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For Spiders, It's Cruel to Be Kind

It turns out nice guys do finish last, at least among arachnids. A 6-year study of a New World spider reveals that although colonies composed of docile individuals fare better in the short term, their passive behavior ultimately does them in. A species may need a mean personality to keep from going extinct, the results suggest.

Not all spiders earn their frightening reputations. Even within a single species, some individuals are much mellower than others. Take the social spider Anelosimus studiosus, a native of North and South American forests that builds collective webs that house 40 to 100 individuals. In 2005, ecologists discovered that not all A. studiosus had the same disposition. When two spiders shared a container overnight, docile animals remained beside each other the whole time, whereas aggressive ones attacked each other and then moved to opposite corners. Jonathan Pruitt, an ecologist at the University of Pittsburgh in Pennsylvania, wondered which personality was more successful in the wild.

To find out, Pruitt performed personality tests on dozens of A. studiosus spiders and then arranged them into 90 couples consisting of an aggressive pair, a docile pair, or an aggressive spider matched with a docile one. The arachnids' personalities are heritable, so a docile pair produces almost exclusively docile offspring, aggressive mates mainly make aggressive offspring, and mixed pairs produce a combination of docile and aggressive babies. After 1 week in the lab, each of the pairs had created small webs, or nests, on chicken wire within separate containers.

Pruitt returned to the Tennessee woods where he originally collected the spiders and wired each of the 90 nests onto trees and shrubs. For the next 5 years, he removed other species of spiders from the territory surrounding half of the webs. These 45 webs served as a control to test the hypothesis that disposition matters when hungry, solitary spiders abound in nature. The colonies in these well-maintained territories faired roughly the same as one another between 2007 and 2012, no matter the personality of their founders.

In contrast, colonies in the areas that were open to invaders differed from one another over time as solitary spiders began to infest the webs. Colonies founded by aggressive spiders successfully fought the intruders off, but produced fewer offspring because of the continuous conflict. In contrast, the predominantly docile colonies ignored intruders and continued to reproduce. In 2009, the docile colonies were flourishing, and their offspring had begun three times as many new colonies on nearby trees and shrubs compared with offspring from aggressive communities. Yet by 2010, the docile spiders' apparent advantage began to wane as invaders increasingly ate them and stole the insects snagged by the colonies' webs. By 2012, not a thread remained from the webs established by docile pairs, and only a quarter of those started by mixed pairs were left. Meanwhile, three-quarters of the original 15 nests founded by aggressive pairs stood strong, the team reports today in Ecology Letters.

In nature, A. studiosus colonies consist of a mix of docile and aggressive individuals. In short-term studies, Pruitt says, aggressive spiders appear to be troublemakers because they often brawl with members of their own group. However, this study showed their importance when it comes to defense. "Originally, I thought aggressive spiders exploited docile ones, but now I see that the aggressive ones catch most of the food and take care of the society," he says. Without aggressive spiders to care for them, docile spiders would go extinct whenever other spiders abound. Pruitt speculates that docile behavior still exists because it is useful to the colony in small doses. Perhaps docile individuals provide better care to hatchlings, he says.

For these spiders, passivity represents an "evolutionary dead end" because it comes with quick payoffs but dooms the lineage over time, Pruitt says. Much of the evidence for dead-end strategies comes from mathematical models that predict extinction after a tipping point, but this study documents such a strategy in action and defines the conditions that lead to a lineage's demise. "The tipping point occurs when invaders are abundant," Pruitt says. "Without them, colonies founded by docile individuals would flourish, but with them, they succumb to extinction." The results from this study suggest something about aggression in general, Pruitt adds. "Species without defense might be driven to extinction by enemies".

"This is a great, robust study that takes the study of animal temperament—which is kind of narrow—and puts it into a broad evolutionary framework," says James Traniello, a behavioral ecologist at Boston University. "The whole idea of evolutionary dead-end strategies is poorly understood," he says. A number of studies, such as those on Darwin's finches, document how species diversify in real time, Traniello says, "and here we have a study that shows what goes on at the opposite side, how lineages decline."