Group selection and adaptation in social spiders: an entangled web (y’see what I did there? clever wordplay)

Why biologists say group selection is wrong, but it’s not, but it is… kinda.

Whenever I talk about vampire bat food sharing to a public audience, someone will inevitably say something like, “Wow! It’s amazing that vampire bats will feed each other to perpetuate their species” or “It’s so interesting how vampire bats will act for the good of the group” (this despite the fact that a main point of my talk is that they don’t act for the good of the group). The idea is pervasive, “Animal X does Y to perpetuate the species/group/population/ecosystem.” It originates, I presume, from years of Disney animal documentaries on how lions eat zebras to keep the circle of life going. Little do people realize that if you make this simple innocent statement in the presence of a talkative biologist, it will induce a frustrated sigh followed by a boring and condescending monologue that begins something like:

Aaactually… that’s not really how evolution works… [bla bla bla]”.

Behavioral ecologists refer to this popular idea, which they love to hate, as “group selection” and many consider it to be an out-of-date theory, or biological myth, akin to Lamarck’s famously wrong idea that giraffe necks are big because they keep stretching them to reach stuff. Richard Dawkins is well-known among biologists not for being an outspoken atheist, but because he wrote a book, The Selfish Gene, that could have just well been called The Group Selection Delusion.

But Aaaactually

In modern evolutionary biology, there is nothing controversial about the existence of group selection. It occurs when individuals live in social groups and those groups go extinct or proliferate at different rates.  You can easily create group selection in the lab and show that it produces certain traits, and stable social groups in the wild can clearly have differing rates of extinction.

Yet, for many evolutionary biologists, talking about group selection is almost like talking about gender politics, gun control, or the Israeli-Palestine conflict. You better tread carefully. Group selection has been a controversial topic in evolution since this 1964 exchange in the journal Nature and biologists are still reading and writing exchanges on it. Researchers who invoke the theory of group selection in their work are always on the defensive, wary of being discriminated against as someone who doesn’t really understand social evolution.* Why all the controversy?

The real controversial question is: Under what conditions does group selection lead to group-level adaptation? That is, when should we expect individuals to act or possess traits “for the good of the group”?

The textbook answer is basically, never– adaptive behavior maximizes gene propagation not success of social groups. But a more correct answer is that individuals can be said to act for the good of the group under two specific conditions. First, when the groups are genetically identical (in this case, the group selection can be equivalently viewed as kin selection). Second, when all competition exists between groups rather than within groups (ie “altruism” within the group can be equivalently understood as cooperation with group members in collective competition with all others in the population). This is what happens when you perform group selection in the lab: you are effectively suppressing genetic competition within groups and creating genetic competition between groups.

If either of these two conditions are met, individuals can eventually possess traits that appear to exist for the good of the group even at the expense of their own reproduction (such as worker bees that sacrifice their lives for the bee colony). In many cases, both conditions are met. For example, all your (non-cancerous) cells act for the good of the group (i.e. your body) because the cells share the same genome (more or less); but in addition, competition between your cells is suppressed, because the best bet for each cell to compete with all the other living cells in the world is not to selfishly replicate as a rogue individual (like a cancer cell), but rather to collectively and cooperatively coordinate their actions with other cells in your body to make babies. As an animal, there’s a limit on how many cells your body can make through growth; but there’s essentially no limit on how many new bodies (and hence cells) your own body can make through reproduction.**

OK, now on to the spiders!

In summary, evolutionary theory tells us that group selection does not really lead to group-level adaptation, except under the strict conditions when the groups are clonal or devoid of any within-group competition. Theorists have shown this many times in many ways.***

But a recent (soon to be controversial) Nature paper claims to have done the impossible: demonstrated that group selection has lead to a group-level adaptation even in groups that are neither clonal nor devoid of competition. The paper entitled Site-specific group selection drives locally adapted group compositions is fascinating. I posted the PDF here (because the journal Nature charges you money to read an article that the author gives away for free).

Anelosimus studiosus (from
Social spider webs can get really big (from

Before you get lost on the internet and destroy an hour reading about how interesting social spiders are, here’s the basic group selection story in a nutshell. In these amazingly cool group-living spiders (Anelosimus studiosus), the individuals can have two distinct personalities: aggressive or docile. Each group of spiders has a stable ratio of aggressive to docile spiders, and the optimal ratio is different in different environments (just like the optimal phenotypic trait like skin color differs across different environments). This optimal ratio persists when a spider group is moved to a different environment (just like how your skin color largely remains the same when you move to a new environment). Each group has some evolved optimal ratio of aggressive: docile spiders, and the actions of the individual spiders somehow move the group towards that optimal ratio and maintain it there. In conclusion, this optimal ratio is a group-level adaptation that is driven by group selection.

In the authors’ own words:

Our observation that groups matched their compositions to the one optimal at their site of origin (regardless of their current habitat) is particularly important given that many respected researchers have argued that group selection cannot lead to group adaptation except in clonal groups and that group selection theory is inefficient and bankrupt.

Our study shows group selection acting in a natural setting, on a trait known to be heritable, and that has led to a colony-level adaptation.

Does this mean that all these evolutionary theorists were wrong? No. I think (and please someone correct me if I’m wrong) that the contradiction comes from two different meanings of group-level adaptation. When I think of a “group-level adaptation” I think of a phenotypic trait of an individual bee that maximizes the success of the bee colony. And I think this is how most theorists were using the term as well. When you think in terms of inclusive fitness (fitness is a property of individuals not groups), you also tend to think of “adaptive traits” as properties of individuals rather than groups (one level up) or cells (one level down).

A different meaning of a group-level adaptation–the one used by these authors in the spider study– is the “trait” of a colony that cannot be reduced down to the traits of the individuals. For example, this could be the size of the bee colony, the ratio of types in a spider colony, or the diversity of personalities in a human tribe.

So really, we have two different types of group-level adaptation. It seems that group selection is not a good explanation for the first kind (heritable traits of individuals that maximize group survival), but it can explain (and perhaps it’s the only explanation) for the other kind of group adaptation (heritable “traits” of entire groups). It’s important not to confuse these two different things that are often labeled by the same term. In the latter case, does it really make sense to ignore the individuals and talk about group-level fitness or group-level adaptations? I don’t know, maybe.

I used to be really annoyed by group selection, because it always seemed to just glaze over what I thought were the interesting aspects of behavior (the strategies and interactions of individuals within the groups). Just showing that cooperative groups outperform non-cooperative groups, does not explain what makes cooperation stable within each group. That seemed like the real difficult question. In my mind, groups don’t perform “behaviors”, individuals do. So talking about collective actions of groups, without understanding what the individuals are doing just seemed confusing to me.

But now after reading this spider paper and others like it, I am beginning to see more and more that being able to “zoom out” and see groups as having “traits” might be useful in some cases. This is not necessarily just taking the group mean and ignoring the variance (as you do when you talk about things like “bat roost 1 kinship vs bat roost 2 kinship” or “boy height vs girl height” or “white wealth vs black wealth” where you reduce populations to a single average value). Just like a t-test, we can simplify matters by talking about mean differences between groups without losing sight of variation within-groups.

But I still think it’s crucial to figure out what the individuals are actually doing to create this emergent behavior. In this case, we still don’t know. What exactly are the individual spiders doing to reach their optimal ratio? Are they monitoring and policing certain types? Are certain types leaving the group to start new groups? Are they switching groups? I don’t feel like I can understand what’s going on until I can answer these questions. The trick of using group selection theory is to figure out when it’s really solving a puzzle or when it’s just obscuring it.

Should we always try to reduce the properties of groups to the individuals and their interactions? Or should we allow ourselves to think of groups as “individuals”?

I think both. The semantics are confusing, but there’s no contradiction whatsoever between these perspectives. Even if one can’t keep both perspectives in focus at once (I can’t), one should be able to think in both ways and switch between them. If you can’t explain the behavior of the whole using the interactions between the parts, then you don’t really understand the whole. But if you can’t switch perspectives and zoom out to see the whole as an individual node in an even larger network, then you can’t see the bigger picture. (If you like that idea, you’ll love this.)


* At conferences, I’ve had conversation with graduate students working on group selection, who are obviously try to suss out where I stand on the issue to figure out “Is this safe place to discuss group selection?” and on the other side of the coin I’ve also heard one researcher say something like, “Did he just invoke group selection? Jesus Christ.”

**I guess there’s actually an interesting exception: the immortal Hela cancer cells, which are from one woman’s cervix and are now in labs all over the world and collectively weigh more than 20 tons. If these human cells were all in one place, there could be a giant human cervix tumor that weighs the equivalent of 250 humans. So this woman’s cancer cells were much more evolutionarily successful than her other cells, whose DNA has been diluted by 1/2 down every generation.

***By “demonstrate” I mean using models and theory laden with partial differential equations and other mathematical arguments that more simple biologists– like myself– don’t 100% follow while reading the paper, but we will never admit that because we are too embarrassed of our mathematical incompetence and want to believe we are real scientists too.

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