Introduction
I’ve spent most of this week reading and thinking about varroa so Tom’s follow up blog post couldn’t have arrived at a better time. Once again, thank you, Tom. I’m indebted to you for your support and for providing topical articles to help readers with many aspects of beekeeping. Another big thank you goes out to my regular sponsors and those who donate sometimes to the upkeep of this site. To my friends who are helping me find varroa resistant traits, photograph the evidence, and display the data from daily mite monitoring; Steve R, Cynthia and Louise–I appreciate your support enormously.
I also appreciate Steve Donohoe’s excellent blog and that he can produce such interesting and varied blogs every week. For beekeepers who think that leaving colonies alone to die out, or survive to be tolerant to varroa is the way to go will be enlightened by a recent blog post of Steve’s. It clarifies the differences between tolerance and resistance and why we must put in the groundwork and steer towards reducing varroa levels and promoting resistance. https://thewalrusandthehoneybee.com/varroa-why-treat/
Museum samples revealed rapid evolution of resistance to Varroa destructor in wild colonies
In my last piece for The Beelistener, I described how Varroa destructor reached where I live in New York State in the mid 1990s. Also, I discussed how a genetic comparison of worker bees that I collected from wild colonies in 1977 and in 2011—thus, 17 years before and 17 years after I first spotted V. destructor in my managed colonies in 1994—revealed that Varroa destructor had temporarily killed off most of the wild colonies living in trees and buildings in my area. Furthermore, I described how I discovered in the summer of 2001 that there were still wild colonies living in the Arnot Forest, a 16-km2 research forest that is owned by Cornell University. In this article, I will present a more detailed picture of how the natural selection for resistance to Varroa took place within the population of wild colonies living in the forests where I live.
To begin, I will share an aerial view of the area south of Ithaca, New York in which I have conducted most of my studies of wild colonies of honey bees. See Fig. 1. This is the region where I collected, in 1977 and again in 2011, samples of worker bees from wild colonies. This map shows the locations of the homes of the wild colonies that I located in 2011 and then monitored for many years thereafter. Some of these wild colonies were living in trees in the Arnot Forest, but others were living in various trees, barns, and farmhouses scattered across the hilly, and largely forested, countryside south of Ithaca.
Fig. 1. Map of the locations of the 38 wild honey bee colonies from which I collected samples of 100 worker bees per colony in 2011. The area shown in this map is approximately 40 km west to east and 30 km north to south.
In 1974, I started monitoring—in May, July, and September—the home sites of 42 wild colonies to learn about their longevity (Seeley 1978). As part of this study, I collected samples of worker bees from 32 of these wild colonies: 10 in the Arnot Forest and 22 in the forested hills south of Ithaca. From each colony, I collected a sample of ca. 100 worker bees, and I mounted each bee on an insect pin with a label that indicated the bee’s collection site and collection date. These pinned specimens were then archived in the Cornell University Insect Collection.
In 2011, I repeated the entire process of finding 32 wild colonies and then collecting samples of worker bees from these colonies. Again, 10 of the colonies were living in trees in the Arnot Forest, and the other 22 colonies were living in trees and buildings in the forested hills south of Ithaca. Fig. 2 shows the locations of the wild colonies that I sampled in the Arnot Forest. Fig. 3 shows what this forest looks like in autumn, when the trees have started to show their beautiful fall colors.
Fig. 2. Map of the Arnot Forest and adjacent land showing the locations of the 10 bee-tree colonies located in August 2011 and of the two commercial apiaries outside the Arnot Forest.
The apiary near the southeast corner of the Arnot Forest was short-lived; a black bear destroyed it in November 2011. Ever since then, this apiary site has been abandoned.
Fig. 3. View of the Arnot Forest in mid-September, looking east, from its highest point, ca. 600 meters above sea level.
In 2011, as in 1974, I collected a sample of ca. 100 worker bees from each colony. What motivated me to do this second round of specimen collecting was a chance visit in 2011 by a former Cornell student who had been my summer research assistant in 2000: Professor Sasha (Alexander) Mikheyev. Sasha is a Russian-American-Australian evolutionary biologist at the Australian National University (in Canberra) who studies how organisms adapt genetically to rapid ecological changes. When we talked about the arrival of Varroa, Sasha asked if I had samples of worker bees collected from wild colonies in the forests around Ithaca before the arrival of Varroa destructor. Happily, I had just the samples he had in mind… the ones that I had collected 29 years before, in 1977!
Thus it was that in October 2011, I shipped to Sasha 64 samples of worker bees that I had collected from 64 wild colonies living around Ithaca. 32 of these worker-bee samples were collected in 1977, thus 17 years BEFORE the arrival of Varroa in Ithaca in 1994. The other 32 samples were collected in 2011, thus 17 years AFTER the arrival of Varroa in this region. (I had first spotted Varroa in my managed colonies in 1994.)
What did Sasha’s genetic analysis of my samples reveal? First, when he looked at the mitochondrial DNA of the bees (i.e., the DNA that is inherited only maternally), he found a striking loss in its diversity between 1977 and 2011. Fig. 4 shows that nearly all the old (1977) mitochondrial lineages had gone extinct. These findings tell us that even though the density of wild colonies was the same in the 2010s as in the 1970s, most of the wild colonies living near Ithaca in 2010 were descendants of a small number of closely related queens. It is likely, therefore, that this population of wild colonies shrank markedly following the arrival of Varroa destructor. It is also likely that this collapse in the population of wild colonies resulted in very strong selection for colonies able to survive with Varroa. Probably, only a small fraction of the colonies, those with resistance to Varroa, survived. We also found that the worker bees that I collected in 2011 are markedly smaller in body size–that is, in head width and in distance between the bases of their wings–than the worker bees that I collected in 1977. How this reduction in body size contributes (if at all) to resistance to Varroa is unclear.
Fig. 4. Phylogeny of the mitochondrial genomes of the wild colonies of honey bees living in the forests south of Ithaca, New York, for the 1977 population (blue) and for the 2011 population (red). Most of the mitochondrial genetic diversity in the 1977 population is missing in the 2011 population. Evidently, the arrival of Varroa in the 1990s produced heavy mortality among the wild colonies and intense natural selection among these colonies for resistance to Varroa. The 2011 population of colonies has descended from a small number of closely related queens that were in the 1977 population.
Starting in 2015, one of my PhD students, David T. Peck, investigated the mechanisms of resistance to Varroa mites that are possessed by the survivor colonies in the Arnot Forest. There are two general possibilities: attack the adult female (mother) mites during the phoretic phase (when they are clinging to adult bees) or during the reproductive phase (when they are sealed in brood cells). David has found that colonies headed by queens from the Arnot Forest, relative to colonies headed by queens from commercial queen producers, have both a stronger grooming/chewing response to these mites and a higher percentage (ca. 40%) of brood cells that have been uncapped and recapped. The latter is one way that the bees can disrupt the mites’ reproduction.
An important take-home message from David’s work is that the worker bees in the wild colonies living in the Arnot Forest possess multiple behavioral mechanisms for suppressing the mite populations in their colonies. In short, they are deploying a diverse set of behavioral resistance weapons against Varroa destructor, not just a single “silver bullet.”
References
Mikheyev, A.S., M.M.Y. Tin, J. Arora, and T.D. Seeley. 2015. Museum samples reveal rapid evolution by wild honey bees exposed to a novel parasite. Nature Communications 6, 7991. Doi10.1038/nomms8991.
Seeley, T.D. 1978. Life history strategy of the honey bee, Apis mellifera. Oecologia 32,109-118.
Seeley, T.D. 2007. Honey bees of the Arnot Forest: a population of feral colonies persisting with Varroa destructor in the northeastern United States. Apidologie 38, 19-29.
Seeley, T.D. D.R. Tarpy, S.R. Griffin, A. Carcione, and D.A. Delaney. 2015. A survivor population of wild colonies of European honeybees in the northeastern United States: investigating its genetic structure. Apidologie 46, 654-666.
Hi Ann, thanks for your kind words, and for passing on the incredible work done by Tom Seeley. It is amazing to have detailed ‘wild bee’ data over such a long time period. The genetic bottleneck that occurred in the wild bees that Tom studied is something that concerns me, from a loss of diversity perspective. In the wild, the bees were forced into this due to the high selective pressure (death by varroa/DWV), but I would hope that breeding programmes by beekeepers would try to avoid such a loss of potentially useful genetic traits. Over the longer term there is a possibility of population death if the inbreeding gets too much.
Of course, all breeding programmes result in some loss of diversity; the promotion of certain traits and reduction of others. I think the goal of breeders should be resistant bees that are still productive and useful to agriculture. Even partial resistance, so that we only treat once per year using oxalic acid in brood free periods, would be a great step forward. I’m talking about the bees we all keep, not a few pockets that are the exception rather than the rule. As Kirsty points out in her article (the one you linked to), there are challenges in many countries like ours because the background population of honey bees is in a state of continual flux, as humans move them about.
My understanding of human evolution is that all of us, big/small, black/white, came from a tiny ‘survivor population’ in Africa, and that worked out pretty well (for humans, if not the rest of nature). Unless we live in a small part of Africa, we are all immigrants, and an invasive species!
best wishes,
Steve