Could inbreeding be causing the honey bee health challenges we see today? Many people think so, but it’s not supported by the science. Regardless, I have seen this argument made not only in news articles, but also by hobbyist beekeepers and even in US federal reports. I have been speaking with Dr. Amro Zayed (from York University, Canada) about the topic, and here I’ll start unpacking the diversity dispute.

Let’s first explore how the misunderstanding arose. It’s true that genetic diversity is key for species’ survival, including honey bees. Evolutionary theory states that if there’s more diversity in the population, chances are higher that some individuals will persist, or even thrive, when a disaster strikes (read: Varroa destructor). We also know that domesticating animals – like we’ve been doing with honey bees for the last ~9,000 years – usually stifles genetic diversity. Whereas natural selection favours the fittest individuals (those which are best at surviving and reproducing), domestication via human selection puts intense pressure on a few traits which are often not aiding survival, like gentleness or colour. Usually, this involves inbreeding. Dogs are one of the most extreme victims of this: breeds have been so inbred that they are plagued with diseases like hip dysplasia and cancer – a phenomenon which is also known as inbreeding depression.

Managed honey bee colonies in Europe and North America do have far lower genetic diversity compared to their wild African counterparts. Combined with observing that African colonies are more resilient to diseases and pests, this sparked the idea that domestication could be blamed for many of our beekeeping woes. But Brock Harpur, Amro Zayed and their colleagues saw some fundamental flaws in this logic. “We are interested in understanding if managed bees have different levels of genetic diversity than the ‘pure’ subspecies they were derived from,” Zayed explains. In their 2012 Molecular Ecology paper, they argue that to make claims about the human influence on honey bee diversity, we should not compare managed colonies to wild African ones, but to the specific population that gave rise to the domestic stock we have today. Here’s why.

founder
Figure 1. Illustrating the founder effect and admixture. Colours represent genetic diversity (more colours = higher diversity). 1) The founder effect happens when a small group of individuals found a new population. Since there are few founders, they usually carry little genetic diversity. 2) Admixture via human movement of colonies across geographic barriers introduces new genetic diversity.

 

Right now, our best guess is that honey bees migrated out of North Africa or the Middle East to colonize other parts of Asia and Europe. A small subset of colonies participated in this geographic expansion, which means that they probably also had only a fraction of all the genetic diversity of the bigger ancestral pool (Figure 1). This is a well-known phenomenon in biology called the founder effect. Importantly, this means the new European populations (which gave rise to our domestic stock) might have already had limited diversity before domestication even happened. Previous researchers unknowingly mixed up human effects and the founder effect, with no way to disentangle them – until now.

Harpur and Zayed found that while domestic honey bees do have lower diversity compared to wild African colonies, they have significantly higher diversity than the founder populations they originated from. This means that honey bees went through a genetic bottleneck when they colonized Europe initially, but human management is reversing this effect, not aggravating it. “The paper was vigorously challenged by some colleagues,” Zayed admits. It was published a long time ago, by scientific standards (2012) “but it’s gaining in influence, if recent citations are an indictor of this.” One criticism of their work is that they measured diversity using old sequencing technology and looked at only a fraction of the whole genome. However, Zayed notes that the findings have been validated by much larger studies using whole genome sequencing (a more sophisticated technique).

In the paper, they explain that managed colonies gain higher diversity because of admixture, or genetic mixing of previously isolated populations. For example, humans tend to move colonies across long distances – between states, countries and continents – allowing queens to mate with drones they would otherwise never contact. Although this increases the diversity, it does not mean that moving colonies around the world is always a good thing.

While some admixture is helpful, it can also have consequences. “A little genetic exchange can be beneficial because it helps maintain levels of genetic diversity, and genetic diversity is important because it fuels evolutionary change. But too much can limit a population’s abilities to adapt to its local environment.” Biologists call this outbreeding depression. To illustrate why this is a problem, imagine you’re trying to breed a line of hygienic bees, but you (or your neighbours) occasionally replace your dead-outs with imports. If mating isn’t 100% controlled, genetic mixing between your hygienic line and the unselected, maladapted imports will dilute your efforts. In nature, admixture can be harmful for locally adapted native honey bees if they breed with imports that are less fit for that geographical region. Furthermore, colony movement also accelerates spreading disease. The most obvious example of this is the varroa mite, which has hitch-hiked to every habitable continent during the last half century (including Australia, which was mite-free until 2016).

Several other features of honey bee biology give them an upper hand when it comes to promoting diversity, too. Natural selection (and beekeeper selection) disfavours colonies headed by inbred queens because they tend to be weaker than their outbred counterparts. They lay shotgun brood patterns, which happen because inbreeding increases the chances of laying abnormal drones. To explain, a special sequence of DNA called the csd locus (which stands for complimentary sex determination) dictates a bee’s sex. Normally, bees with one copy of the csd locus develop into drones and bees with two copies develop into workers, but drones can also develop if the two copies of the sequences are identical. This makes the second copy biologically invisible, tricking the embryo to become male even though the rest of its DNA resembles a female’s. The adult workers notice this and kill most of the abnormal drones before they become adults, but since these sacrificed brethren were meant to be workers, the colony’s workforce weakens, making it less fit than outbred colonies. Furthermore, queens with fewer mates, even if they’re outbred, also have shorter life spans compared to queens with many mates.

Finally, and what might be most interesting for molecular biologists like myself, honey bees have incredibly high rates of genetic recombination, which is like molecular mixing and matching of DNA (Figure 2). When sperm and eggs are made, pieces of DNA are swapped between chromosomes to create new sequence combinations. Honey bees do this more than any other animal that’s been measured, although we’re not sure why. To put it into perspective, in humans there are about 2 or 3 DNA swapping events per chromosome whereas in bees, there are up to 50. The number of new sequences that can be made with these kinds of recombination rates, given some baseline level of diversity, is staggering.

Fig2
Figure 2. Genetic recombination in humans and honey bees. In the early steps of forming sperm and eggs, pieces of DNA are swapped between chromosomes to create new sequences: a process which occurs excessively in honey bees.

Limited genetic diversity could still become an issue for honey bees in the future and researchers agree that diversity should be promoted and preserved where possible. After all, the most efficient way of solving a problem is to prevent it from ever happening. “Managed bees have a lot of genetic diversity, and arguments suggesting that low diversity or inbreeding is impacting honey bee health are not warranted,” Zayed summarizes. There are other things humans do that cause problems for bee health, like over-using pesticides or inadequately managing disease, but for once genetics is an area where we are so far not the problem.

This article appeared in the June 2017 issue of American Bee Journal.

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