacteria can alter spiders’ behavior, but details remain scant. For Eileen Hebets, an ecologist at the University of Nebraska-Lincoln who was not involved in the new research, it’s too early to figure out what the results from this study really mean. But, she added, "it's intriguing that they did find very, very clear results.”

“It's a very convoluted thing,” said Keiser. “But I think that's interesting and generates countless new questions that can be asked.” 

Hebets agreed. Because the researchers only analyzed the bacteria from two males and two females, she would like to know how variable and relevant the microbiome really is within this species and across the sexes. “At this point," she said, "the world of microbes and spider behavior, I think, is wide open.”