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 Genetic Aspects of Queen Production

Presented by Tom Glenn at the A.N.E.R.C.E.A. queen breeders meeting in Abbeyville, France 11/24/07

Gyandromorph  honeybee

I have looked at around one billion bees over the last 30 years, and in all of those bees, this is the only one I’ve seen quite like this one.
Take a good look at this drone because he appears to be a paradox. A drone only has one parent, and a single set of genes, so he should either have the normal dark eyes or a mutation like this white eye, but not both. This is a mystery that we will solve by the end of this talk.
In the process we will also discover some of the fundamental reasons why bees organize into such successful societies.
As beekeepers we are working with colonies rather than just individual animals. That makes bee breeding both more complex and interesting than breeding any other animal on earth.

 

Haplo/diploidy is key in explaining the nature of bees

In fact, it is the the odd genetic quirk of the drone hatching from an unfertilized egg, and thus having only one parent, that makes breeding bees different than breeding any other animal. This haplo/diploid genetic system is a key factor in why bees have developed as social insects. It explains why it makes genetic sense for the workers to not lay eggs, but to instead work cooperatively with their sisters to help the queen reproduce.


The key point is that drones hatch from eggs which are not fertilized by sperm. Since he receives a random half of the queens genes in a single set of 16 chromosomes he is termed haploid. Females, either workers or queens, get a set of 16 chromosomes from both the egg and the sperm. They carry 32 chromosomes in each of their cells, so are diploid, two sets of chromosomes.


Every bee is unique because of recombination of the queen’s chromosomes during egg formation (meiosis). So every individual, male or female has a unique genotype, no two bees are the same. In fact it’s been found that there is far more recombination or "crossing over" of chromosomes in honeybees than in any other animal studied so far. Recombination is a source of variation, and variation is the raw material of adaptation. It seems that the bees’ own genetic strategy is to generate and maintain an extra large degree of genetic variation. Perhaps this what has allowed them to adapt to nearly all areas of the Earth.


There are two very important aspects about haploid drones that bee breeders need to consider:


1) Drones produced from a queen contain only her genes. Drone eggs are not fertilized. A drone will contain only the queens genes no matter whom the queen has mated to. When we are selecting drones, we pay attention to the genetics of the queen alone, not who she was inseminated with. Her drones would be the same drones as if she was unmated. This fact can be used to advantage in breeding programs. Even uncontrolled naturally mated queens can be used to produce pure drones of the line of the queen.


2) Since a drone has only one set of chromosomes, all 10 million sperm can only contain that single identical set of chromosomes, so the sperm are all clones. Whereas the eggs have a great deal of genetic diversity, the sperm have none.
This has an interesting effect on the genetic relationships of bees in a colony. Eggs that are fertilized with one drone’s sperm produce a subfamily of very closely related workers and are termed supersisters. They share 75% of their genes because they share on average 50% of the queen’s genes but 100% of the drone’s genes.


A basic principle of evolution is that organisms do what ever will get more of their genes into the next generation. This puts the worker in an unusual evolutionary position. If a worker were to lay eggs, her own offspring would share only 50% of her genes, but a supersister shares 75%. From a worker’s point of view it is better to help the queen raise more supersisters than it would be for her to reproduce herself. Workers have given up reproduction because it makes genetic sense for them to do so. By all the workers cooperating in brood rearing, and resource gathering they have discovered the great advantages in social living and have become one of the most successful organisms on earth.

 

Good brood patterns depend on sex allele diversity

Honey bee sex alleles. Complentary sex determination

I just stated that drones hatch from unfertilized eggs, but there is a little more to the story. The more complete reason is that there is a single gene called the sex allele which has at least 19 variations. There is a very simple rule that determines if an egg will develop into a male or female. A female must always haves two different variations or alleles, receiving one from the mother and one from her father. But if there is only one allele present then the bee develops as a male.
There are two ways that only a single variation may be present. The egg may not be fertilized, so can have only one variation and so becomes a drone. But another way is for a fertilized egg to by chance receive the same allele from both mother and father. In this case the bee develops into a diploid drone. The diploid drone will be infertile because normal sperm can not develop. Because this bee is of no use to the colony the larva is eaten by workers as soon as it is recognized. The effects we see are empty cells scattered among the brood. This is a severe form of inbreeding depression which puts limits on the practicality of utilizing close inbreeding in the breeding of bees.
If you inseminate queens with a single drone you will find most of them will have excellent brood patterns because none of their brood is wasted. But sometimes if they had the unlucky combination only 50% of their brood is viable, and the brood pattern is spotty, a condition known as shot brood.

Doubles, you lose.
Inbreeding causes shot brood patterns.

One effect of this gene is that rare variations are favored because they rarely meet another one similar to itself. But over time as they become more common in the population, they are more likely to be weeded out and then less favored. So negative feedback tends to maintain a balance of genetic diversity. This is Shot broodGood brood patternanother mechanism the bees have of maintaining a lot of genetic diversity.
This is why it is good to keep a few new genes entering your breeding population, to maintain good brood viability.

 

It is hard to say what is cause and what is effect, but this single gene, the sex allele may be the reason why queens mate with so many drones.

 

 

Multiple mating of queens (polyandry)

One way to reduce the risk of having a weakened colony because of poor brood viability is for the queen to mate with a lot of different drones. Chances are that if a queen mates with 10-20 drones, only a small number of them will share sex alleles in common with the queen. So there is less risk that an unlucky mating will hurt her colony. Multiple mating of honeybees


Drone congregation areas draw thousands of drones from hundreds of different colonies. They are beautifully designed to let the queen collect genes from kilometers around. They believe in mixing things up a bit when it comes to mating. This is yet another way that the bees’ own natural mating system maintains a lot of genetic diversity.Multiple mating in honeybees


 

 

 

Polyandry must be very important to the survival and evolution of the honeybee species. Mating is risky, it entails the queen flying far away from the hive into a dangerous world. She puts herself at extra risk by spending the time and effort to mate with so many drones. The sperm mix in the queen's oviducts and then migrate to her spermatheca where it is stored for years. She ends up storing only the amount from about one half of one drone's amount of sperm, yet she goes out of her way to mate with 10-20 drones. By instinct the queen is collecting a good sample of the genetic diversity available. DNA is really just information collected by the species from millions of years of survival, and the honeybee strategy is to utilize as much of this information as possible. It was just recently proven that this extra genetic diversity does in fact give a colony more resistance to diseases.

So it could be that this single gene, the sex allele, is the cause of polyandry; with the side effect of disease resistance, something natural selection would certainly reward.

Next page: Dominant Traits of Honeybees

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