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Host brood traits, independent of adult behaviours, reduce Varroa destructor
mite reproduction in resistant honeybee populations
Nicholas Scaramella, Ashley Burke, Melissa Oddie, Bjørn Dahle, Joachim de
Miranda, Fanny Mondet, Peter Rosenkranze, Peter Neumann, Barbara Locke
PII: S0020-7519(23)00092-9
DOI: https://doi.org/10.1016/j.ijpara.2023.04.001
Reference: PARA 4553
To appear in: International Journal for Parasitology
Received Date: 16 December 2022
Revised Date: 12 February 2023
Accepted Date: 5 April 2023
Please cite this article as: Scaramella, N., Burke, A., Oddie, M., Dahle, B., de Miranda, J., Mondet, F.,
Rosenkranze, P., Neumann, P., Locke, B., Host brood traits, independent of adult behaviours, reduce Varroa
destructor mite reproduction in resistant honeybee populations, International Journal for Parasitology (2023),
doi: https://doi.org/10.1016/j.ijpara.2023.04.001
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Host brood traits, independent of adult behaviours, reduce Varroa
destructor mite reproduction in resistant honeybee populations
Nicholas Scaramellaa,*, Ashley Burkea, Melissa Oddieb, Bjørn Dahleb,c, Joachim de
Mirandaa, Fanny Mondetd, Peter Rosenkranze, Peter Neumannf,g, Barbara Lockea
aDepartment of Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden
bNorges Birøkterlag, Dyrskuevegen 20, 2040 Kløfta, Norway
cFaculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences,
Ås, Norway
dINRAE, UR 406 Abeilles et Environnement, 84914 Avignon, France
eApiculture State Institute, University of Hohenheim, Erna-hruschka-Weg 6, 70599 Stuttgart, Germany
fVetsuisse Faculty, University of Bern, Bern, Switzerland
gAgroscope, Swiss Bee Research Center, Bern, Switzerland
*Corresponding author. Nicholas ScaramellaInst för Ekologi, Box 7044, 750 07, Uppsala, Sweden.
E-mail address: : Nicholas.Scaramella@slu.se
2
Abstract
The ectoparasitic mite Varroa destructor is an invasive species of Western honey bees (Apis
mellifera) and the largest pathogenic threat to their health world-wide. Its successful invasion
and expansion is related to its ability to exploit the worker brood for reproduction, which results
in an exponential population growth rate in the new host. With invasion of the mite, wild
honeybee populations have been nearly eradicated from Europe and North America, and the
survival of managed honeybee populations relies on mite population control treatments.
However, there are a few documented honeybee populations surviving extended periods
without control treatments due to adapted host traits that directly impact Varroa mite fitness.
The aim of this study was to investigate if Varroa mite reproductive success was affected by
traits of adult bee behaviours or by traits of the worker brood, in three mite-resistant honey bee
populations from Sweden, France and Norway. The mite’s reproductive success was measured
and compared in broods that were either exposed to, or excluded from, adult bee access. Mite-
resistant bee populations were also compared with a local mite-susceptible population, as a
control group. Our results show that mite reproductive success rates and mite fecundity in the
three mite-resistant populations were significantly different from the control population, with
the French and Swedish populations having significantly lower reproductive rates than the
Norwegian population. When comparing mite reproduction in exposed or excluded brood
treatments, no differences were observed, regardless of population. This result clearly
demonstrates that Varroa mite reproductive success can be suppressed by traits of the brood,
independent of adult worker bees.
Keywords: Apis mellifera, Varroa destructor, Natural selection, Suppressed mite reproduction
(SMR), Varroa-resistant honey bees
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1. Introduction
The Varroa destructor mite is an invasive ectoparasite of the Western honey bee (Apis
mellifera) and undeniably the largest pathogenic threat to honey bee health, severely impacting
apiculture and agricultural crop production that relies on honey bees for pollination services.
The Varroa mite is completely dependent on the honey bee colony for survival with a
reproduction cycle tightly synchronized to pupa development inside brood cells (Steiner et al.,
1995; Rosenkranz et al., 2010). In the mid-20th century, the Varroa mite made a host jump
from the Asian honey bee (Apis cerana) to the Western honey bee species and has successfully
spread throughout the world, with only a few isolated locations remaining mite-free (de
Guzman and Rinderer, 1999; Oldroyd, 1999; Rosenkranz et al., 2010).
One of the most significant factors influencing the successful invasion and expansion of
the Varroa mite with its new host is the ability of the mite to exploit and capitalize on the worker
brood for reproduction. In contrast, Asian honey bees exhibit a variety of host traits that limit
the ability of mites to reproduce in worker brood cells, acting as a natural control of the mite
population growth (Lin et al., 2018; Wang et al., 2020). While some similar host traits exist in
Western honey bees, they are far less pronounced and highly variable between subspecies
(Corrêa-Marques et al., 2002; Danka et al., 2011; Lin et al., 2016). Unrestricted access to
thousands of worker brood cells in colonies of Western honey bees provides the mite with many
more opportunities to reproduce, compared with Eastern honey bees. This contributes to an
exponential population growth rate of the mite in this new host.. During the mite’s reproductive
phase, it feeds on developing pupae and vectors detrimental honey bee viruses, in particular
Deformed wing virus (DWV), causing crippled, flightless adult honey bees with significantly
shortened life spans, ultimately resulting in the loss of colony function (de Miranda and
Genersch, 2010; Wilfert et al., 2016). To avoid viral infections killing the honey bee colony,
mite population control treatments are required in apiculture. The Varroa-virus complex has
caused a near complete eradication of wild honey bee colonies in Europe and North America
(Le Conte et al., 2010). However, there are small sub-populations that have survived extended
periods without Varroa mite control treatment and have documented resistant and tolerant host
phenotypes to both the Varroa mite and their viruses (Locke et al., 2012; Locke, 2016a; Oddie
et al., 2018).
Within populations of A. mellifera there is large natural variation in the mite’s
reproductive success, which is rarely 100% (Gregorc et al., 2016; Mondet et al., 2020). Mite
reproductive success is defined as the ability of a mother mite to produce a viable mated female
offspring before the bee emerges from its brood cell as an adult. Suppressed mite reproduction
(SMR), is a term first coined by Harbo and Harris (1999), referring to a hereditary phenotype
of a honey bee colony that causes Varroa mites to have a reduced reproductive success rate.
This phenotype will undoubtedly have a significant influence on mite population growth and
thus the development of virus infections and the life-span of the colony. It is also a trait of
economic importance as a selection criterion for honey bee mite-resistant breeding programs.
In naturally adapted mite-resistant honey bee populations, the mite’s reproductive success rate
has been recorded to be as low as 50% (Locke et al., 2012; Locke, 2016a; Oddie et al., 2018).
However, the underlying host mechanisms responsible for expression of the SMR phenotype
in any honey bee population, those in breeding programs or those that are naturally mite-
resistant, remain elusive. It has been proposed that SMR is related to adult honey bee hygienic
behaviors (Harbo and Harris, 2005; Harris, 2007). An example is Varroa Sensitive Hygiene
(VSH) behavior, where adult bees selectively remove brood parasitized with reproducing mites
while ignoring brood with non-reproductive mites. This behavior results in the appearance of a
higher rate of non-reproducing mites (Ibrahim and Spivak, 2006; Danka et al., 2011; Harris et
al., 2012). Another honey bee behviour that could relate to the SMR phenotype is uncapping
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and recapping of the wax cap placed over the brood cell by adult workers. This behavior could
potentially disrupt the timing of mite reproduction, or even physically displace or damage the
mites in the brood cell (Oddie et al., 2018, 2021). Another explanation for the SMR phenotype
is related to traits of the worker brood such as altered volatile expression patterns that could
inhibit mite reproduction (Locke et al., 2012; Frey et al., 2013). The mite uses volatile
compounds from the cuticle of the larvae and pupae, that vary during specific developmental
stages through pupation, as the signal to either initiate or inhibit the onset of egg laying (Frey
et al., 2013; Nazzi and Le Conte, 2016).
The aim of this study was to gain a better understanding of the honey bee host
mechanisms responsible for the SMR phenotype. This was approached by separating the adult
bee behaviors from brood traits and measuring the rate of Varroa mite reproductive success.
We examined three naturally adapted mite-resistant honey bee populations from Sweden,
Norway and France that express SMR (Locke and Fries 2011; Locke et al., 2012; Oddie et al.,
2017) and compared them with a local mite-susceptible population as a control group. The
origin and phenotypes of the three naturally surviving honey bee populations examined in this
study have been abundantly described (Locke, 2016a; Oddie et al., 2017). Briefly, these
populations have evolved independently without mite control since 1994 (Avignon, France; (Le
Conte et al., 2007)), 1999 (Gotland, Sweden; (Fries et al., 2003)) and 2001 (Oslo, Norway;
(Oddie et al., 2017)). Adult bees were restricted from sections of brood on the same hive frame
as brood that was exposed to adult bees. The hypothesis was that if mite reproductive success
was reduced in the worker brood that was excluded from adult bees, then brood traits would be
a significant contributor to the SMR expression in these populations, independent of the adult
worker behaviors. Specific reasons for failed mite reproduction were also examined to compare
and identify differences between the mite-resistant populations.
2. Materials and methods
2.1. Genetic background and colony establishment
During the summer of 2016, queens from each of these three populations were produced,
mated in their original geographic locations and transported to Sweden according to European
Union (EU) legislation guidelines. Queens from a local Swedish mite-susceptible honey bee
population were similarly produced and used as controls. All queens were established in
Swedish standard hives (Lågnormal, LP Biodling, Sweden) at a single apiary located at the
Swedish University of Agricultural Sciences, Uppsala, at the Lövsta research station (GPS
Coordinates: 59° 50’ 2.544”N, 17° 48’ 47.447”E). In the autumn of 2016, all colonies were
treated against Varroa mites using tai-fluvalinate (ApistanRegisted, Vita Europe, UK) to
equalize the mite infestation pressure.
2.2. Experimental design
The study was performed during August of 2017 with additional data collected in
August 2019. The experiemental mite-resistant colonies had their genetic origin in Norway (n
= 3), Sweden (n = 5) and France (n = 4), meaning the queens of these colonies were produced,
mated and transported from their country of origin. A control group of colonies was included
in the study with their origin being a Swedish mite-susceptible population (n = 5). The queens
from each colony were confined to a single frame of drawn-out wax using a queen-excluder
frame-cage in order to obtain frames with brood of uniform age. After 48 – 72 h, when the
frames were full of eggs, the queen excluder was removed. Then, frames were checked daily to
monitor the brood development and observe when the brood started to be capped. At ~8-9 days
after queen egg laying, when the majority of the larval brood cells had just been sealed for
5
pupation, a section covering an estimated 500 sealed brood cells was designated for the
exclusion treatment and isolated from contact with adult workers. Initially a metal cage was
pressed into the wax around the designated brood to exclude adult bee access (Fig. 1A). While
this metal cage generally served its purpose in excluding adult bees, it was inconsistant and
adult bees managed to dig through the wax to get inside the caged area in a few colonies, which
were then excluded from the analysis. Therefore, the brood exclusion method was adapted to
use a nylon covering stapled to the wooden frame (Fig. 1B). This method was more consistent
and effective at excluding adult bees from the brood. Approximately 500 worker brood cells on
the same frame were used as the adult honey bee exposure treatment group.
2.3. Frame dissection and mite reproduction evaluation
When the brood cells were ~9 days post capping, at which time mite reproductive
success is possible to assess, the frames were removed from the colonies for dissection. In order
to evaluate the mite reproductive success in individual brood cells, cell caps were removed
using a scalpel, and the pupa and mite families were carefully removed from the cell using
forceps and a fine paint brush according to standard methods (Dietemann et al., 2013; Table 1).
Individual cell content was analyzed using a stereoscopic microscope (Leica MZ75, 6.5X
magnification, Leica Microsystems, Germany). The pupal developmental stage, the number of
mite offspring and their developmental stage, were recorded and compared with each other to
evaluate mite reproductive success (Supplementary Table S1). A mite was considered to have
successfully reproduced if it had produced a male offspring and a viable female offspring that
would mature and mate with each other before the bee emerges from the brood cell as an adult
(Dietemann et al., 2013). If a mite failed to reproduce, the reason for failure (absence of a male,
delayed egg laying, dead progeny or infertility of the mother mite) was recorded
(Supplementary Table S1), together with mite fecundity (total number of offspring produced;
Dietemann et al., 2013). Brood cells were opened until a minimum of 30 infested cells were
uncovered, or until all available cells were opened.
2.4. Statistical analyses
Statistical analyses were performed using R version 4.0.1 R Development Core Team,
2010. A language and environment for statistical computing: reference index. R Foundation for
Statistical Computing, Vienna) and R Studio Version 1.3.959 (R Studio Team, 2020. RStudio:
Integrated Development for R). Data was shown to be normally distributed using a Shapiro
normality test. A linear mixed-effect model was performed with rate of mite reproductive
success as the response variable, population origin and excluder treatment as the independent
variables and colony and year as random effect variables. This was done to compare treatments
across populations, to compare treatments within each population, and to compare fecundity
using the packages “multcomp”, “lme4”, “nlme”, “car”, “lmertest”, “lsmeans”, and “dplyr”.
Least-square means of the model were used to compare treatments between individual
populations using the package “emmeans”. Interactions were included in the model and
sequentially removed when significance was not detected. P value threshold of 0.05 was used
to determine significance. All graphs were made using the package “ggplot2”.
2.5. Data accessibility
The datasets generated and/or analysed during the current study are available at the
Swedish National Data Service, https://doi.org/10.5878/znc2-9b12.
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3. Results
Mite reproductive success rates did not significantly differ between treatment groups of
either caged brood or brood exposed to adult bees and their possible removal behaviors,
irrespective of the population’s genetic background (2 = 2.45, degrees of freedom (df) = 1, P
> 0.11). The only variable that did influence Varroa mite reproductive success was the
population’s genetic background, irrespective of treatment (2 = 44.51, df =3, P < 0.005).
The average mite reproductive success rates were significantly lower in the French
(estimate = 0.326, df = 14, t.ratio = 3.89, P = 0.008) and Swedish ( estimate = 0.125, df = 14,
t.ratio = 0.0784, P < 0.005) mite-resistant populations compared with the mite-susceptible
control group (Fig. 2). The mite reproductive success in the Norwegian population was slightly
lower than in the mite-susceptible controls, but was not significantly different (estimate = 0.125,
df = 14, t.ratio = 1.35, P = 0.55; Fig. 2), while the average mite reproductive success rates were
not different between the French and Swedish colonies (estimate= 0.121, df = 14, t.ratio = 1.57,
P = 0.42; Fig. 2). Mite fecundity was also not affected by treatment (2 = 0.806, df = 1, P =
0.37), but was significantly affected by the colony background (2 = 31.11, df = 3, P < 0.001).
The mite fecundity in the French and Swedish populations were similar to each other (estimate
= 0.045, df = 14, t.ratio = 0.194, P = 0.997), but both were significantly different from the
controls (Control-Sweden: estimate = 1.05, df = 14, t.ratio = 4.52, P = 0.002; Control-France:
estimate = 1.01, df = 14, t.ratio = 4.00, P =0.006), while the mites in the Norwegian colonies
had similar fecundity rates to those in the control group (estimate = 0.38, df = 14, t. ratio – 1.41,
P = 0.52).
Failed mite reproductive success, either due to the absence of a male mite, delayed egg
laying, dead progeny or mite infertility was excluded from statistical analysis due to the small
and uneven sample size (Table 2). Delayed egg laying was the most common reason for failed
mite reproduction across all populations, while the absence of male mites occured more often
in the French and Swedish colonies than in the Norwegian and control colonies (Fig. 3).
4. Discussion
The mite reproductive success rates and mite reproductive fecundity in this study were
similarily low whether the parasitized brood was exposed to, or blocked off from, adult worker
bees. This clearly demonstrates that Varroa destructor mite reproductive success can be
suppressed by traits of the honey bee host brood, independent of adult worker behavioral traits.
With host-parasite relationships being particularly complex and intertwined, we do not
exlude the potential for an additive effect of adult bee behavior on the expression of the SMR
phenotype in any of these populations. However we believe these results eloquently reveal
significant information regarding adaptations of host resistance and the SMR phenotype, in
particular highlighting the role of host brood in Varroa-resistant honey bee populations.
The SMR phenotype has been widely considered to be an effect of the adult bee VSH
behaviour (Harbo and Harris, 1999). The results of this study suggest that either VSH is not
expressed to a significant degree in these colonies or that removal behaviors such as VSH do
not specifically target the reproducing mites. A recent study examined the link between VSH
and SMR, and found that the presence of mite offspring was not a crucial trigger for the VSH
behaviour (Sprau et al., 2021).
The evolution of novel behaviors such as VSH is a complex and difficult process, even
in the face of a strong natural selection such as high parasite load (Sokolowski, 2001). However,
7
many honey bee mite-resistant breeding programs focus on behaviors such as VSH, but have
had difficulty in producing sustainable mite resistance. Selecting for these behavioral traits is
laborious and their genetic basis is not entirely understood, with one study only able to explain
10% of variance in the trait (VSH) measured with two quantitative trait loci (Tsuruda et al.,
2012). Other studies looking at the genetic basis for VSH found different genes associated with
the trait, implying that this a multi-loci complex, most likely involving many genes of small
effect (Spötter et al., 2016; Scannapieco et al., 2017).
Frey et al. (2013) showed that the reproductive cycle of the mite is highly sensitive to
changes in the cuticular pheremonal compound profiles of the brood. Honey bees use a variety
of pheromonal compounds, functioning as complex releaser and primer signals, to regulate
social organization in the colony (Nazzi and Le Conte, 2016). Some of these compounds are
exploited by the mites, who use them to locate targets for feeding and reproduction. Fatty acid
esters (FAE) such as methyl palmitate, ethyl palmitate, and methyl linolenate, are pheromones
that signal adult nurse bees to cap the cells of developing bee larvae and have been shown to
also attract mites to the brood cells (Nazzi and Le Conte, 2016). Small changes in brood volatile
quantities or timing could therefore reduce the fitness of the parasites by interrupting their
reproduction cycle. This could potentially be a simpler adaptive strategy for honey bee
resistance as opposed to adult bee behaviors.
There have also been studies indiciating that brood developmental traits influence the
SMR phenotype. Two ecdysone-related genes (Cyp18a1 and Phantom) have been linked to
mite resistance in the Swedish naturally adapted honey bee population using whole-genome
sequencing for a quantitative trait locus analysis of reduced mite reproductive success (Conlon
et al., 2018). These genes regulate important enzymes for pre-pupal development and
metamorphosis by controlling steroid levels (Rewitz et al., 2010). Unusual concentrations of
steroid compounds during the pre-pupal phase could make the age of the pupae appear
suboptimal and the mother mite would suspend oogenesis (Frey et al., 2013; Conlon et al.,
2018). Additionally, the Ecdysone-regulating gene Mblk-1 has been linked with mite resistance
in another honey bee population from Toulous, France (Conlon et al., 2019) and is responsible
for both initiating metamorphosis in insects and initiating the reproduction in Varroa mites,
once they acquire it from their host during feeding (Ureña et al., 2014; Cabrera et al., 2015;
Mondet et al., 2018; Takayanagi-Kiya et al., 2017; Mondet et al., 2018).
Delayed egg laying was the most common reason for failed mite reproduction across all
populations in this study, similar to a pan-European study assessing mite reproduction (Mondet
et al., 2020). However, the absence of male mite offspring was significantly higher in the
Swedish and French populations, which also have on average higher overall mite reproductive
failure, compared with the Norwegian and control populations. The first egg laid by the mother
mite develops into the male offspring (Donzé and Guerin, 1994). Adaptations by the honey bee
brood that disrupt the oviposition or development of the male mite would need to occur early
during the mite reproductive phase. Future research could investigate if differences in the brood
pheromones that mites use to syncronize reproductive timing specifically influence
ovipositioning and timing in relation to the first male egg (Frey et al., 2013). Previous research
on the French and Swedish populations found that the most likely cause for failed reproductive
success was delayed egg laying for the Swedish population and infertility for the French
population (Locke et al., 2012). In this study there were no apparent differences between these
population in the reasons for reproductive failure. This could be due to the different
environmental conditions between this and earlier experiments, the minimal number of
examined brood cells or colonies, or changes in the population phenotypes since last
investigated. Recent studies have found that the Varroa mite has more genetic diversity than
previously thought and therefore is potentially capable of adapting through a host-parasite
evolutionary arms race. (Moro et al., 2020). Further research looking into how honeybees
8
interrupt Varroa mite reproduction would be beneficial in understanding the fluidity of this
system, and what type of selection both the mites and honey bees are undergoing.
The differences between the French and Swedish mite-resistant honey bee populations
and the mite-susceptible control population in this study mirror previous work and suggest the
heritability and fixed genetic nature of the SMR phenotype in these naturally adapted mite-
resistant populations (Locke et al., 2012; Locke, 2016b). The Norwegian honey bee population
mite reproductive success rates were not significantly different from the mite-susceptible
control population, in contrast with the French and Swedish populations which were
significantly different from the control.
This contrasts previous work on the Norwegian population showing more dramatic
differences in SMR between them and susceptible populations, when examined in Norway
(Oddie et al., 2017). This could suggest that either Norwegian honey bees express mite-resistant
phenotypes better in their local environment which they have adapted to, that they are
specifically adapted for Norwegian mites that genetically differ from the mites they were
exposed to in this study (Moro et al., 2020), or there has been a loss of the genetic heritability
of the SMR phenotype in this population. Local adaptation has been shown to be important for
colony survival when exposed to Varroa mite infections (Büchler et al., 2014; Meixner et al.,
2015). Additionally, gene versus environment interaction studies have shown that mite-resistant
populations do not necessarily maintain their resistant traits when moved to a new environment
(Büchler et al., 2014; Meixner et al., 2015; Kovačić et al., 2020). This could mean that the
Norwegian population has some factor that increases their SMR in Norway that is not present
in Sweden. Further, while previous studies found that the mites showed little to no adaptation
since their transition from A. cerana to A. mellifera (Kraus and Hunt, 1995; Solignac et al.,
2005), a recent study has shown that it is possible for mite populations to change their
reproductive strategies in resistant populations (Moro et al., 2021). They investigated an
isolated artificially selected Dutch honey bee population that once displayed VSH (Panziera et
al., 2017), but now shows no signs of VSH 4 years later. Genetic variation in mite genotypes
exist in mite-resistant honey bee populations (Beaurepaire et al., 2019; Moro et al., 2020) which
could potentially influence their reproductive success. However, this variation does not explain
the differences in the SMR phenotype between the colonies examined in this study, since all
the test colonies were managed in the same apiary, originally established from the same local
bees and mites, where drifting of mites between colonies is expected (Frey and Rosenkranz,
2014; Nolan and Delaplane, 2017).
This study clearly distinguishes that adult bee behaviors are not involved in the
expression of the SMR phenotype in these naturally adapted mite-resistant honey bee
populations. Although we hypothesise that the reduced reproduction of mites is influenced by
brood factors in these populations, there could still be factors that we have not examined, such
as hive environment, that could be influencing mite reproduction. Brood transfer experiments
could be used to identify such environmental effects and further studies testing the hypothesis
that brood traits alone regulate the SMR phenotype are ongoing.
The distinction made in this study is an important first known step towards
understanding the mechanisms behind SMR and more generally mite resistance, and opens the
door for future research to discover more precisely what specific brood features are important
for the SMR phenotype. A deeper understanding of the ecological interactions between Varroa
mites and their hosts are also important for efforts in developing mite-resistant breeding
programs. This could potentially simplify selection criteria evaluation methods, selection
strategies, and help develop more efficient and sustainable efforts towards long-term genetic
stock improvements for mite resistance in honey bees.
Acknowledgments
9
The authors would like to thank Naomi Keehnen and Claudia von Brömssen for
statistical input. Funding was provided by the European Research Council (ERC Starting Grant,
action number: 949223) and the Swedish Research Council (FORMAS, dnr. 2016-00481) to
BL. Funding to establish the colonies from different geographical regions was provided by the
Ricola Foundation Nature and Culture, [Switzerland] to PN.
10
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15
Legend to Figures
Fig. 1. Photographs of the two types of experimental frames used to exclude approximately 500
sealed worker brood cells from adult bees (Apis mellifera). (A) Wire mesh cage; (B) nylon mesh
cage. The frame size used is called Swedish Lågnormal, with dimensions 222 mm height x 366
mm width.
Fig. 2. The average rates of Varroa destructor mite reproductive success (means +/- SE)
examined in four honey bee (Apis mellifera) populations (n indicates number of colonies) with
error bars indicating standar error. Bars represent the three mite-resistant populations examined
from: Sweden (n = 6), France (n = 5), and Norway (n = 3), and the mite-suspectable control
group (n = 4). Within each population, treatment groups were differentiated between caged
brood excluded from adult bees (light color) and brood exposed to adult bees (dark color).
Fig. 3. Average rate of reasons for the failed Varroa destructor reproductive success in the three
naturally adapted honey bee (Apis mellifera) populations and control group, exposed and
exluded groups pooled. The recorded reasons are: i) absence of a male; ii) delayed egg laying
as mite offspring were too young to successfully reproduce; and iii) infertility of the foundress.
Highlights
Varroa reproductive success was reduced in three mite-resistant honey bee
populations
Host brood traits reduce mite reproduction, independent of adult bees
The added presence of adult bees did not increase the rate of reduced mite
reproduction
Fundamental understanding of the host brood–parasite relationship is required for
future work
Table 1. Number of examined honey bee (Apis mellifera) worker brood cells, how many were opened, examined,
naturally infested by mites (Varroa destructor), and how many had mites that reproduced successfully.
GENETIC BACKGROUND
MEASUREMENT
EXPOSED BROOD
CAGED BROOD
opened cells
772
937
infested cells
89
73
NORWAY
reproductive mites
70
58
opened cells
1965
1135
infested cells
81
76
FRANCE
reproductive mites
46
39
opened cells
1204
796
infested cells
161
133
SWEDEN
reproductive mites
76
59
opened cells
536
797
infested cells
120
94
CONTROL
reproductive mites
115
83
16
Table 2. The total number of mites (Varroa destructor) with failed reproduction presented for each population
together with the number of failed reproductions due to the specific reasons observed and recorded.
Background
Total failed
reproduction
Infertile
mother
Delayed egg
laying
Absence of
male
Dead
progeny
Sweden
160
43
59
56
2
France
72
19
33
20
0
Norway
34
10
21
3
0
Control
16
6
8
2
0
17
18
19
