The Power of Personality Tests (for spiders)

Most pet owners would agree that animals can have distinct personalities, even the ones who keep Madagascar hissing cockroaches as pets. Fluffy the cat is timid; Mr Darcy the cockroach is hissy. But why does Mr. Darcy hiss more than others of his kind? Why do individual animals differ in the ways they respond to the world, even though natural selection is constantly pruning out the least effective patterns of behaviour?  Isn’t there just one perfect cockroach personality?

I want to talk about a fascinating reason that certain kinds of animals have different personality types, illustrated with an example that involves warfare (between spiders), cannibalism (by spiders), and communes (of spiders). When I talk about ‘personality,’ I mean consistent behavioural differences between individuals of the same species. For example, Jonathan Pruitt, a newly-hired faculty member in my department, consistently speaks faster than most individuals of our species. He has progressed from the trenches of grad school/postdocdom to assistant professorship at a enviably rapid pace, in part thanks to an unassuming but powerful tool: a personality test for spiders.

Here’s how that test works:
•    Take two spiders of the species Anelosimus studiosus.
•    Put them in a box.
•    Come back tomorrow and look at them.

Often, they look something like this:

or something like this:

In the first case, both spiders are hanging out together.  In the second, at least one of the spiders seriously needs its space.
Jonathan found that the distance between the pair of spiders in this test correlates with certain behaviours. These behaviours also correlate with each other, forming a ‘syndrome.’ So, the spiders that hang out together tend to show behaviours that we shorthand as Docile and the ones that can’t be near each other are Aggressive. Here are a few of the behaviours associated with each type:

(In case you’re wondering, pre-copulatory cannibalism means she kills and eats her suitor before he gets the chance to mate with her. Ouch.)

The syndrome is partly hereditary; aggressive parents tend to have aggressive offspring and vice versa. This genetic influence is important because it means that the proportion of the population that is aggressive can change over time by natural selection. So if, for example, aggressive spiders have more surviving offspring than docile spiders, then over the generations the genes that contribute to that aggressiveness should become more common.  Given enough time, selection might leave only aggressives, or only dociles.  But this is not the case – populations vary considerably in the proportions of each type. One of the reasons that these spider populations remain diverse is related to a peculiar fact about A. studiosus.  They often live together in co-operative webs.

Trees cocooned in spiders webs after flooding in Sindh, Pakistan

Giant spiderwebs after the floods in Pakistan last year

Source: Russell Watkins/UK Department for International Development

(OK, so this is probably not the co-operative web of a social spider, and is definitely not spun by A. studiosus. But how often do you have a legitimate reason to use a photo of a giant web?)

The vast majority of spider species are far from social – when confronted with another member of their own species, most spiders would be more inclined to turn to cannibalism than to a domestic arrangement.  But around 0.1% of species are social or sub-social, meaning that females co-operate to various degrees in their daily tasks of maintaining webs, catching food and rearing young. This kind of social strategy seems to pay off in environments with very large, very abundant prey.  So you can probably already see the relevance of the docile personality to the success of a social lifestyle. If you live in a colony, you might need to tolerate the presence of other members of your species.

But the question that now arises is: why isn’t every A. studiosus individual docile?  How can a colony function with all these mean, food-hogging, mate-eating types around? It’s not the case that only dociles work together and that aggressives live a solitary existence; on average, about 40% of individuals in a colony are aggressive. At first, Jonathan thought that the aggressives might be acting like parasites in the dociles’ cozy, hippie communes. Were they just freeloading, taking advantage of the communal web, and making a mess?

In short, no. It seems that the colony as a whole does better if both nasty and nice spiders are present. This means the reproductive fitness of an individual of either type is increased in a mixed-personality colony. To put it crudely: a colony made up of only dociles is not very good at catching prey and is more likely to starve through inaction; a colony of aggressives spends too much energy fighting and is more likely to starve through distraction.

Aggressive females also play an important role in defending the colony from marauding invaders – other spider species that are typically much larger than A. studiosus. Aggressives are more likely than dociles to pick a fight with these unwelcome visitors, putting themselves at greater personal risk. Jonathan sees this as a rudimentary division of labour, analogous to the defense castes in more extreme insect societies.

Examples of ant castes in a single species: Left-most 7 are workers of various castes, right 2 are queens

Source: Sarefo via wikimedia commons; modified by GameKeeper

Ant colonies, for instance, divide up their physical and reproductive work between distinct castes, such as soldiers and workers. In fact, most of the ants in a colony are sterile, with sexual reproduction left to the queens and drones. This kind of extreme division of labor is only possible for social groups, because the overall success of the colony is what makes up for the loss of reproductive fitness of some of its members. Even though A. studiosus is considerably less committed to the social lifestyle, there is evidence that its behavioural diversity is directly related to its tendency to live in groups.

So, in other words, one reason that there are A. studiosus individuals with different personalities is simply that their individual successes sometimes depend on the success of those around them, and it turns out that it takes all personality types for a group (of spiders) to function well.

Pruitt JN, Riechert SE (2011) Within-group behavioral variation promoted biased task performance and the emergence of a defensive caste in a social spiderBehavioral Ecology and Sociobiology 65:1055–1060.
Pruitt JN, Riechert SE (2011) How within-group behavioural variation and task efficiency enhance fitness in a social group. Proceedings of the Royal Society of London Series B 278:1209-1215.
Pruitt JN, Riechert SE (2009) Frequency dependent success of cheaters during foraging bouts might limit their spread within colonies of a socially polymorphic spiderEvolution 63: 2966-2973.
Pruitt JN, Riechert SE (2009) Male mating preference is associated with risk of pre-copulatory cannibalism in a socially polymorphic spiderBehavioral Ecology and Sociobiology 63:1573-1580.
Pruitt JN, Riechert SE, Jones TC (2008) Behavioral syndromes and their fitness consequences in a socially polymorphic spider, Anelosimus studiosusAnimal Behaviour 76: 871-879.

I’m submitting this for the NESCent evolution blog contest.  Wish me luck!


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