This week at the collaborative science blog Nothing in Biology Makes Sense!, contributor Devin Drown discusses a new study of bacterium-on-bacterium violence:
The bacteria produce chemical weapons, bateriocins, which can broadly harm other isolates, but relatives are left unharmed. These chemical weapons can be classified as spiteful: in the process of harming others they also harm the focal individual. This self-harm comes from the cost of making the chemical weapon. Others have labeled this antagonistic trait a greenbeard gene.
To learn what a bacterial chemical weapon has to do with what might otherwise sound like an overenthusiastic celebration of Saint Patrick’s Day—and how both might explain the diversity of living populations, read the whole thing. ◼
The cover article for last week’s issue of Nature promised to be the last word in a long-running scientific argument over the evolution of cooperation—but it really just rejiggers the terms of the debate. Instead of solving the problem of how cooperative behavior can evolve, the new paper presents a model of maternal enslavement [$a]. These are not, it turns out, quite the same thing.
Group selection versus kin selection
Let’s start with some background. Unselfish, cooperative behavior has long been a puzzle in evolutionary biology, because natural selection should never favor individuals who make significant sacrifices for the benefit of others. Sure, an unselfish individual might expect those she helps to reciprocate later; but a population of the unselfish would be easily overrun by those who don’t reciprocate.
There have historically been two answers to the problem of the selfish out-competing the unselfish. The first case is basically an extension of logic we all learned in kindergarten: cooperative groups can do things that uncooperative groups can’t. Like, for instance, start a neighborhood garden.
Under this model, neighborhoods of cooperative, garden-making people are nicer places to live, and their inhabitants can collectively out-compete other neighborhoods that can’t get it together to start a community garden. In evolutionary terms, this is group selection—even if individuals sacrifice to build the garden, the group as a whole benefits. Unfortunately, this breaks down if the new garden attracts selfish people to move to the neighborhood, buy up all the cheap real estate, and open Urban Outfitters franchises.
There’s another possibility, though. What if unselfish behavior isn’t always truly unselfish? For instance, if you help your relatives, you’re actually helping some of your own genes. You share half your genes with your siblings, a quarter of your genes with half-siblings, an eighth of your genes with first cousins, and so on. This means that Michael Bluth might be on to something.
Evolutionarily speaking, it doesn’t matter if Michael spends all his time helping his feckless family, as long those efforts help someone in the family (G.O.B., most likely) reproduce and perpetuate some of the genes that Michael shares with him or her. This idea was advanced by W.D. Hamilton in two 1964 papers, one mathematical [PDF], and one more focused on real-world examples [PDF]; we now know it as kin selection. It doesn’t hold up so well for maintaining the kind of complex society humans have today, where we interact with lots of completely unrelated people—but it might have got the ball rolling toward the wheel, war, New York and so forth by selecting for cooperative behaviors within small tribes back at the dawn of history.
The group selection versus kin selection debate has gone back and forth for decades, and the new paper is a shot across the bow of kin selection. The authors, Martin Nowak, Corina Tarnita, and E.O. Wilson, aim to do two things: first, prove that kin selection is wrong; and second, describe an alternative explanation. For the first, they argue that kin selection only applies in narrow circumstances, that those circumstances never show up in nature, and that empirical studies just don’t support the model. Johnny Humphreys makes some reasonable objections to these arguments, and so do several folks interviewed by Carl Zimmer, and I’ll refer you there rather than try to improve on them.* I’m more interested in the second part: the alternative explanation.
Enslaved by Mom
No individual fitness for you—you’re cogs in the Superorganism. Photo by jby.
Nowak et al. propose to explain the evolution of unselfishness as it applies to eusociality—organisms like ants or bees or naked mole rats, in which colonies of (closely related) individuals defer most or all of their opportunities to reproduce, in order to support one or a few individuals that reproduce a lot. As Johnny points out in his critique, it’s not clear that eusociality is the same thing as unselfishness at all, even though it’s historically cited as an example of unselfishness [$a]. The new model that Nowak et al. develop actually makes the difference between eusociality and unselfishness even clearer. Under their model, it’s not that worker ants give up reproductive opportunities to help their mother, the Queen, reproduce—it’s that the Queen takes away their reproductive opportunities.
The key insight of the new model is that, in evolving from a non-social insect to a eusocial one, the natural selection that matters affects not the individuals evolving into workers, but the individual who would be Queen. Consider an insect similar to the probable ancestor of ants: females build nests, provision them with food, and lay eggs inside. Nowak et al. propose that a female who evolved the ability to lay “worker” eggs—females that grow up not to found their own nest, but to help in their mother’s—would have greater fitness than females without such helpful offspring.
Aside from the probability of evolving “worker” eggs (which is not a small issue, I think), this shift in perspective from the fitness of the worker to the fitness of the Queen makes all sorts of sense to me. I’ve often wondered why myrmecologists don’t treat ant colonies as single organisms, rather than collections of cooperating individuals.
But this approach also seems to sidestep the key question biologists hope to answer with kin selection and group selection models—these models aim to explain how individuals can come together to cooperate, but Nowak et al. have built a model that looks more like enslavement. I can’t learn anything about how unselfish behavior can spontaneously evolve in a population by looking at a population that has had unselfishness imposed upon it. To indulge in one last especially geeky pop culture reference, it’d be like trying to learn about market economics by studying The Borg.
Nowak, Tarnita, and Wilson might have come up with a very good model for the evolution of eusociality; but if so, it means that eusociality is a bad model for the evolution of cooperation as we usually conceive it.
———— * I will, however, note that Nowak et al. do something I’ve never seen in a scholarly paper before—in dismissing empirical studies of kin selection, they defer substantive discussion to the Supplementary Information. There are, in fact, 43 pages of SI for this 6-page paper, including two major mathematical models and the discussion of empirical kin selection studies. This is a problem, but one that is beyond the scope of this already-long post.
Axelrod, R., & Hamilton, W. (1981). The evolution of cooperation. Science, 211 (4489), 1390-1396 DOI: 10.1126/science.7466396
Hamilton, W.D. (1964). The genetical evolution of social behaviour. I. Journal of Theoretical Biology, 7 (1), 1-16 DOI: 10.1016/0022-5193(64)90038-4
Hamilton, W.D. (1964). The genetical evolution of social behaviour. II. Journal of Theoretical Biology, 7 (1), 17-52 DOI: 10.1016/0022-5193(64)90039-6
Nowak, M., Tarnita, C., & Wilson, E. (2010). The evolution of eusociality. Nature, 466 (7310), 1057-62 DOI: 10.1038/nature09205
For cooperation to work, everyone involved needs to know what the others are willing to contribute in order to decide what she will contribute. You might think that only humans can achieve that kind of back-and-forth negotiation, but a paper recently published online by Proceedings of the Royal Society suggests otherwise. In it, ornithologists decode the negotiations [$a] that allow sociable birds to share the task of watching for predators.
The southern pied babbler, Turdoides bicolor. Photo by Blake Matheson.
Pied babblers (Turdoides bicolor) are sociable South African songbirds, which live and forage for food in groups. During foraging, some adult babblers act as sentinels, perching above the ground to scan for predators, and alerting the rest of the foragers if any danger shows up. Sentinel behavior is cooperative—sentinels free the rest of the group to concentrate on feeding, but sentinels themselves cannot forage. The study’s authors, Bell et al. hypothesized that sentinels might communicate how long they’re willing to stand watch to the rest of the group, so as to prompt new birds to take up watch and given the current sentinels a break to feed. The authors first established that how hungry a babbler is determines how long he or she is willing to stand watch, which they did by feeding the birds with meal worms immediately after they concluded a period of sentinel duty. Babblers receiving ten worms returned to duty faster than those receiving just one, and stayed on duty longer. Further feeding experiments and observations established that both foragers and sentinels called to each other less frequently when they were well fed, that sentinels called more frequently the longer they stayed on watch, and that sentinels who ultimately stayed on watch the longest also called the least frequently in their first minute on watch.
So call frequency is the babblers’ signal for how badly they want to forage—foragers hearing higher-frequency calls from sentinels should take them as a call for relief; and sentinels hearing lower-frequency calls from foragers should take them as permission to leave the watch and start foraging. To test this hypothesis, the authors played recorded calls to foragers and sentinels, and found that the birds responded as I’ve just described. The apparent babble of the babblers, then, is actually a perpetual negotiation about who should be on sentinel duty—sentinels complaining when they get hungry, and foragers telling the sentinels, “Not yet! I just need to catch a few more worms.”
Bell, M., Radford, A., Smith, R., Thompson, A., & Ridley, A. (2010). Bargaining babblers: vocal negotiation of cooperative behaviour in a social bird. Proc. Royal Soc. B DOI: 10.1098/rspb.2010.0643
In social insects, colonies of hundreds or thousands of workers and soldiers forgo reproduction to support one or a few “reproductives” — drones and a queen. In most cases, this isn’t as selfless as it might seem. Because the workers in a colony are all offspring of the queen, they’re really reproducing through her — because the queen shares genes with the workers, when she reproduces it contributes to their evolutionary fitness.
The termite Zootermopsis nevadensis lives in small, socially-stratified colonies that tunnel through rotting logs. Each colony has a pair of reproductive individuals, a king and queen, served by sterile workers and soldiers. Multiple unrelated colonies usually nest in a single log, and when they encroach on each other’s territory, something interesting happens — they merge.
In what the authors refer to obliquely as the “interaction” that precedes a merger, the king and queen of one or both colonies may die. Mergers occur in the aftermath, as workers from the two colonies began to work in concert, and one or a few of them become replacement reproductives. This ability of sterile workers to start reproducing in the absence of a king and queen is unique to termites. DNA analysis shows what happened after mergers — new reproductives could arise come from either or both colonies, and that in some cases they interbred.
It’s this possibility to become genetically invested in the newly merged colony, the authors say, that motivates workers from two unrelated colonies to work together. If this is the case, it means that kin selection is not what keeps merged colonies together. Group selection might be a better explanation. Kin selection is often contrasted with group selection, in which unrelated individuals sacrifice their own interests to those of a larger group, so that their colony can better compete against rival colonies. In a classic 1964 Nature paper [$-a], John Maynard Smith discussed the conditions under which kin selection operates well:
By kin selection I mean the evolution of characteristics which favour the survival of close relatives of the affected individual, by processes which do not require any discontinuities in population breeding structure.
And contrasts them to conditions necessary for group selection to work:
[Under group selection] … If all members of a group acquire some characteristic which, although individually diadvantageous, increases the fitness of the group, then that group is more likely to split into two, and in this way bring about an increase in the proportion of individuals in the whole population with the characteristic in question. The unit on which selection is operating is the group and not the individual.
The ecology of Zootermopsis nevadensis may set the stage for group selection to overpower kin selection. With many small colonies competing for a single rotting log, the benefits of possibly contributing to the reproduction of a larger, more competitive colony make mergers worthwhile. Something similar has been documented in ants, which can form supercolonies of unrelated colonies if there is some external threat (another ant species) to force them to band together — you can find discussion of a recent paper on this case over at Primate Diaries.
SMITH, J. (1964). Group selection and kin selection Nature, 201 (4924), 1145-1147 DOI: 10.1038/2011145a0
Johns, P., Howard, K., Breisch, N., Rivera, A., & Thorne, B. (2009). Nonrelatives inherit colony resources in a primitive termite Proc. Nat. Acad. Sci. USA, 106 (41), 17452-6 DOI: 10.1073/pnas.0907961106
The search for a mate is traditionally a selfish enterprise. After all, the ultimate goal is reproduction, and — barring any effect of kin selection — natural selection only cares about how many babies you make, not how many you help to make. This is fundamentally a biological question, though, and if there’s a universal rule in biology, it’s that nature is good at making exceptions.
(I seem to recall that there’s also some excellent footage of manakin dancing in David Attenborough’s The Life of Birds.)
To dance for females, male manakins gather at locations called “leks,” where most try to establish a small territory to perform. Among wire-tailed manakins, though, some males will team up to dance — presumably because if one brightly-colored male jumping around on a branch is attention-grabbing, two or three are even more so. But in these “coordinated displays,” one performer, the socially dominant one, is most likely to mate with the females who like the performance. So what’s in it for the other guys?
There seem to be two possible (though not mutually exclusive) explanations [$-a]: (1) that the mate-attracting dancing does double duty to establish social dominance relationships among males, and (2) that, even if it wins fewer mates than the “lead” role, being a supporting player in a successful cooperative display means better mating prospects than trying to go it alone. To try and disentangle these two possibilities, the new study’s authors followed the behavior of wire-tailed manakins at several leks for four years, building a “social network” of male-male cooperation at the leks and counting the offspring each male bird by taking DNA fingerprints of the males and of newly-hatched chicks in the nests of females who attended each lek.
Although the most reproductively successful males at each lek were all territorial, defending their own spot at the lek and dominating other males who joined in the display on that territory, non-territorial “floater” males tended to make more babies if they joined in more displays. In fact, the number of offspring produced was best predicted by the number of cooperative display interactions in which a male joined, whether he had his own territory or not. This complements an earlier study by the same group [$-a], which showed that a male’s “tenure” — how long he had been dominant in a territory within a lek — was the best predictor of mating success, but that a male’s rise through the social hierarchy at a lek was facilitated by cooperative interactions with other males.
In short, male manakins seem to help each other in mating displays for essentially selfish reasons. Being a supporting dancer has a coattail effect, earning more mates than trying to go solo, and it helps young males improve their social status toward the day when they can establish their own display territory.
Prum, R.O. (1994). Phylogenetic analysis of the evolution of alternative social behavior in the manakins (Aves: Pipridae). Evolution, 48, 1657-75 DOI: http://www.jstor.org/stable/2410255
Ryder, T., McDonald, D., Blake, J., Parker, P., & Loiselle, B. (2008). Social networks in the lek-mating wire-tailed manakin (Pipra filicauda) Proc.R. Soc. B, 275 (1641), 1367-74 DOI: 10.1098/rspb.2008.0205
Ryder, T., Parker, P., Blake, J., & Loiselle, B. (2009). It takes two to tango: reproductive skew and social correlates of male mating success in a lek-breeding bird Proc. R. Soc. B, 276 (1666), 2377-84 DOI: 10.1098/rspb.2009.0208
This week’s PNAS has another (open access!) paper taking a crack at the problem of how cooperation can evolve. The authors create a world where cooperation arises spontaneously in a population of selfish individuals by modeling a fundamental human drive: the desire for a good neighborhood.
Helbing and Yu set up a model world ruled by the Prisoner’s Dilemma, a common game theory scenario in which pairs of interacting individuals can choose to cooperate or not cooperate with each other. If both refuse to cooperate, neither gets anything; if one cooperates and the other doesn’t, the cheater gets a reward, but the cooperator pays a cost; if both cooperate, then they both get a smaller reward. If neither interactor can predict the other’s choice, the most sensible strategy is to just never cooperate – you make out pretty well when the other guy is silly enough to cooperate with you, and you’re no worse off than you started out if you both refuse to cooperate.
Previous models have made cooperation work in Prisoner’s Dilemma situations a few different ways. One way is to allow individuals to remember how they have treated each other over multiple iterations of the PD interaction, so that cheaters can be punished [$-a]; another is to let the game play out across space in such a way that cooperators can cluster together, so that they are more likely to interact with other cooperators [$-a].
Helbing and Yu’s model is a variation on the “spatial” flavor – individuals occupy cells in a grid, and interact with those in adjacent cells. Strictly speaking, it isn’t an evolutionary model (even though the authors describe it as such), because there doesn’t seem to be any inheritance of behavior from one generation to another; instead, individuals “learn” from their neighbors, imitating the ones who are most successful in terms of interaction rewards. There’s a random element to individual behavior, to approximate trial and error strategies. Perhaps most importantly, individuals can migrate across the grid, moving to adjacent unoccupied cells where they expect to find a greater reward.
Neither imitation nor migration alone allow cooperation to survive in this model world, but some interaction between the two does. This result holds, apparently, for a wide range of possible combinations of payoff conditions. For some conditions, the model will even allow cooperators to “invade” a world full of non-cooperators. The speed with which individuals can move across the grid – cooperators seeking other cooperators, and avoiding cheaters – is critical, say the authors. They call this “success-driven migration” – and it does seem to allow cooperation – though not altruism – to arise out of selfishness.
In evolutionary ecology, cooperation is a perpetual puzzle. It makes sense for organisms to help each other if they can reliably expect to be repaid in kind some time in the future, but cooperative societies are vulnerable to invasion by folks who selfishly accept help without returning the favor. The classical theoretical result is that, once selfishness evolves in a cooperative society, selfish individuals are able to out-compete cooperative ones, until cooperation (and, potentially, the society) dies away altogether.
One possible way to prevent this outcome is for cooperative individuals to punish selfishness, for instance by refusing to help those who don’t reciprocate. In this week’s PNAS, a new paper suggests that another way to stabilize cooperation is to have selfish individuals punish selfishness themselves [subscription needed].
As the authors put it,
This behavior might seem hypocritical in moral terms, but it makes sense as an evolutionary strategy. It can even be looked upon as a division of labor, or mutualism, whereby cheating during first-order interactions becomes a “payment” for altruism (punishment) in second-order interactions.
In other words, these “selfish punishers” may not return cooperation in kind, but they pay for it by punishing other selfish individuals. Ayn Rand would probably love this stuff, but it puts me in mind not of unfettered individualism but a feudal society – a mass of cooperators working for the benefit of the “greater good,” with a handful of punishers taking the benefits of that work and keeping everyone else in line.