The Hive Mind

Feature / by Benjamin Phelan /

Is understanding the selfless behavior of ants, bees, and wasps the key to a new evolutionary synthesis?

Craig Packer, a biologist at the Univeristy of Minnesota who has done work in Africa describing altruistic behaviors in groups of lions, says that sometimes people are “too avidly keen” on group selection. “It can become very superficial.”

Bert Hölldobler cites dominance hierarchies in groups of wolves as one of the classic phenomena that group selection got wrong. A wolf that is challenged by a higher-ranking member of the pack will expose its belly, prompting the aggressor to stop attacking. Group selectionists explained the behavior using the good-for-thespecies chestnut. “If one member of a species kills another,” as Hölldobler puts it, “it doesn’t help maintain the species. This was the argument, and it was wrong.” The simpler and correct interpretation is that both wolves are protecting their own interests, each avoiding actual fighting because neither can afford the risk. The good of the group is irrelevant.

But in observing ants, Darwin was confronted by a version of altruism so extreme that it didn’t readily fit explanations based on natural selection. In fact, as he wrote in On the Origin of Species, ant behavior constituted the “one special difficulty, which at first appeared to me insuperable, and actually fatal to the whole theory.” Darwin, who had a dramatic streak, was inclined to write things like that, but in this case he was not exaggerating.

In most circumstances, the persistence of altruism is not difficult to understand, because even the most altruistic individual — say, someone tending to the infected sores of beggars in a slum — suffers only a partial reduction in the likelihood of reproducing and passing on the trait to offspring. Surviving long enough to reproduce may be unlikely for someone exposed to so much contagion. But it is still possible, and so it happens from time to time, and that’s all that is required to keep the trait of altruism alive. But ants — along with termites, some bees and wasps, Crespi’s thrips, and a handful of other organisms — are eusocial, meaning that reproduction is severely restricted, usually to a single queen and whatever male inseminates her; that multiple generations live together; and that young are reared not by the queen, but by the colony’s other members, which do not reproduce. There, for Darwin, was the rub. For how will a sterile worker ant that will never bear offspring pass on her genes? And yet there have evolved specific castes of sterile ants that perform the same tasks from generation to generation, despite the fact that there is no line of descent to propagate their altruistic behaviors.

Darwin’s insight was that groups tend to be related, and relatives tend to share traits. From animal breeding, he knew that if a cow produced well-marbled beef, chances were good that its siblings did too. This is in fact how lineages of beef cattle are established, as you never know if a cow’s flesh is tasty until it is deceased, at which point it cannot be bred. So you breed its siblings. By analogy, as Darwin correctly reasoned, the trait of sterility must somehow be carried, but not expressed, in reproductive ants. (The exact mechanism of heritability would have to wait for Mendel and the discovery of DNA.) In helping her sisters to reproduce, a sterile ant is indirectly helping herself, insofar as her behavior ensures that her own traits, including sterility, will be passed on to some of her nieces.

Darwin’s reasoning formed the basis for W.D. Hamilton’s theory of kin selection: When calculating an individual’s fitness, one must include the behavior of the relatives among whom it lives, since their behavior has an effect on its fitness. Evolutionary fitness thus became a larger concept, one that extends beyond the individual. For this reason, the animating principle of kin selection came to be called inclusive fitness. Inclusive fitness replaced the woolly thinking of naive group selectionism with stricter reasoning and a measure of mathematical rigor.

Of course, as Crespi points out, woolly thinking can be a hazard to inclusive fitness, too, as its proponents sometimes unwittingly ascribe consciousness to a gene: One hears about a gene “helping” copies of itself in the bodies of relatives. It’s a formulation that makes for a useful approximation, but it’s sloppy and creates bad intuition. Rather, he says, inclusive fitness is characterized by “an allele having effects that lead to increased replication of itself relative to alternative alleles.” Genes contributing to altruistic behaviors have no intrinsic goal, in other words, and a gene cannot act “selfishly” to help copies of itself in other organisms. They spread in a population because the individuals who benefit from altruism also possess the trait (whether they express it or not), and are therefore more likely to bear altruistic offspring who both benefit from the trait’s presence in their kin and help those kin themselves.

“But,” Crespi says, “it’s always best to take the mathematical perspective as well: rb-c>0.”

This tidy inequality, known as Hamilton’s rule, posits that a trait tends to increase in a population if the benefit (b) to a relative (r), minus the cost to the individual (c), is greater than zero. With the discovery of Hamilton’s rule, E.O. Wilson declared that the fundamental problem of sociobiology had been solved.

“I lavished attention and praise on it in my two main books in the ’70s, but now it seems like a mostly useless abstraction,” Wilson says. “It’s manifestly true that if benefit exceeds cost it will result in a trajectory of gene frequency upward. It’s also manifestly true that it will be discounted by the degree of relatedness. It explains nothing because it explains everything.”

Despite such critiques, the Hamilton inequality remains the foundation of kin selection and inclusive fitness, which is more or less how theoreticians and experimentalists practice the study of evolution. But overreliance on the inequality led Hamilton himself to make a mistake about the origin of eusociality in insects, which the Wilsons argue shows that inclusive fitness’s explanatory power is not as great as its supporters would like to think.

Ants, bees, and wasps belong to the insect order Hymenoptera, and they all have an unusual reproductive system, called haplodiploidy, that gives rise to a pattern of relatedness that alters the rb-c algebra in a suggestive and significant way. Females are born from a fertilized egg and so possess one set of chromosomes from a mother and one from a father: They are diploid. This is the familiar system that governs reproduction in most animals, including humans. But males in haplodiploid species are born from an unfertilized egg and have half as much genetic material as their sisters. They are haploid, receiving their one set of chromosomes, unmixed and unrecombined, directly from their mother, with no contribution from a father. So a male ant has no father and cannot have sons. (But, oddly, he has a grandfather —  though only one — and can have grandsons.)

The consequences for females are different, but equally odd. Because females in haplodiploid species receive half their chromosomes, unrecombined, directly from their father, and a random, recombined half from their mother, they are more related to each other (by 3/4) than to their parents or any offspring (by 1/2), or to their brothers (1/4).

That pattern of relatedness led Hamilton to propose that haplodiploidy alone would tend to give rise to eusociality and its sterile castes, since a female increases her inclusive fitness more by caring for her sisters than by reproducing. But the discovery of fully diploid species (having genetic systems like ours) that are also eusocial, as well as the fact that most Hymenoptera, despite being haplodiploid, are not eusocial, put the claim to rest. A weird genetic system alone is neither necessary nor sufficient to cause eusociality, although it still could make eusociality more likely. But for E.O. Wilson, “close relatedness is not that important” to eusociality at all.

Crespi disagrees. “Wilson has a point in saying that colony-level selection is not given as much attention as it deserves,” he says. “But to take it as far as he has, saying inclusive fitness and kin selection aren’t necessary, is just wrongheaded.” Kin selection, says Crespi, is central to evolutionary biology, especially to the study of social evolution. “One simply can’t say that it’s unimportant based on the large body of evidence. And it’s no coincidence that he works on ants.”

That’s because, out of all insects, ants have evolved the most elaborate forms of eusociality. They became eusocial some 100 million years ago, and natural selection has been tinkering with and elaborating their society ever since. Crespi and others argue that ants make poor study organisms for the origin of eusociality because it’s impossible to look at them now and infer what their ancestral state may have been. So while it’s true that ants in a given colony are not closely related — which the Wilsons also point out as evidence against kin selection — that doesn’t mean that the first eusocial ants were not closely related. And recent work by William O.H. Hughes at the University of Leeds seems to bear this out: Ancestral populations of eusocial insects apparently mated monogamously, which, as a consequence of the genetic inheritance patterns of haplodiploidy, would have made each female member 3/4 identical to all her sisters. Hughes’s discovery fits neatly with the prediction that high degrees of relatedness encourage the evolution of eusociality, but it is nonetheless insufficient to confirm that the close relatedness is enough to have caused eusociality. Despite all the great efforts of the mathematical biologists to explain evolution, something has been missing from the picture.

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