For the Good of the Gene

Infanticidal lions, adulterous swallows, and sex‑ratio‑skewing warblers may give the impression that animal life is little more than sexual selfishness. And yet in many cases, evolution has produced animals that have given up their own struggle for sex altogether.

William Hamilton was intrigued by this paradox, particularly in the case of bees and other social insects. In a honeybee hive, there is a single queen, a few males, and 20,000 to 40,000 female workers. The workers cannot reproduce on their own; they spend their lives gathering nectar, keeping the hive in good working order, and feeding the queen’s larvae. They will defend their hive against attackers, dying in the process. In terms of evolution, it seems like a mass suicide.

But Hamilton suggested that thanks to the peculiar genetics of honeybees and related insect species, the workers are actually working for the long‑term benefit of their genes. A queen makes sons and daughters in distinctly different ways. Males start out as unfertilized eggs, which divide and develop into full‑grown insects without any sperm. Because they don’t receive any DNA from a father, male honeybees have only one copy of each gene. On the other hand, a queen mates with one of her male consorts and uses a standard Mendelian shuffle to create daughters, each with two copies of each gene.

Sister bees thus have a remarkably close bond–closer than human sisters. Human sisters inherit one of their father’s two genes, and one of their mother’s pair. Since the chance of inheriting any particular gene is thus 50 percent, human sisters share, on average, half of their genes. Sister bees, on the other hand, inherit identical genes from their father, because male bees have only a single set to give. Combined with their mother’s DNA, sister bees thus share on average three‑quarters of their genes. If a female bee were to have a daughter of her own, she would share only half of her genes with her offspring, the rest of them coming from her mate. A female honeybee thus has more in common with her sisters than her daughters.

Under these circumstances, Hamilton argued, it’s not surprising that worker bees forgo their own reproduction to work for the good of the hive. The larvae that they help to raise are so closely related to them that they can spread their genes more quickly than if they tried mating themselves.

With one swift jab, Hamilton punched through the paradox of altruism that had puzzled biologists since Darwin’s day. If evolution consists of a competition among individuals for survival and reproduction, it makes little sense to help others. Perhaps, some researchers suggested, animals acted selflessly for the good of the species or at least the good of a group. But that kind of altruism simply didn’t square with what biologists knew about how genes spread over time.

Hamilton looked at the question of altruism from the gene’s point of view. Altruism might not benefit the altruistic individual, but it might be a good way to make more copies of the altruistic individual’s gene. It raises an animal’s fitness, but not because it raises the animal’s own chances of reproducing. Hamilton called this indirect benefit of altruism “inclusive fitness.”

Hamilton’s rule of inclusive fitness has been confirmed splendidly. Not only are female workers more closely related to their sisters than to their own daughters, but they are more closely related to one another than to their own brothers. Brothers don’t receive any of the paternal genes that their sisters inherit from their father, and they share only half of their mother’s genes. Thus while a sister shares 75 percent of the genes of her sisters, she shares only 25 percent of her brother’s genes. In other words, she is three times more closely related to her sisters than to her brothers. This difference is reflected in the ratio of brothers and sisters in a nest. In the colonies of many social insects, the ratio of females to males is 3 to 1. It is the worker females, not the queen, who set that ratio. They take worse care of the male larvae than the female ones.

But inclusive fitness should produce the 3‑to‑1 ratio only in nests where the queen mates once and uses that same sperm to create her entire colony. If a queen should mate with another male and use his sperm as well, the sisters will not share their father’s genes. Liselotte Sundstrom, a Finnish entomologist, discovered colonies of Formica ants in which the queens mate either once or multiple times. In the single‑father colonies, she found that the 3‑to‑1 ratio of larvae reigns. But in the multiple‑father colonies, the ratio is close to 1‑to‑1. Since sisters are no more closely related to one another than to their brothers, there is no incentive to the workers to favor one sex over the other.