Honey bee sex determination: why a drone has no father

Honey bee sex determination creates a family tree that would look impossible in humans: a normal drone has a mother but no father. He can, however, have a maternal grandfather. This is a direct consequence of the way bees use fertilized and unfertilized eggs.

Humans are diploid: most of our cells carry two chromosome sets, one from each parent. Many bees, wasps, and ants use a different arrangement called haplodiploidy. Females are usually diploid, while males are haploid and carry only one chromosome set.

One chromosome set instead of two

In the western honey bee, Apis mellifera, females have 32 chromosomes, arranged as two sets of 16. A normal drone has only 16, all inherited from his mother.

After mating, a queen stores sperm and can use it when laying eggs. A fertilized egg receives one chromosome set from the queen and one from a male. It will usually develop as a female, becoming either a worker or a future queen.

An unfertilized egg receives no paternal chromosome set, yet development can still proceed. It normally becomes a drone. This is a form of parthenogenesis: development without fertilization.

That produces the apparent genealogical paradox. A drone has no biological father because no sperm contributed to the egg from which he developed. But his mother is a diploid female that herself came from a fertilized egg. So the drone can have a maternal grandfather even though he has no father.

There is another unusual consequence. A drone receives his entire genome from his mother and passes his single chromosome set to his daughters. Genetic relationships inside a bee colony therefore do not follow the same arithmetic as relationships in an ordinary diploid family.

The molecular switch is more complicated than the simple rule

The textbook shortcut “unfertilized egg equals male, fertilized egg equals female” is useful, but in honey bees it is not the whole mechanism.

In 2003, Martin Beye and colleagues identified the molecular basis of a key sex-determining switch in Apis mellifera. The gene is called complementary sex determiner, or csd.

The csd gene exists in many alternative versions, or alleles. When a developing embryo carries two different csd alleles, the female developmental pathway is activated. A normal haploid male has only one copy and therefore only one allele.

But there is an important exception. A fertilized egg can inherit the same csd allele from both parents. It is diploid, yet it can develop as a diploid male rather than a female. Two chromosome sets alone are therefore not sufficient to guarantee female development.

The probability of producing such diploid males rises when a population has fewer csd alleles and genetically similar parents are more likely to carry matching versions. In honey bee colonies, workers commonly remove diploid male larvae, so producing them represents a real loss of brood.

This distinction matters beyond honey bees. Haplodiploidy describes the broad organization of chromosome inheritance, but the molecular machinery that determines sex is not identical across all Hymenoptera. The csd mechanism of Apis mellifera should not simply be assumed to apply to every bee, wasp, or ant.

What this does to relatedness inside a colony

Haplodiploidy also changes how closely colony members are genetically related.

In the simplest case, if a queen mates with only one male, all of her daughters receive the same paternal haploid chromosome set. From the queen, each daughter receives a different random half of her maternal genetic material.

Under those idealized conditions, full sisters can have an average relatedness of 0.75, compared with about 0.5 for ordinary diploid siblings. This unusual arithmetic became an important part of evolutionary thinking about social behavior in Hymenoptera.

But haplodiploidy is not a complete explanation for eusociality. Many haplodiploid species are solitary, and honey bee queens normally mate with multiple males, making the real pattern of relatedness within a colony more complicated than the textbook example.

Sex and caste are also separate questions. Both workers and queens are female. Once an embryo is on the female developmental pathway, other mechanisms determine whether it becomes a worker or a reproductive queen. In Apis mellifera, larval nutrition and developmental signaling are central. In stingless bees of the genus Melipona, studied extensively by Brazilian geneticist Warwick Estevam Kerr, genetic factors can also contribute to caste development.

Kerr is often remembered by the public because of the history of Africanized honey bees. Yet his work on bee genetics points to a more fundamental story: in these insects, even the structure of a family tree follows rules very different from our own.

A normal drone has no father. That does not mean he has no male ancestors. To find one, you simply have to move one generation farther back.