Sex-ratio conflict in social Hymenoptera

Sex-ratio conflict in social Hymenoptera is a conflict between queens and workers over how much a colony invests in male and female reproductives. Its significance in the book’s argument is that even where individuals share genes and depend on one another, their positions within a reproductive system can give them different genetic interests: the queen’s predicted optimum is equal investment in the sexes, while the workers’ is three parts female to one part male. A comparison of 20 ant species found a close fit to the workers’ prediction, suggesting that the workers’ practical control of the nursery helps determine the colony’s reproductive allocation.

The reproductive interests behind the conflict

In the account’s gene-centered framework, reproductive outcomes matter because they affect how copies of genes are propagated. A queen and her workers are not genetically different kinds of individuals in the sense relevant to this argument. Yet the same gene can have different opportunities depending on whether it operates through a queen’s body or a worker’s. From the queen’s position, equal investment in male and female reproductive offspring is favored. From a worker’s position, investing more heavily in females is advantageous, because workers are more closely related to their full sisters than to their brothers.

The tension becomes especially clear when the workers are described as farming their mother as a producer of reproductive siblings. Workers need to curb the queen’s tendency to produce equal numbers of males and females if the colony is to maximize the spread of the workers’ genes. Calling the queen a brood mare and the workers farmers captures the book’s model of the relationship, but the image also expresses a contest over control: the queen produces the offspring, while workers can influence how the colony allocates its care and resources.

Why the predicted ratios differ

The contrast depends on the relatedness calculations used for Hymenoptera. Full sisters share a father, and the two sperm cells that conceived them are identical in every gene. A female therefore has a 50 percent chance of sharing with her sister a gene inherited from their mother, but a 100 percent chance of sharing a gene inherited from their father. The resulting relatedness between full sisters is three-quarters, rather than the one-half expected between siblings in ordinary sexual animals.

This high relatedness makes a worker’s sisters especially valuable from the gene’s-eye perspective. A worker is more closely related to her full sisters than to her own offspring of either sex, which can favor foregoing reproduction and instead influencing the mother to produce more sisters. The advantage is not identical from the queen’s perspective. A queen’s stable investment ratio remains one to one, whereas the worker’s stable ratio is three to one in favor of sisters over brothers. The difference is a conflict between positions in the same system, not a contradiction about what genes are: a gene’s advantageous strategy depends on the body and the means of influence available to it.

The conflict as a testable prediction

Robert Trivers and Hare translated the difference in relatedness into a prediction about investment in reproductives. They calculated that the queen’s optimum is equal investment in males and females, while the worker’s is three to one in favor of females. The prediction concerns investment, not simply head counts. Since male and female reproductives can differ greatly in size, counting individuals alone would not provide the relevant comparison.

To test the theory, Trivers and Hare examined 20 ant species and estimated the reproductive sex ratio by weighing the large winged males and females. These are the reproductives that leave the nest in periodic bursts for mating flights; young queens may then attempt to establish colonies. By measuring investment in the two sexes, the researchers addressed the distinction between numbers and resources that the prediction requires. Their results showed a close fit to the predicted three-to-one female-to-male investment ratio.

Who controls the nursery

The measured result supports the interpretation that, in the ants studied, the workers win this conflict of interest. The account links that outcome to practical power rather than to a difference in genetic identity: worker bodies guard the nurseries and can exercise greater influence over the reproductive system than queen bodies. Genes acting through workers can therefore outmaneuver genes acting through queens, even though the queen is the mother of the reproductives and the workers are her offspring.

The result also makes the ratio an indicator of competing interests, rather than a simple expression of one colony-wide optimum. A ratio nearer three female units of investment for each male accords with the workers’ predicted interest; equal investment accords with the queen’s. The ant comparison thus turns an abstract disagreement about relatedness into an empirical question about who has practical control over the brood and whether the resulting allocation follows the workers’ or the queen’s predicted strategy.