Haploid drones are mortally sensitive to environmental stress, but this could actually lead to stronger colonies
Drones might look robust, with their wide bodies, large eyes, and powerful wing muscles. But despite their skookum appearance, they are shockingly sensitive to environmental stress. Compared to workers, they are more likely to die from exposure to disease, toxins, or temperature stress. New research by Dr. Selina Bruckner and her colleagues shows that drones are also disproportionately harmed by varroa infestation and insecticide exposure — a feature that is rooted in their DNA.
At the 2021 American Bee Research Conference, Bruckner, a postdoc at Auburn University, Alabama, described how drones are more likely to perish when they are infested by varroa as developing pupae, with higher death rates than what had been previously observed in workers. And by feeding colonies pollen patties laced with small amounts of thiamethoxam and clothianidin (two common neonicotinoid pesticides), Bruckner and her colleagues discovered that mortality was biased towards drones there, too, and was higher than in colonies fed pollen patties alone.
“Both neonicotinoids and varroa mites individually reduced survival of drones,” Bruckner says, “but this reduction was even greater when drones were exposed to both stressors together.” Drones that experienced both the pesticides and varroa infestation had such a high mortality that it qualified as a synergistic effect, where the combined treatment was more lethal than the summed effect of individual parts. Other research that Bruckner was involved in showed that the drones which did survive pesticide exposure suffered from developmental abnormalities.1
“Drones are generally overlooked in research because they are only seasonally produced and don’t participate in division of labor,” says Bruckner. “But having good quality drones is very important for the long term since the queen relies on their sperm in order to lay eggs.” Most research on drones agrees that they are more sensitive to stress than females, but exactly why this is the case is less certain.
The haploid handicap
Some scientists suggest that drones are so fragile because they have only one set of chromosomes (also known as being “haploid”), giving them no opportunity to compensate for inferior genes with alternate gene versions (alleles). Workers, on the other hand, have two sets of chromosomes (they are “diploid”); therefore, if one gene has a harmful mutation, they have another copy to fall back on, making them more likely to be able to withstand challenges like pesticides and parasites.
This idea, known as the haploid susceptibility hypothesis, is not unique to honey bees; it has also been supported in other insects with haploid males, such as ants and wasps.2,3 This apparent handicap is even evident in varroa mites, which follow the same sex system as honey bees. Most people have never even seen a male varroa mite, for example, since they die shortly after their host bee emerges.
But although it is widespread, haploid susceptibility seems counter-intuitive: A drone’s specialty is reproduction, arguably the most important job to ensure the survival of a species. So, how could such an ostensibly deleterious system — male haploidy — even evolve?
Like many aspects of a drone’s life, haploid susceptibility could be viewed as a sacrificial act, helping to sustain higher species fitness through a form of genetic cleansing. With no alternative alleles to compensate for those with lethal mutations, haploid drones carrying harmful alleles act as genetic martyrs, leaving behind a population of males with more robust genes to pass on to the next generation.
Since drones are born from unfertilized eggs, all of their genes come from the queen, and haploid susceptibility helps maintain a lineage that is free of genetic aberrations. This stabilizing effect doesn’t exactly explain how male haploidy arose, but it could promote its success once the transition is underway.
The Selfish Queen
Another driving force behind the evolution of male haploidy is that from the queen’s perspective, male haploidy is advantageous because it enables her to propagate a larger fraction of her genes. Female advantages are more strongly favored because females typically invest more resources into reproduction than males — a honey bee egg is roughly a million times bigger than a sperm cell, for example. Producing larger sex cells and, in the case of mammals, nurturing a developing fetus, are costly activities, thus limiting the number of offspring females can produce relative to males. Females, therefore, have fewer opportunities to propagate their genes, and are under strong selection to maximize their genetic contributions in other ways.
A female advantage helps balance the scale, but in the case of the honey bee, that scale has tipped far in the females’ favour. “The queen’s aim is to pass on as many of her own genes as possible,” Buckner explains. “She is basically monopolizing the gene pool. Her sons will always pass on her genetic material, and since those drones are going to be mating with new queens, she is distributing her genes into other colonies.”
As Richard Dawkins argues in “The Selfish Gene,” natural selection acts on genes indirectly through the individual carrying them, who can be regarded as merely a vehicle. Sex systems like haplodiploidy (where males are haploid and females are diploid) give the queen a selective advantage because a greater fraction of her genes may go forth and prosper than if the males were diploid too.
By this view, drones are really just vectors of the queen’s genes, and haploid susceptibility weeds out the ones with bad alleles.
“The genes are master programmers,” Dawkins writes, “and they are programming for their lives. They are judged according to the success of their programs in coping with all the hazards which life throws at their survival machines [bodies], and the judge is the ruthless judge of the court of survival.”
Likewise, this idea of genes being the fundamental unit of selection is the widely accepted rationale behind the evolution of insect societies, where sisters are unusually closely related. Consider humans, where both males and females have two sets of chromosomes: One of your sets comes from a shuffled mix of your mother’s chromosomes, and the other is a shuffled mix of your father’s. If you have a sibling, this means that the two of you share about half your genetic material, and likewise, you would share half with your child. In honey bees, since the father has only one set of chromosomes, no shuffling can occur, and full sisters receive ….