Why do queen bees mate with so many drones? How does the colony decide what drones to evict? And, while we are at it, why are there drones at all…? Science writer Dave Black scours beekeeping literature for the answers, pulling a 100 year-old leather-bound ‘treatise’ from his bookshelf before detailing the latest findings from academia.
By Dave Black
My favourite ‘bee book’ must be Life of the Bee. I have a leather-bound pocket edition from April 1910, printed in Edinburgh and translated from the original French La Vie des abeilles by Alfred Sutro, a friend of the author, Maurice Polydore Marie Bernard Maeterlinck[i].
It’s an unlikely, but worthwhile, combination. Maeterlinck was a Belgian symbolist writer, playwright, and poet, beekeeper but not a scientist. The book is as well observed and technically accurate as any 100 year-old bee treatise could be, just better written than most. As it should be from a Literature Nobel Laureate.
In the penultimate chapter ‘The Massacre of the Males’ he describes the hive’s autumn wind-down, and the fate of the drones:
"Indelicate and wasteful, sleek and corpulent, fully content with their idle existence as honorary lovers, they feast and carouse, throng the alleys, obstruct the passages and hinder the work, jostling and jostled, fatuously pompous, swelled with foolish good natured contempt; harbouring never a suspicion of the deep and calculating scorn wherewith the workers regard them, of the constantly growing hatred to which they give rise, or of the destiny that awaits them."
The drones of course are not just sacrificed for the coming winter, a colony’s investment in potent males is one of a number of outcomes that advantage the colony’s reproduction in one way or another. Drones may or may not be as uselessly indolent as Maeterlinck thinks, but the deeper question is why are there drones (plural) at all; why polyandry (many fathers) when you could have just one (monandry), and why as many as 30 or more, and not, say, six? While we’re at it, why not polygyny, (multiple mothers), surely that’s an equivalent outcome? As all these permutations are found in the Hymenoptera order of insects, more empirically we might ask ‘how’ instead (Science doesn’t do ‘why’) can we explain the evolution of multiple mating?
Kinship
One explanation for colonies of social insects is that they gather because of a common interest in reproducing their genes, they could be highly related families. In other words, social because ‘kinship’. This is especially true if the male mate has a half set of chromosomes. These haploid males are of course, relatively frail, with a limited number of genetic answers to environmental challenges they may face. A female mated to such a male (haploid/diploid mating) produces offspring closely related to the parents, although multiple mates would actually reduce the degree of relatedness.
Despite this, multiple mates confer a number of advantages. In honeybees, sex chromosomes need to be pairs of different chromosomes (for females), or unpaired (for hemizygous, haploid males). Pairs of the same chromosomes (in diploid males) are a fatal combination. More mates reduce the chance of the female mating with a male carrying a matching chromosome and producing inviable (male) eggs. It also allows her to ‘harvest’ a greater quantity of spermatozoa, she can lay more eggs for longer, without having to risk subsequent mating trips. Less obviously, the queen and her worker family have to resolve a strategic conflict over which sex to invest their resources in. In order to promulgate their genes workers should invest in producing more queens, not drones, because queens are the only ‘sister’ that mates and are more closely related. While queens (equally related to their sons or daughters), should have no preference. Multiple mating minimises this conflict as the worker ‘relatedness’ decreases.
Not only can these multiple-mating colonies be big, and long-lived, but there’s a strength in diversity. The greater number of possible genetic combinations produce slightly different individuals, permits task specialisation and division of labour, and increases the group’s tolerance to a greater range of environmental challenges, pathogens and parasites. However, the Law of Diminishing Returns applies, you can have too much of a good thing.
Assessing the Family
It's not very likely that one or other of these reasons is the important one, but that all of these reasons at one time or another, have had a different value for the evolution of the six or so species of Apis bees we have today. Nor is this a settled process, the closer we look we continue to see that this subtle genetic competition between the interested parties continues. In a paper published this March a group at Purdue University wondered if non-reproducing workers can assess the reproductive quality of their queen, it wouldn’t be surprising if they could assess their drones too. After all, they are not particularly related, and drones are very ‘expensive’. Do workers ‘harbour a deep and calculating scorn’ for drones as Maeterlinck would have it?
The Purdue study[ii] took measures of drone quality, size, and cuticular hydrocarbon profile (CHC, the waxy layer on the outside of the exoskeleton, can be an indicator of ‘unhealthy’ individuals), and looked to see if the workers discriminated against drones using differences in these indicators. They carefully measured drones, before subjecting some of them to an ‘immune challenge’ by injecting them with part of the lipopolysaccharide membrane from Escherichia coli, and then verified that the immune-challenged (IC) males actually lost weight and shifted their CHC profile.
The drones were added to colonies set up to test whether the workers would assess and evict the IC drones more frequently, and it was clear that IC drones, and small drones regardless of their health status, were evicted significantly more often. However, it wasn’t clear that the workers used CHC profiles at all and the study suggested they pay no attention to the CHC on a drone. They do pay attention to size. Lots of research as well has shown that larger drones are more likely to be found at drone congregation areas, more likely to mate successfully, and that size correlates with their fertility.
So, does nature select for lots of big drones? Not exactly. Apis colonies may have the ability to be choosy, but are they always? Large colonies can host more drones than smaller ones, they don’t need to be as fussy. If colony resources are low, as in the autumn Maeterlinck presages, drones are evicted. During any periods of abundant food availability eviction becomes a less likely choice. Size also correlates with flight onset in drones (smaller drones start to fly earlier than a larger individual of equivalent age) and they go on mating flights more often[iii]. By doing this, at a colony level, the dispersal of mating flights from drones over the course of time increases the chances of mating with nearby queens, a rationale of ‘if you aren’t the best, be the first’. Nature always hedges her bets.
I’ll leave the last word to my man Maurice, from one of his earlier essays. “How strangely do we diminish a thing as soon as we try to express it in words”.[iv]
Dave Black is a commercial-beekeeper-turned-hobbyist, now working in the kiwifruit industry. He is a regular science writer providing commentary on “what the books don't tell you”, via his Substack Beyond Bee Books, to which you can subscribe here.
References
[i] Even with the current ridiculously long copyright terms, copyright on this work expired long ago and it’s easy to find free reproductions of the text on the internet.
[ii] Gilchrist, I.R., Nixon, J.M., Shultz, R.R., Ginzel, M.D., Harpur, B.A., 2024. To house or oust: Honey bee (Apis mellifera) colonies can evaluate and evict drones of low quality. Behav Ecol Sociobiol 78, 47. https://doi.org/10.1007/s00265-024-03461-8
[iii] Metz, B.N., Tarpy, D.R., 2022. Variation in the reproductive quality of honey bee males affects their age of flight attempt. PeerJ 10, e13859. https://doi.org/10.7717/peerj.13859
[iv] The Treasure of the Humble (Le Trésor des humbles): Maurice Maeterlinck, 1897
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