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Natural Varroa mite-surviving Apis mellifera honeybee populations


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The Varroa destructor mite is the largest threat to apiculture worldwide and has been responsible for devastating losses of wild honeybee populations in Europe and North America. However, Varroa mite-resistant populations of A. mellifera honeybees have been reported and documented around the world with a variety of explanations for their long-term survival with uncontrolled mite infestation. This review synthesizes the work on naturally occurring survival to Varroa mites and discusses what these honeybee populations can signify for apiculture.
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Natural Varr oa mite-surviving Apis mellifera
honeybee populations
Barbara LOCKE
Department of Ecology, Swedish University of Agricultural Sciences, PO Box 7044, 750 07, Uppsala, Sweden
Received 18 April 2015 Revised 28 September 2015 Accepted 6 November 2015
Abstract The Varroa destructor mite is the largest threat to apiculture worldwide and has been responsible for
devastating losses of wild honeybee populations in Europe and North America. However, Varroa mite-resistant
populations of A. mellifera honeybees have been reported and documented around the world with a variety of
explanations for their long-term survival with uncontrolled mite infestation. This review synthesizes the work on
naturally occurring survival to Varroa mites and discusses what these honeybee populations can signify for
Varroa destructor / mite resistance / host-parasite adaptations / natural selection / apiculture
The European honeybee, Apis mellifera ,isthe
only Apis species that does not have a natural
parasitic brood mite but is nevertheless highly
susceptible to at least two mites that are native to
other honeybee species (Varroa destructor and
Tropilaelaps clareae ; Oldroyd 1999). The ecto-
parasitic mite, Varroa destructor , is of particular
importance as it is currently considered the largest
threat to apiculture worldwide and inflicts more
damage and higher economic costs than all other
known apicultural diseases (Boecking and
Genersch 2008).
The Varro a mites natural host is the Asian
hive bee, Apis cerana . Damage to Asian honey-
bee colonies is rarely experienced since a stable
host-parasite relationship has been established
over a long evolutionary scale (Rath 1999). Such
a relationship is distinguishably missing with the
European honeybee. In Asian hive bee colonies,
the mites reproduction is restricted to drone brood
(Boot et al.1999). and when mites try to enter
worker brood cells, the infested pupa along with
the mites are removed by the hygienic behavior of
adult bees (Peng et al.1987). Also, adult bees
with grooming behavior capture and kill the
phoretic mites in the colony (Peng et al.1987).
European honeybees have behavioral defenses
similar to the Asian hive bee such as grooming
and hygienic behavior but they are typically less
pronounced (Fries et al. 1996) and variable be-
tween A. mellifera races (Moretto 2002; Moretto
et al. 1991a). The specific removal of mite-infested
brood has been termed Varroa -sensitive hygienic
(VSH) behavior (Harris 2007; Ibrahim and Spivak
2006; Spivak 1996). Both hygienic behavior and
VSH behavior remove dead or diseased brood, as
well as mite-infested brood, but the later is more
effective toward mite infestation (Boecking and
Spivak 1999; Ibrahim and Spivak 2006; Danka
et al.2013). The distinction between VSH behav-
ior and regular hygienic behavior may be in the
detection stimulus of the adult bees which for VSH
seems to be indirect effects of mite infestation such
as pupal virus levels or faults in pupal develop-
ment (Mondet 2014). Differentiating between
Corresponding author: B. Locke,
Manuscript editor: Yves Le Conte
Apidologie Review article
*INRA, DIB and Springer-Verlag France, 2015.
This article is published with open access at
DOI: 10.1007/s13592-015-0412-8
these behaviors in a colony is difficult and depends
on how the behavior is measured. This review
distinguishes these behaviors based on the testing
methods in the original work. Whether the mite
removal is due to general hygienic behavior or
VSH behavior, most mites are not killed and in-
stead escape during the removal process.
Nevertheless, this results in an interruption of the
mites reproductive cycle, which can slow
down the mite population growth (Boecking and
Spivak 1999).
Since the Varro a mite made the host switch to
the European honeybee, it has successfully spread
throughout the world, and today, only Australia and
a few isolated locations and islands are considered
mite-free (Rosenkranz et al.2010). In Europe and
North America, the Varro a mite has caused devas-
tating losses of wild A. mellifera honeybee popula-
tions in these regions (Le Conte et al. 2010;
Neumann and Carreck 2010). The Varro a
destructor species includes several mitochondrial
haplotypes, but only two are able to reproduce in A.
mellifera colonies: the Korean haplotype that has a
worldwide distribution and the Japanese haplotype
that has only been reported in Japan, Thailand, and
North and South America and is considered less
virulent than the Korean type (Anderson and
Trueman 2000; de Guzman and Rinderer 1999).
The big difference between the Asian and
European bee species is that the mite is able to
reproduce in worker brood cells of A. mellifera
honeybees (Boot et al.1999). This results in an
exponential mite population growth (Fries et al.
1994) that can lead to colony death typically with-
in a few years if mite population control is not
practiced by beekeepers (Boecking and Genersch
2008). While feeding on bee hemolymph, the mite
damages the developing worker pupae (De Jong et
al.1982; Schneider and Drescher 1987;Kraljet
al.2007) and is associated to several lethal hon-
eybee viruses (Bailey and Ball 1991; Ball and
Allen 1988). Deformed wing virus (DWV) is the
most prevalent honeybee virus worldwide due to
Varro a -mediated transmission and replication (de
Miranda and Genersch 2010; Sumpter and Martin
Despite this grave situation, survival of the
mite is documented in A. mellifera honeybees,
most notably in the African race, Apis mellifera
scutellata , in Brazil (Rosenkranz 1999)andmore
recently in Africa (Allsopp 2006). Even small
subpopulations of European races have been well
documented as surviving with uncontrolled
Varroa mite infestation for a decade or longer
(De Jong and Soares 1997; Fries et al.2006;
Le Conte et al.2007;Rindereretal.2001;
Seeley 2007). These populations of A. mellifera
honeybees surviving Varroa mites may reveal
genetic and ecological factors that enable mite
resistance including important mite-resistant traits
that could be adopted in breeding programs. This
review synthesizes the documentation of Va r ro a
mite-surviving populations and discusses what
their long-term survival with Va r ro a can signify
for apiculture.
2.1. A. m. scutellata in Brazil and South
The Varro a mite was first reported in Africanized
honeybees in Brazil in the early 1970s (Goncalves
and De Jong 1981). Originally, the Japanese haplo-
type was described but is now replaced by the
Korean haplotype on most of the continent (de
Guzman and Rinderer 1999; Anderson and
Trueman 2000; Rosenkranz et al.2010). Initially,
the presence of the mite in Brazil was thought to
pose a serious threat, since high infestation rates
were recorded (Morse and Goncalves 1979).
However, a subsequent reduction in mite infestation
was observed that suggested an adaptive process by
the host in the population (Moretto et al.1995).
Africanizedbeesdonotrequire mite control and
maintain lower mite infestation rates (34mites/
100 bees) than any other A. mellifera race
(Rosenkranz 1999; Moretto et al.1995).
Hygienic and grooming behavior are important
mite-resistant host traits of Africanized bees in
Brazil (Correa-Marques and De Jong 1998;
Moretto 2002; Moretto et al.1993)andin
Mexico (Guzman-Novoa et al.1999; Mondragon
et al.2005). Lower brood attractivity for reproduc-
ing mites has been reported in Africanized honey-
bees (Guzman-Novoa et al.1999), but the trait
could not be attributed to larval volatiles since
B. Locke
differences in volatiles with that of European races
were not found (Aumeier et al.2002).
Mite fertility has been observed as low as 50 %
in Africanized honeybees in Brazil (Rosenkranz
and Engels 1994;Rosenkranz1999) but has in-
creased over the years to >80 %, probably due to
the replacement of the less virulent Japanese mite
haplotype by the more virulent Korean mite hap-
lotype (de Guzman and Rinderer 1999;Garrido
et al.2003). Carneiro et al.2007 reported an
increase of mite fertility in Brazil from 56 % in
the 1980s to 86 % in 20052006. Mite haplotype
virulence could also explain the higher mite fer-
tility rates found in Africanized honeybees in
Mexico since only the Korean haplotype has been
found there (Medina and Martin 1999;
Mondragon et al.2005;deGuzmanand
Rinderer, 1999;deGuzmanetal.1999).
Despite an increase in mite fertility or the
presence of the Korean mite haplotype, the
Africanized honeybee population remains sta-
ble in Brazil and there have been no reports of
increased mite infestation rates (Carneiro et al.
2007; Garrido et al.2003; Vandame and
Palacio 2010). This suggests that mite resis-
tance in this population is (a) based on host
factors rather than parasitic virulence and (b)
probably owing to a combination of traits ad-
ditively reducing the mite population growth
rather than a single trait alone, such as reduced
mite fertility.
Since the mite was introduced to South Africa
in 1997, South African bee races (A. m. scutellata
and A. m. capensis ) have been effectively mite
resistant and mite control is not required (Allsopp
2006). By contrast to Brazil, only the Korean mite
haplotype has been reported in this region
(Anderson and Trueman 2000). When the mite
was found in South Africa, mites reproduced as
successfully in A. m. scutellata brood as they did
in European races and it was suspected that api-
culture in Africa would experience a similar neg-
ative impact from the presence of mites (Martin
and Kryger 2002). Some colony losses were re-
ported just after the mite was introduced, but the
situation is now stable, which could suggest that
an adaptive response by the host has occurred in
response to mite infestation (Allsopp 2006). Even
though Var r o a mites are extremely common in
South Africa, infestation rates never exceed 4
mites/100 bees (Strauss et al.2013).
The Varro a mite has since been found in
Eastern Africa in early 2009, including Kenya,
Tanzania, and Uganda with even a few observa-
tions in Ghana suggesting a now westward spread
of the mite across Africa (Frazier et al.2010).
Beekeepers in these countries were not even
aware of the presence of the mite nor have they
experienced any negative impact on colony sur-
vival or productivity (Frazier et al.2010).
Previously, A. m. intermissa honeybees in
Tunisia have been described as mite-resistant with
increased grooming and hygienic behavior
(Boecking and Ritter 1993). Kefuss et al.(2004)
imported A. m. intermissa queens to France and
have observed reduced mite infestations in their
The Africanized bees of Brazil are genetically
identical to their ancestral African race, A. m.
scutellata , due to genotypic qualities thatoutcom-
pete the European race (Schneider et al.2004).
Therefore, the mite resistance of A. m. scutellata
honeybees in both Brazil and Africa could be
explained by shared pre-existing genetic elements
of parasitic resistance. Besides active defensive
behaviors, additional characteristics of the A. m.
scutellata race that may in combination support
low mite population growth include higher rates
of absconding, migratory swarming, faster colony
development, and generally smaller colonies
(Fletcher 1978;MoritzandJordan1992;
Schneider et al.2004). Further, a reduced bee
developmental time (Buchler and Drescher
1990; Moritz and Jordan 1992; Rosenkranz and
Engels 1994) and reduced comb cell size
(Message and Goncalves 1995;Medinaand
Martin 1999; Piccirillo and De Jong 2004)can
reduce the ability of mother mites to produce
viable mated female offspring before the adult
bee emerges from the cell. However, Seeley and
Griffin (2011) have clearly demonstrated that
small comb cell size did not reduce Varroa mite
infestations for European races of A. mellifera .
Climate has also been suggested to play a role in
reduced mite infestation (Moretto et al.1991b).
Although it is more likely that climate indi-
rectly affects mite population growth by reg-
ulating honeybee brood amounts or
Natural Va rro a mite-surviving Apis mellifera honeybee populations
influencing the activeness of bee defense be-
haviors (Rosenkranz et al.2010).
Virus infections have been detected at low
levels in South African bees but do not seem to
affect the health status of these colonies, and
DWV was notably absent (Strauss et al.2013).
DWV has been reported in Brazil along with other
viruses (Freiberg et al.2012; Teixeira et al. 2008).
but negative effects of virus infections are not
experienced there either (Neumann and Carreck
2.2. Island of Fernando de Noronha
In 1984, an isolated population of Italian hon-
eybees (A. m. ligustica ) was established on the
Island of Fernando de Noronha off the coast off
Brazil (De Jong and Soares 1997). This popula-
tion was initiated to provide plant pollinators,
enable Islanders to be self-sufficient in honey
production, and to offer mainland beekeepers a
nearby isolated breeding population of a
European honeybee race with a gentler tempera-
ment than the Africanized honeybees (De Jong
and Soares 1997). Queens from Italy were intro-
duced to queenless Brazilian colonies from the
mainland, which were infested with Va r r oa mites.
The honeybee population on the island grew in
numbers; mite control was not required for over
12 years; and the colonies were gentle, large, and
productive (De Jong and Soares 1997). Mite in-
festation rates were higher on the island than
reported in mainland Africanized bees but
dropped in the population between 1991 and
1996 from 26 to 14 mites/100 bees, and host
adaptations of mite resistance were suspected
(De Jong and Soares 1997).
Mite fertility on the island was high (>80 %; De
Jong and Soares 1997) in contrast to Africanized
bees on the mainland at the time (around 50 %;
Rosenkranz and Engels 1994). Hygienic behavior
in Fernando de Noronha colonies was similar to
other European races and almost 50 % lower than
Africanized bee colonies (Guerra et al.2000).
Correa-Marques et al.(2002) brought queens
from Fernando de Noronha to Germany to make
pairwise comparisons with local mite-susceptible
honeybees (A. m. carnica ), but no differences in
mite infestation rates were found. Moreover,
grooming behavior was significantly lower in the
colonies headed by Fernando de Noronha queens
(Correa-Marques et al.2002). Whatever was en-
abling the bees of Fernando de Noronha to main-
tain a low mite infestation was not effective in
Germany. This suggested that their ability to sur-
vive is due to something other than genetic host-
resistant mechanisms (Correa-Marques et al.
Mitochondrial DNA analysis demonstrated
that all the colonies sampled in 1996 were still
100 % of the A. m. ligustica race without hybrid-
izing with Africanized bees (De Jong and Soares
1997). It was also reported by Correa-Marques
et al. (2002) that there were 100 Italian honeybee
colonies on the island, with half of them in man-
aged hives and the other half living wild in
hollowed tree cavities.
Importantly, the Island of Fernando de
Noronha is still parasitized by the original
Japanese mite haplotype that was introduced from
mainland Brazil when the islands honeybee pop-
ulation was first established (Strapazzon et al.
2009). The presence of the less virulent Japanese
mite haplotype on the island could explain how
this honeybee population manages to survive with
uncontrolled Varroa mite infestation. The isola-
tion of this population may have additionally
prevented the introduction of honeybee viruses,
which would contribute tothe overallhealth status
and survival of the population. More studies on
this population are required to better understand
their survival with Va r r o a andtodetermine
whether it is a result of bee adaptations, mite
virulence or a combination of both.
2.3. Primorsky, Russia
The longest known association of A. mellifera
honeybees and Va r ro a mites is from far eastern
Russia (Primorsky), where from the mid-1800s
contact between the A. cerana population edge
and introduced A. mellifera colonies lead to the
Varro a mites host switch (Danka et al.1995).
Initial examinations of these European bee
colonies suggested that they might be mite-
resistant through natural selection due to a
long association with the mite (Danka et al.
1995). Honeybee stock from this region was
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imported to the USA for evaluating mite re-
sistance (Rinderer et al.2001).
Pairwise investigations with local mite-
susceptible honeybees in the USA demonstrated
that Russian honeybees had a slower mite popu-
lation growth (Rinderer et al.2001). increased
hygienic behavior (de Guzman et al.2002)and
grooming behavior (Rinderer et al.2001). had
less attractive brood for Va r roa mite infestation
(Rinderer et al. 2001). and had reduced mite re-
productive success including high infertility rates
of around 50 % (de Guzman et al. 2008). A large
mite-resistant breeding program has been
established in the USA based on this Russian
honeybee population, and queens are available
commercially (re viewed by Rinderer et al.2010).
2.4. Gotland, Sweden
At the end of the 1990s, an isolated population
of 150 honeybee colonies was established on the
southern tip of Gotland, an island in the Baltic Sea
off the eastern coast of Sweden. The colonies
came from a variety of locations around Sweden
and included a diversity of honeybee races (Fries
et al.2003). The experimental purpose was to
evaluate if Varro a mites would eradicate the
population under Nordic conditions without
mite control treatments. The colonies were
artificially infested with equal amounts of
Varro a mites, were unmanaged, and free to
swarm (Fries et al. 2003).
The population was continuously monitored
for swarming, winter losses, autumn mite infesta-
tion rates, and colony size in the spring. Within the
first 3 years, more than 80 % of the colonies died
due to the rapid buildup of mite infestations (Fries
et al.2003). Many colonies swarmed during the
first 2 years, but by the third year, swarming
decreased since colonies were too weak (Fries
et al.2003). After the initial losses, the autumn
mite infestation rates decreased, winter mortal-
ity decreased, and the incidence of swarming
increased again as colonies recovered (Fries
et al. 2006).
A cross-infection experiment with mite-
susceptible bees showed that the Gotland mite-
resistant colonies had an 82 % lower mite popu-
lation growth rate irrespective of the mite source
(Fries and Bommarco 2007). This study clearly
demonstrated that the long-term survival of the
Gotland honeybees with uncontrolled mite infes-
tation was due to host traits rather than reduced
mite virulence and suggested that host adaptations
had occurred through natural selection in the pop-
ulation (Fries and Bommarco 2007).
The mite-resistant colonies on Gotland are
small compared to mite-susceptible colonies in
the same environment (Locke and Fries 2011).
They have fewer adult bees through the summer,
about half the amount of worker brood and one
tenth the amount of drone brood (Locke and Fries
2011). Reduced colony size and brood amounts
may be an adaptive strategy to limit mite repro-
ductive opportunities and slow the mite popula-
tion growth, especially considering the attractive-
ness of drone brood for mite reproduction (Boot
et al.1993,1994;Calisetal.1999;Fuchs1990;
Fries et al.1994). The incidence of swarming
typically causes a loss of 4070 % of the adult
worker bee population along with many of the
phoretic mites followed by a broodless period
when mite reproduction is restrained (Wilde
et al.2005). Although swarming in the Gotland
population did initially reduced mite infestations
in mother colonies, it could not prevent the devel-
opment of high mite levels in the autumn (Fries
et al.2003). Differences in brood attractivity,
hygienic behavior, and grooming behavior were
not apparent between the Gotland colonies and
local mite-susceptible colonies (Locke and Fries
2011). suggesting that these traits were probably
not as important for the Gotland populations re-
sistance as they are for Africanized honeybees.
Only about 50 % of the mites in Gotland col-
onies successfully produce viable mated daughter
mites that contribute to the colonys mite popula-
tion, compared to about 80 % in local mite-
susceptible colonies (Locke and Fries 2011).
Delayed egg-laying by mother mites and dead
mite offspring were reported as the most common
causes of failure to reproduce successfully (Locke
and Fries 2011). A potential explanation for the
reduced reproductive success in the Gotland pop-
ulation could be altered brood volatiles that are
responsible for initiating oogenesis in mites
(Garrido and Rosenkranz 2004; Nazzi and
Milani 1996; Trouiller and Milani 1999;Frey
Natural Va rro a mite-surviving Apis mellifera honeybee populations
et al.2013). The higher proportion of dead mite
offspring observed in the Gotland colonies may be
an additional consequence of delayed egg-laying
since soft-bodied immature mites are vulnerable
to damage when exposed to older bee pupae that
are molting or have increased movement in the
cell (Calderon et al.2012; Martin 1994). A re-
duced post-capping period, which influences mite
reproductive success by limiting mite offspring
developmental time, was not observed in this
population (Locke and Fries, unpublished data ).
The inheritance of the reduced mite reproduc-
tive success in the Gotland population was inves-
tigated by examining the trait in daughter colonies
established through artificial inseminations of
mite-resistant and mite-susceptible bees along
with their reciprocal crosses. Reduced mite repro-
ductive success was expressed almost equally in
all colonies with a genetic origin from the Gotland
mite-resistant honeybees regardless if the genetic
contribution was maternal, paternal, or both
(Locke 2015). These results demonstrated that this
trait has a strong genetic component to its inheri-
tance in the Gotland mite-resistant honeybee pop-
ulation (Locke 2015).
Behrens et al.(2011) screened the genome of
haploid drones with and without reproducing
mites to identify quantitative trait loci (QTLs)
possibly involved in the inhibition of mite repro-
duction. The drones in their study were reared by
hybrid daughters of queens from the Gotland pop-
ulation (Behrens et al.2011). Their analysis found
target regions on three chromosomes with QTL
that seemed to interfere with mite reproduction
(Behrens et al.2011). In a follow-up study,
Lattorff et al.(2015) scanned these QTL regions
in samples of bees from the Gotland population
before (in 2000) and after natural selection had
occurred (in 2007). They found a strong overall
loss of heterozygosity in these regions, suggesting
that genetic drift, selection, or both had occurred in
the population. On two loci on chromosome 7, the
reduction was greater than what could be expected
from genetic drift alone (Lattorff et al.2015).
suggesting that this small genomic region experi-
enced strong selection (Lattorff et al.2015). A
promising candidate gene identified in this geno-
mic region of the honeybee that may be significant
in affecting the mites reproduction was a glucose-
methanol-choline oxidoreductase (GMCOX18).
Oxidoreductase genes have been reported to be
involved in diverse functions for A. mellifera in-
cluding cuticle biosynthesis (Kunieda et al.2006)
and are involved in larval chemical defenses in
other insects, such as leaf beetles, by displaying a
glandular secretion that repels enemies
(Chrysomelidae ; Michalski et al.2008;Rahfeld
et al.2014). This candidate gene could be in-
volved in altered brood volatiles that influence
mite oogenesis, which would support earlier hy-
potheses for the mechanisms behind the reduced
mite reproductive success in the population.
Autumn mite infestation rates can be high in the
Gotland population (Locke et al.2014) relative to
the winter mortality threshold for the region (>0.3
mites/bee; Fries et al. 2003). yet the mite popula-
tion growth is slower than in mite-susceptible col-
onies and the Gotland colonies are able to survive
the winters. By contrast, local mite susceptible
colonies all perished with drastically high mite
infestation only after one season without mite con-
trol treatment (>1 mite/bee; Locke et al.2014).
Even though they survive, Gotland colonies often
have DWV symptomatic adult bees with deformed
wings and can have high DWV infections similar
to mite-susceptible colonies (Locke et al.2014).
This could suggest that the population has also
acquired a colony-level tolerance to DWV in ad-
dition to their adapted resistance to the mite as they
manage to survive with high DWV infections
when mite-susceptible colonies perish. Black
queen cell virus (BQCV) and sac brood virus
(SBV) infections both decreased dramatically by
the autumn in the Gotland mite-resistant colonies
butincreasedinmite-susceptible colonies
(Locke et al.2014). Although BQCV and SBV
are seldom responsible for colony death, they
are both virulent brood diseases that can have
quite damaging effects on colony functioning
and overall health (Ribière et al.2008;
Bailey and Ball 1991; Bailey and Fernando
1972; Anderson and Giacon 1992). A reduc-
tion of these viruses in the autumn could sup-
port better general health of overwintering
adult bees that are responsible for colony
growth in the spring.
The Gotland population today consists of 20
30 colonies. Current projects on this population
B. Locke
involve identifying changes in brood volatiles
and gene expression that play a role in mite
reproductive success, as well as investigating
through genomic screening any microbial dif-
ferences in this population that may support
its overall colony longevity. Although the
Gotland bees are relatively non-aggressive,
the colonies are small and therefore do not
produce much honey yield. Introducing these
honeybees into a breeding program that can
maintain Varro a resistance but enhance com-
mercially desirable traits is of interest.
2.5. Avignon, France
Throughout the 1990s, honeybee colonies that
were wild or from abandoned apiaries and had not
been treated for Varroa for at least 3 years were
being collected in two locations in South and west-
ern France, Avignon and Le Mans, respectively
(Le Conte et al. 2007). Additional colonies were
collected based on beekeeper responses to a survey
and had not been treated against mites for at least
2 years (Le Conte et al. 2007). By the end of the
decade, a total of 52 colonies were in Avignon and
30 in Le Mans (Le Conte et al. 2007). Swarming in
these colonies was not prevented, mite control was
not used, and management was limited to honey
collection (Le Conte et al.2007).
For over 7 years (19992005), there were no
significant differences in annual colony mortality
between the untreated colonies and treated mite-
susceptible colonies nearby. Mite infestation rates
however remained three times lower in the un-
treated colonies, suggesting that they were able in
some way to inhibit the mites population growth
(Le Conte et al. 2007). The mite-susceptible col-
onies produced almost twice the amount of honey
compared to the mite-resistant colonies, and no
major differences in swarming tendency were ob-
served (Le Conte et al.2007).
Navajas et al.(2008) compared gene expression
in honeybees of the Avignon mite-resistant popu-
lation and local mite-susceptible honeybees. Their
study interestingly found that several genes in-
volved in olfactory cognition and neuronal excit-
ability were upregulated in the mite-resistant hon-
eybees (Navajas et al.2008). The Avignon mite-
resistant honeybees could have a higher
sensitivity to environmental stimuli and be better
adapted for detecting and removing mite-infested
brood cells (Navajas et al.2008). It is not clear how
bees are able to recognize the mite in brood cells
but it may be by an unspecified stress reaction of
the pupae (Aumeier and Rosenkranz 2001).
Hygienic behavior or even specifically VSH be-
havior could explain the mite resistance in this
population, since it has been shown that generally
hygienic honeybees have higher olfactory sensitiv-
ity and responsiveness compared to non-hygienic
bees (Gramacho and Spivak 2003; Masterman
et al.2001). Early work on the initial colonies of
the Avignon mite-surviving honeybee population
demonstrated that they had a better antennal re-
sponse to identified Varro a mite compounds with
a greater sensitivity and capacity for detection of
mites compared to heavily mite-infested honeybee
colonies (Martin et al.2001).
Mite reproductive success in the Avignon mite-
resistant population was reduced by 30 % com-
pared to local mite-susceptible colonies, a similar
trend to the mite-resistant population on Gotland
(Locke et al.2012b). However, the Avignon pop-
ulation had a significantly higher percentage of
infertile mites than what was observed in the
Gotland population (Locke et al.2012b). when
mother mites reproduce their offspring collective-
ly feed on the developing bee pupa inducing more
damage and a stronger stress stimulus than pupae
with non-reproducing mites. Harbo and Harris
(2005) have suggested that VSH bees removed
reproducing mites more often than non-
reproducing mites, which resulted in the appear-
ance of a high infertility rate. If adult bees of the
Avignon mite-resistant population have VSH be-
havior, they may be selectively removing repro-
ducing mites and the high mite infertility rates
observed may be an indicator of this behavior.
Uncapped pupae, a typical characteristic of VSH
behavior, have been observed in the Avignon pop-
ulation (Le Conte, personal communications ).
Quantifying hygienic and VSH behaviors in this
population is a current research goal.
Today, the Avignon mite-resistant population is
not isolated but has maintained mite-resistant
characteristics. The colonies however can be ag-
gressive and typically do not produce much honey.
In a recent Europe-wide genotype-environment
Natural Va rro a mite-surviving Apis mellifera honeybee populations
interaction, experiment descendant colonies from
the Avignon mite-resistant population did not
demonstrate better or worse survival in different
environments compared to unselected local colo-
nies (Meixner et al. 2015). This could suggest an
environmental influence in the populations mite
resistance in Avignon but needs further study,
which could also be applied to other mite-resistant
honeybee populations. In Le Mans, western
France, colonies still survive without Varr o a con-
trol and may have adapted different mechanisms
for survival worth investigating.
2.6. Arnot Forest, Ithaca, NY, USA
The Arnot Forest is a large research reserve south
of Ithaca, NY, and is owned by Cornell University.
The honeybee population in this forest is unique to
other mite-resistant populations reviewed herein
that it is entirely composed of wild colonies nesting
in hollowed tree cavities rather than movable frame
hives. The first census of this population was carried
out in 1978 when 18 colonies were located, approx-
imately 10 years before the mite was reported in
New York State (Visscher and Seeley 1982). The
census was repeated in 2002 and confirmed the
continual survival of the population with an esti-
mated 16 colonies, 15 years after the arrival of
Varro a mites to the region (Seeley 2007).
Bait hives were set out in the Arnot Forest in
early spring 2003 to collect swarms into movable
frame hives so mite infestation could be investi-
gated (Seeley 2007). The bait hives were kept in
the forest, and mite infestations were recorded
monthly until the colonies were lost to black bear
attacks the following winter of 20042005
(Seeley 2007). Continued inspection of the colo-
nies living in tree cavities showed that the popu-
lation as a whole remained stable over 3 years
despite mite infestation (Seeley 2007). A pairwise
comparison of colonies established by Arnot
Forest queens from the bait hives and colonies of
unrelated mite-susceptible bees did not reveal dif-
ferences in mite infestation growth (Seeley 2007).
It was therefore suggested that the Arnot Forest
honeybees are not better at limiting the mite pop-
ulation growth and perhaps have no adapted
mechanisms to do so (Seeley 2007). The survival
of the population was rather suggested to be due to
avirulent mites either by the presence of the less
virulent Japanese mite haplotype, reported spo-
radically through North America (de Guzman
et al.1999). or by adaptations of the mite
(Seeley 2007). Colony level adapted tolerance to
mite infestation could be an additional explana-
tion for the survival of this population with a
similar mite population growth rate as mite-
susceptible colonies.
The small nest cavities in the forest result in
generally smaller colonies causing limited brood
production that may consequently slow the mite
population growth. Small nest cavities can also
cause an increased rate of swarming (Seeley and
Morse 1976) and provide more vertical transmission
opportunities for the mite that would promote avir-
ulent adaptations (Fries and Camazine 2001).
Moreover, horizontal transmission pathways that
select for more virulent mites (Fries and Camazine
2001) are reduced in this population since the colo-
nies are so widely dispersed (Seeley et al.2015).
Genetic structure analysis revealed that the
Arnot Forest honeybees are a genetically distinct
self-sustaining population that is not supported by
an influx of swarms by nearby managed apiaries
(Seeley et al.2015). Mitotyping analysis revealed
that haplotypes common to A. m. ligustica and A.
m. carnica distributed almost evenly in the Arnot
Forest honeybees, revealing that the population
was probably not ancestral to the A. m. mellifera
race that first colonized the region in the 1600s
(Seeley et al.2015).
Genomic changes in the Arnot Forest bee pop-
ulation before and after the mite was introduced
were analyzed by sequencing the whole genome
of historical honeybee samples collected from the
population in 1978 compared to samples taken in
2010 (Mikheyev et al.2015). This study has
shown that the population evidently crashed, like-
ly after the arrival of Varro a , and that during this
time, colonies were too weak to swarm or produce
queens, which resulted in a loss of haplotypic
diversity in the population (Mikheyev et al.
2015). During this bottleneck, colonies were still
able to produce drones so nucleic genetic diversity
remained unchanged (Mikheyev et al.2015). At
least 232 genes spread throughout the honeybee
genome showed signs of selection in this popula-
tion, but there was no evidence of a hard selective
B. Locke
sweep (Mikheyev et al.2015). Further, none of
the genes under selection were associated with the
immune response suggesting that resistance to
viruses, for example, was unlikely to be involved
in the survival of this population (Mikheyev et al.
2015). Higher intracolony genetic diversity can
improve disease resistance and colony health
(Tarpy 2003). However, it could not explain the
survival of the Arnot Forest population, as these
queens did not have a higher mating frequency
than queens from nearby managed colonies
(Tarpy et al.2015).
Mikheyev et al.(2015) did find that half of the
genes showing signs of selection in the Arnot
Forest screen were related to bee development.
This could suggest that changes in the beesde-
velopmental program could influence the mites
population growth in the colonies since, for ex-
ample, mite reproduction is directly synchronized
with the developing pupa (Martin 1994).
Morphological differences were observed with
Arnot Forest bees having a smaller body size,
more similar to Africanized bees, than typical
European honeybees (Mikheyev et al. 2015).
This could mean a shorter developmental duration
or inadequate cell space for mite reproduction in
the Arnot Forest bees, even though these charac-
teristics are not enough to fully support mite re-
sistance (Martin 1998; Seeley and Griffin 2011).
Today, there are an estimated 18colonies living
in the forest from a census performed in 2011
(Seeley et al.2015). Having access to the Arnot
Forest bees in movable frame hives is a main goal
to enable investigations on both bee and mite
characteristics that support the continued survival
of this population without mite control.
The populations reviewed here demonstrate that
mite resistance is possible for A. mellifera honey-
bees around the world (Figure 1) and that there are
multiple genetic adaptive routes to achieving a
sustainable mite resistance (Table I). In all of the
populations, there seems to be a variety of mite-
resistant traits that additively contribute to reduc-
ing the mite population growth within the colony,
as opposed to a single super trait.
3.1. Mite-resistant mechanisms
Host resistance is defined as the ability of the
host to reduce the fitness of the parasite, while
host tolerance is defined as the ability of the host
to reduce the effect of the parasite (Schmid-
Hempel 2011). It remains to be clarified whether
the survival of the Arnot Forest bees and the
Italian bees on Fernando de Noronha is due to
an adaptive resistance by the host, host tolerance
to mite infestation, or reduced virulence by the
mite either by the mites haplotype or adaptive
reduced virulence. While many of these popula-
tions reviewed here clearly demonstrate adapted
host resistance or at least tolerance, investigations
have been very bee-centric, likely due to the com-
mon acceptance that the Varroa mite has a low
genetic variation in Europe due to its clonal origin
(Solignac et al. 2005). A deeper understanding of
the mites passive or active role in the co-evolu-
tion among all of these populations would be
Behavioral resistant mechanisms such as hy-
gienic behavior and grooming behavior seem to
play an important role inthe resistance of the A. m.
scutellata honeybee populations in Brazil and
South Africa and even in the honeybee population
in far eastern Russia (Table I). However, they did
not seem to be significantly more expressed in the
Gotland mite-resistant population compared to
local mite-susceptible honeybees (Table I).
Studies on the mite-resistant Asian hive bee (A.
cerana ) have shown that hygienic and grooming
behavior are less pronounced than previously stat-
ed and rather additively contribute to their overall
resistance rather than explain it (Fries et al.1996;
Rosenkranz et al.1993).
It seems clear that the Gotland, Avignon, and
Russian honeybee populations have evolved mite
resistance as they are able, in yet unknown ways,
to reduce the mites reproductive success
(Table I). Simulation modeling of A. cerana col-
ony dynamics has suggested that the lack of mite
reproduction and limited available drone brood
was sufficient enough to explain the mite resis-
tance of this species (Fries et al.1994). The A.
mellifera honeybee populations with reduced
mite reproductive success reviewed here may
have unique ways of achieving this specific
Natural Va rro a mite-surviving Apis mellifera honeybee populations
mite-resistant mechanism that could include
changes in brood volatiles, adult VSH behavior
selectively removing reproducing mites, or even
both mechanisms combined.
Reduced colony size is an interesting mite-
resistant parameter expressed in the honeybee
populations in Brazil, South Africa, Gotland, and
in the Arnot Forest but not in Russia or the Island
of Fernando de Noronha (Table I). A reduced
colony size and reduced brood production (spe-
cifically drone brood production) means limited
opportunities for mite reproduction and is a very
important mite-resistant characteristic of the
Asian hive bee (Fries et al.1994). A noteworthy
observation is that small colony size seems to be a
common trait of populations with wild honeybees
(such as Brazil, South Africa, and the Arnot
Forest) or with less intensified management (as
on Gotland).
3.2. Insights on apicultural management
Importantly, all the mite-resistant populations in
this review have experienced a general lack of, or
Figure 1. The global distribution of naturally occurring Var roa mite-surviving A. mellifera populations.
Table I. A summary of important mite-resistant traits investigated in the naturally occurring Varroa mite-surviving
honeybee populations showing the variety and diversity of the importance of traits within and between populations.
A check-mark indicates a significant difference from mite-susceptible honeybees, while a cross indicates a non-
significant difference and an empty box indicates that trait has not yet been measured.
B. Locke
less intensified, apicultural management. The api-
cultural industry is drastically threatened by cata-
strophic colony losses due to the spread of honey-
bee diseases and parasites, especially the Varro a
mite (Neumann and Carreck 2010; Ratnieks and
Carreck 2010). Ironically, the spread of these dis-
eases in apiculture is facilitated through intensified
management practices (Fries and Camazine 2001).
Co-evolutionary processes such as natural selec-
tion that lead to a stable host-parasite relationship
dered for the European honeybee host since api-
cultural practices remove the mite and conse-
quently the selective pressure required for such
an adaptive process to occur. On top of that,
pesticides administered to colonies by beekeepers
to treat against mite infestation can actually cause
more damage to bee health (Haarmann et al.
2002;Johnsonetal.2009; Locke et al.2012a).
Adaptations by the mite towards reduced viru-
lence depend on the available transmission routes
within the honeybee population, which can be
altered by apiculture. Vertical transmission from
mother to daughter leads to reduced virulence
adaptations, while horizontal transmission be-
tween colonies leads to increased mite virulence
(Schmid-Hempel 2011). Modern apicultural prac-
tices actually favor parasitic transmission routes
that select for higher virulence, mainly by
preventing swarming, crowding colonies in high-
density apiaries, and by exchanging hive equip-
ment between diseased or dead colonies (Fries
and Camazine 2001; Seeley and Smith 2015).
These mite-resistant A. mellifera populations
have all experienced natural mite infestation pres-
sure and have been given the opportunity for
natural adaptations without the influence of typi-
cal apicultural practices. Wild honeybees in Brazil
and Africa experiencing natural mite infestation
selection pressure may pass heritable adaptive
resistance to managed colonies that contribute to
the stability of the population. This constant se-
lection pressure may be necessary even though the
A. m. scutellata honey bees in Brazil and Africa
have a somewhat genetic pre-disposition for mite
Many of these natural Va r ro a mite-surviving
A. mellifera populations are smaller colonies than
seen in apiculture as the artificial selection
pressure for high honey yields insisted in apicul-
ture has been removed. The ability for colonies to
swarm might not completely prevent the mite
population buildup by the autumn, but when com-
bined together with other colony population dy-
namics and mite-resistant traits, it can contribute
to reducing the mite population growth and im-
proving colony longevity.
Unnaturally high colony density in apiculture
leads to higher mite re-infestation and increased
spread of disease (Seeley and Smith 2015).
However, high colony density is not typical for
these mite-resistant A. mellifera populations.
There is an estimated 10 million colonies in South
Africa with only about 1 % of them being managed
by beekeepers (Strauss et al.2013). Apiculture is
generally less intensified here, and colonies are
often captured wild swarms. A similar situation is
seen in Brazil with less intensified management and
a larger wild population of honeybees than man-
aged (Vandame and Palacio 2010). By contrast,
most colonies in Europe and North America are
managed by beekeepers and wild colonies are typ-
ically swarms that have escaped from apiaries. The
Arnot Forest population on the other hand has a
density of 1 colony/km
, much less than the typical
colony density for managed apiaries in the region
(Seeley et al.2015).
There is an urgent need for a sustainable
solution to the threat of Varro a mites for the
economic viability of apiculture and agriculture,
as well as for honeybee health, conservation, and
for ecosystem services. Understanding the natu-
ral interactions and adaptations between honey-
bees and Va rr o a mites is an essential first step
towards achieving this goal. These mite-resistant
honeybee populations provide valuable insight
and give hope for a potentially sustainable solu-
tion through mite resistance. Importantly, they
actasexamplesthatbreedingforVa r r o a mite
resistance is possible in all honeybee populations
throughout the world. One potential avenue is by
breeding genetically inheritable adapted mite-
resistant traits from these populations such as
behavioral defenses or reduced mite reproductive
success. However, these populations also
Natural Va rro a mite-surviving Apis mellifera honeybee populations
emphasize the influence that apiculture has on
the development of infections in honeybee colo-
nies, and consequently, by example suggest that
the most effective solution for sustainably im-
proving honeybee health would come from
adopting better management practices.
I would like to thank the editorial board for the
invitation to write this review article as well as two
anonymous reviewers for providing helpful comments
to improve this review. Joachim de Miranda and
Ingemar Fries are also thanked for their earlier com-
ments on the manuscript. Financial support was provid-
ed by The Swedish Research Council Formas, diarienr.
This article is distributed under the terms of the
Creative Commons Attribution 4.0 International Li-
cense (,
which permits unrestricted use, distribution, and repro-
duction in any medium, provided you give appropriate
credit to the original author(s) and the source, provide a
link to the Creative Commons license, and indicate if
changes were made.
Populations dabeilles ( Apis mellifera ) survivant
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Natürliche Honigbienenpopulationen, die trotz
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Varroa destructor / Varroaresistenz / Parasit-Wirt-
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... These parameters affect infestation rates and hence potential damage inflicted to host colonies. Their quantification is thus fundamental to our understanding of the mechanisms sustaining the coevolved and balanced host-parasite relationship (Locke, 2016) and to our ability to limit the damage generated by the parasite by, for example, selecting for host resistance traits (Dietemann et al., 2012). To fill the lack of data on infestation and reproduction of Varroa spp. on their original host, we measured adult and brood infestation rates, as well as several parameters of reproductive output of V. destructor and V. jacobsonii mites naturally infesting A. cerana. ...
... Nevertheless, some patterns emerge (Table S7). The similarities in mite reproduction between A. cerana and A. mellifera suggest yet undescribed common resistance mechanisms (this study; Locke, 2016;Wang et al., 2019;Z Lin, S Wang, P Neumann, G Chen, P Page, L Li, F Hu, H Zheng & V Dietemann, unpublished data). Indeed, the number of viable daughters produced (0.5-2.5) appears to be in the same range for both hosts species (Table S7). ...
... The most obvious difference between coevolved and noncoevolved taxa is the long known absence of reproduction in worker brood of A. cerana (Table S7). Although this trait may represent the central resistance mechanism of A. cerana, several populations of A. mellifera nevertheless survive V. destructor infestations despite such reproduction (Locke, 2016;Oddie et al., 2018; Even though high infestation rates of drone brood have been reported in A. mellifera (up to 51% in untreated colonies;Martin, 1995) and those of A. cerana being generally low, the highest values have actually been measured in A. cerana (Table S7). Together with generally lower fecundity and percentage of fertile mites infesting A. mellifera compared to A. cerana drones (Table S7), this suggests low selective pressure on the invasive lineage of V. destructor for maximizing reproduction on A. mellifera drones, possibly due their ability to reproduce on the more readily available worker brood in this host. ...
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Parasite host shifts can impose a high selective pressure on novel hosts. Even though the coevolved systems can reveal fundamental aspects of host-parasite interactions, research often focuses on the new host-parasite relationships. This holds true for two ectoparasitic mite species, Varroa destructor and Varroa jacobsonii, which have shifted hosts from Eastern honey bees, Apis cerana, to Western honey bees, Apis mellifera, generating colony losses of these pollinators globally. Here, we study infestation rates and reproduction of V. destructor and V. jacobsonii haplotypes in 185 A. cerana colonies of six populations in China and Thailand to investigate how co-evolution shaped these features. Reproductive success was mostly similar and low, indicating constraints imposed by hosts and/or mite physiology. Infestation rates varied between mite haplotypes, suggesting distinct local co-evolutionary scenarios. The differences in infestation rates and reproductive output between haplotypes did not correlate with the virulence of the respective host-shifted lineages suggesting distinct selection scenarios in novel and original host. The occasional worker brood infestation was significantly lower than that of drone brood, except for the V. destruc-tor haplotype (Korea) from which the invasive lineage derived. Whether mites infesting and reproducing in atypical intraspecific hosts (i.e., workers and queens) actually predisposes for and may govern the impact of host shifts on novel hosts should be determined by identifying the underlying mechanisms. In general, the apparent gaps in our knowledge of this coevolved system need to be further addressed to foster the adequate protection of wild and managed honey bees from these mites globally.
... Several traits observed in naturally surviving populations have been proposed to contribute to the survival of A. mellifera colonies infested by V. destructor [64,70]. The expression of some of these traits is thought to lead to the reduction of reproduction and/or survival of the mite within the honey bee brood cell. ...
... The main reason for this weak link is that most of the studies were performed on treated colonies, which restrains the amount of data available to accurately determine effects in terms of improved colony survival. Another contentious point is that several traits (e.g., VSH, MNR, uncapping-recapping and hygienic behaviour towards dead brood) have only been observed in some naturally surviving populations [64,70,115]. Even within a single honey bee population, the contribution of a particular trait to survival can be unclear: in Africanized honey bees, two studies indicated that VSH may reduce infestation level [167,168], whereas another concluded that it is not a key resistance factor [169] (see Additional file 3: Table S3). ...
... Similarly, V. destructor-infested A. mellifera colonies in Papua New Guinea and Solomon Islands survive without acaricidal treatments, which could be due to the absence of deformed wing virus (DWV) in these populations [201]. The survival of the Gotland population in Sweden was also partly attributed to a tolerance against viral infections [70,[202][203][204]. Tolerance to viruses could result from natural selection for more virus-tolerant colonies [204] and/or for less virulent viruses [203]. ...
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Background In spite of the implementation of control strategies in honey bee ( Apis mellifera ) keeping, the invasive parasitic mite Varroa destructor remains one of the main causes of colony losses in numerous countries. Therefore, this parasite represents a serious threat to beekeeping and agro-ecosystems that benefit from the pollination services provided by honey bees. To maintain their stocks, beekeepers have to treat their colonies with acaricides every year. Selecting lineages that are resistant to infestations is deemed to be a more sustainable approach. Review Over the last three decades, numerous selection programs have been initiated to improve the host–parasite relationship and to support honey bee survival in the presence of the parasite without the need for acaricide treatments. Although resistance traits have been included in the selection strategy of honey bees, it has not been possible to globally solve the V. destructor problem. In this study, we review the literature on the reasons that have potentially limited the success of such selection programs. We compile the available information to assess the relevance of selected traits and the potential environmental effects that distort trait expression and colony survival. Limitations to the implementation of these traits in the field are also discussed. Conclusions Improving our knowledge of the mechanisms underlying resistance to V. destructor to increase trait relevance, optimizing selection programs to reduce environmental effects, and communicating selection outcomes are all crucial to efforts aiming at establishing a balanced relationship between the invasive parasite and its new host.
... Today, most managed A. mellifera colonies depend on mite control treatments to survive (Rosenkranz et al., 2010). However, several Varroa-surviving honey bee populations have been documented around the world as a result of selective breeding or natural selection (e.g., Locke, 2016;Le Conte and Mondet, 2017). Bees may survive Varroa through the expression of resistance or tolerance traits. ...
... Such developments relied on the identification of specific traits that characterize these populations. This is a critical point since some characteristics that strongly confer mite resistance to some bee populations may not have a great influence on others (Locke, 2016). In Argentina, efforts have been made to identify and select local stocks that survive without mite treatment and characterize the underlying mechanisms. ...
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The Western honey bee, Apis mellifera, is an important species in providing honey and pollination services globally. The mite Varroa destructor is the major threat to A. mellifera, and it is associated with the severe colony winter mortality reported in recent decades. However, Varroa mite tolerant or resistant populations of A. mellifera have been detected around the world. A proposed mechanism responsible for limiting mite population growth in the colonies is grooming behavior, the physical removal and injury of mites from the adult bee bodies by individual workers or by their nest-mates. This behavioral strategy has been poorly studied in V. destructor-resistant colonies worldwide, especially in honey bee populations of European origin. In Argentina, honey bee stocks showing survival without mite treatment have been reported. In the present study, European-derived A. mellifera populations established in the Transition Chaco eco-region (Santa Fe province), with a subtropical climate, were characterized at the colony level. A honey bee stock showing natural Varroa-resistance (M) was compared to a Varroa-susceptible stock (C) for parameters of colony status (colony strength, percentage of Varroa infestation in adults and brood, hygienic behavior) and for indirect measures of grooming (percentage of fallen mites and damaged mites). M colonies showed lower phoretic and brood infestation and higher hygienic behavior in early autumn, and higher survival and population strength after wintering, in comparison with C colonies. The mean percentages of fallen mites and of damaged mites, and the injury to mites were higher in M than in C colonies. Our results suggest that, by modulating the parasitization dynamics in colonies, grooming behavior would be associated with the higher survival of Varroa-resistant stock. This study sheds light on how honey bee colonies can adaptively respond to mite pressure by modeling their behavior to resist Varroosis and provides evidence for grooming as an emerging factor evolving by natural selection. Percentage of damaged mites appears to be a reliable measure to enhance this behavior in honey bee colonies by selective breeding. Finally, the importance of improving and protecting locally adapted honey bee populations with natural Varroa resistance for regional apiculture is discussed.
... In addition, populations of A. mellifera were identified that survived and coexist with V. destructor for a long time. Evaluation of such colonies showed that they have a high level of Varroa sensitive and grooming behavior (Locke, 2016b). On the basis of genomic and transcriptome studies, loci and genes associated with Varroa resistance were identified. ...
Full-text available
In the mid-20th century, the first case of infection of European bees Apis mellifera L. with the ectoparasite mite Varroa destructor was recorded. The original host of this mite is the Asian bee Apis cerana. The mite V. destructor was widespread throughout Europe, North and South America, and Australia remained the only continent free from this parasite. Without acaricide treatment any honeybee colony dies within 1–4 years. The use of synthetic acaricides has not justified itself – they make beekeeping products unsuitable and mites develop resistance to them, which forces the use of even greater concentrations that can be toxic to the bees. Therefore, the only safe measure to combat the mite is the use of biological control methods. One of these methods is the selection of bee colonies with natural mite resistance. In this article we summarize publications devoted to the search for genetic markers associated with resistance to V. destructor. The first part discusses the basic mechanisms of bee resistance (Varroa sensitive hygienic behavior and grooming) and methods for their assessment. The second part focuses on research aimed at searching for loci and candidate genes associated with resistance to varroosis by mapping quantitative traits loci and genome-wide association studies. The third part summarizes studies of the transcriptome profile of Varroa resistant bees. The last part discusses the most likely candidate genes – potential markers for breeding Varroa resistant bees. Resistance to the mite is manifested in a variety of phenotypes and is under polygenic control. The establishing of gene pathways involved in resistance to Varroa will help create a methodological basis for the selection of Varroa resistant honeybee colonies.
... For example, in A. mellifera, hygienic and grooming behaviors are expressed more highly in Africanized honey bees than in European ones. Perhaps this explains the higher resistance of Africanized bees to V. destructor compared to European bees [71]. ...
Full-text available
The microsporidian Nosema parasites, primarily Nosema ceranae, remain critical threats to the health of the honey bee Apis mellifera. One promising intervention approach is the breeding of Nosema-resistant honey bee colonies using molecular technologies, for example marker-assisted selection (MAS). For this, specific genetic markers used in bee selection should be developed. The objective of the paper is to search for associations between some microsatellite markers and Nosema disease in a dark forest bee Apis mellifera mellifera. For the dark forest bee, the most promising molecular genetic markers for determining resistance to nosemosis are microsatellite loci AC117, Ap243 and SV185, the alleles of which (“177”, “263” and “269”, respectively) were associated with a low level of Nosema infection. This article is the first associative study aimed at finding DNA loci of resistance to nosemosis in the dark forest bee. Nevertheless, microsatellite markers identified can be used to predict the risk of developing the Nosema disease.
... While naturally resistant strains mainly consist of feral colonies with no impact of the beekeeper, another approach can be mass selection using a large group of varroa infested honey bee colonies, which are allowed to live with the mite without any treatment and either die or survive. This has been called the "Bond test" ("Live and let die!"), and was developed in Sweden and in France and then in a few other European countries [6]. ...
Full-text available
Developing resistance to the varroa mite in honey bees is a major goal for apicultural science and practice, the development of selection strategies and the availability of resistant stock. Here we present an extended literature review and survey of resistant populations and selection programs in the EU and elsewhere, including expert interviews. We illustrate the practical experiences of scientists, beekeepers, and breeders in search of resistant bees. We describe numerous resistant populations surviving without acaricide treatments, most of which developed under natural infestation pressure. Their common characteristics: reduced brood development; limited mite population growth; and low mite reproduction, may cause conflict with the interests of commercial beekeeping. Since environmental factors affect varroa mite resistance, particular honey bee strains must be evaluated under different local conditions and colony management. The resistance traits of grooming, hygienic behavior and mite reproduction, together with simple testing of mite population development and colony survival, are significant in recent selection programs. Advanced breeding techniques and genetic and physiological selection tools will be essential in the future. Despite huge demand, there is no well-established market for resistant stock in Europe. Moreover, reliable experience or experimental evidence regarding the resistance of stocks under different environmental and management conditions is still lacking.
... Some viruses show pathogenicity only under certain favorable environmental conditions. Varroa mites V. destructor are considered to be the main transmitter of many honey bee viruses: deformed wing virus (DWV); acute bee paralysis virus (ABPV), Kashmir bee virus (KBV), and Israeli acute paralysis virus (IAPV) [39,54]. Furthermore, three viruses in the transmission of which Varroa seems to play no significant role, namely, chronic bee paralysis virus (CBPV), sacbrood virus (SBV), and black queen cell virus (BQCV) are also frequently surveyed [55,56]. ...
Full-text available
The Western honey bee (Apis mellifera L., Hymenoptera: Apidae) is a species of crucial economic, agricultural and environmental importance. In the last ten years, some regions of the world have suffered from a significant reduction of honey bee colonies. In fact, honey bee losses are not an unusual phenomenon, but in many countries worldwide there has been a notable decrease in honey bee colonies. The cases in the USA, in many European countries, and in the Middle East have received considerable attention, mostly due to the absence of an easily identifiable cause. It has been difficult to determine the main factors leading to colony losses because of honey bees' diverse social behavior. Moreover, in their daily routine, they make contact with many agents of the environment and are exposed to a plethora of human activities and their consequences. Nevertheless, various factors have been considered to be contributing to honey bee losses, and recent investigations have established some of the most important ones, in particular, pests and diseases, bee management, including bee keeping practices and breeding, the change in climatic conditions, agricultural practices, and the use of pesticides. The global picture highlights the ectoparasitic mite Varroa destructor as a major factor in colony loss. Last but not least, microsporidian parasites, mainly Nosema ceranae, also contribute to the problem. Thus, it is obvious that there are many factors affecting honey bee colony losses globally. Increased monitoring and scientific research should throw new light on the factors involved in recent honey bee colony losses. The present review focuses on the main factors which have been found to have an impact on the increase in honey bee colony losses.
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Populations of European honeybee subspecies, Apis mellifera , have the ability to adapt naturally to the ectoparasitic mite, Varroa destructor . It is possible that a tolerance to mite-vectored viruses may contribute to colony survival. If this is the case, surviving populations should show lower virus titers and prevalence compared to susceptible populations. Here, we investigated the prevalence and titers of 10 viruses, some known to be associated with V. destructor , in adult workers and pupae as well as mites. Samples were collected from both a mite-surviving and mite-susceptible honeybee population in Norway. Surviving colonies had a lower prevalence of a key virus (DWV-A) associated with V. destructor in individual adult bees sampled, and generally lower titers of this virus in mite infested pupae and mites within the colonies when compared to sympatric, susceptible controls. However, these surviving colonies also displayed higher prevalence and titers of two viruses not associated with V. destructor (BQCV & LSV1). The results of this study therefore suggest that general tolerance to virus infections is unlikely to be a key mechanism for natural colony survival in Norway, but evidence may point to mite control as a predominant mechanism.
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Background: Managed, feral and wild populations of European honey bee subspecies, Apis mellifera , are currently facing severe colony losses globally. There is consensus that the ectoparasite mite Varroa destructor , that switched hosts from the Eastern honey bee Apis cerana to the Western honey bee A. mellifera , is a key factor driving these losses. For >20 years, breeding efforts have not achieved that European honey bee colonies survive infestations without the need for mite control. However, at least three populations of European honey bees have developed this by means of natural selection and have been surviving for >10 years without mite treatments. Reduced mite reproductive success has been suggested as a key factor explaining this natural survival. Here, we report a managed A. mellifera population in Norway, that has been naturally surviving consistent V. destructor infestations for >17 years. Methods: Surviving colonies and local susceptible controls were evaluated for mite infestation levels, mite reproductive success and twopotential mechanisms explaining colony survival: grooming of adult worker bees and Varroa Sensitive Hygiene (VSH): adult workers specifically detecting and removing mite-infested brood. Results: Mite infestation levels were significantly lower in surviving colonies and mite reproductive success was reduced by ~30% compared to the controls. No significant differences were found between surviving and control colonies for either grooming or VSH. Discussion: Our data confirm that reduced mite reproductive success seems to be a key factor for natural survival of infested A. mellifera colonies. However, neither grooming nor VSH seem to explain colony survival. Instead, other behaviors of the adult bees seem to be sufficient to hinder mite reproductive success, because brood for this experiment was taken from susceptible donor colonies only. To mitigate the global impact of V. destructor , we suggest learning more from nature, i.e. identifying the obviously efficient mechanisms favored by natural selection.
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In 1993 at Le Born near Toulouse, France 12 Apis mellifera intermissa queens from Tunisian colonies that had been naturally selected for tolerance to varroosis were tested against 12 unselected Apis mellifera carnica queens. We wished to determine if the tolerance of the intermissa queens was genetic in origin or simply due to specific local conditions in Tunisia. Queens were placed in 2 kg swarms of varroa infested bees and allowed to develop without any treatments. Nine colonies from each group over wintered. After exposure to heavy varroa infestations one carnica and seven intermissa queens were still surviving in August 1994. From 1995 to 2004 the surviving experimental colonies hybridized with the local population of bees. The majority of these hybrids were tolerant to Varroa destructor indicating a genetic control of the tolerance.
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The type and degree of damage to adult workers of Apis mellifera from infestation with the parasitic mite Varroa jacobsoni during development was investigated. Mean weights of infested bees upon emergence as adults were 6·3% to 25% less than for healthy bees. Mean % weight loss was correlated at a high level of significance with the number of mites in the cell. Only 6% of infested bees showed obvious physical deformation in the form of wing damage.
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A well-documented population of honey bees on Gotland, Sweden is resistant to Varroa destructor mites and is able in some way to reduce the mite's reproductive success. The aim of this study was to determine the genetic and maternal contribution to the inheritance of the reduced mite reproductive success trait in this population. Four genotypic groups of colonies were established by crossing the mite-resistant population of Gotland with a mite-susceptible population in Uppsala, Sweden, through artificial insemination of reared queens with drone semen. All the colonies in groups with a genetic origin from the resistant population expressed reduced mite reproductive success regardless if the genetic origin was maternal, paternal or both, and no statistical differences were observed between the reciprocal crosses. These results strongly imply a dominant genetic component to the trait's inheritance, as opposed to maternal effects or epigenetic mechanisms, and that the trait can be easily produced through selective breeding using the mite-resistant Gotland bee stock. Varroa destructor / mite resistance / breeding / mite reproduction
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Understanding genetic changes caused by novel pathogens and parasites can reveal mechanisms of adaptation and genetic robustness. Using whole-genome sequencing of museum and modern specimens, we describe the genomic changes in a wild population of honey bees in North America following the introduction of the ectoparasitic mite, Varroa destructor. Even though colony density in the study population is the same today as in the past, a major loss of haplotypic diversity occurred, indicative of a drastic mitochondrial bottleneck, caused by massive colony mortality. In contrast, nuclear genetic diversity did not change, though hundreds of genes show signs of selection. The genetic diversity within each bee colony, particularly as a consequence of polyandry by queens, may enable preservation of genetic diversity even during population bottlenecks. These findings suggest that genetically diverse honey bee populations can recover from introduced diseases by evolving rapid tolerance, while maintaining much of the standing genetic variation.
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Suppressed Mite Reproduction (SMR) is a trait of honey bees that provides resistance to Varroa destructor. The mechanism of resistance in SMR bees is the removal of infested pupae from capped brood, so a better name is VSH bees (acronym for Varroa Sensitive Hygiene). This study compared the removal of infested brood by VSH and control bees to determine whether VSH bees removed infested pupae of different ages at similar rates. A pair of infested combs containing all stages of pupae were transferred into each host colony (six VSH and six control colonies) for 40 hours. VSH bees removed significantly more (55%) infested cells (singly and multiply infested), than controls (13%). They removed significantly more (66%) singly infested pupae aged from one to five days post capping (cohort A) than did controls (16%). The two types did not differ in the removal of singly infested pupae aged five to 10 days post capping (cohort B) (5–22%). Many pupae were found in uncapped cells at the end of the test, and most of the uncapped pupae were infested with mites. None of the uncapped cells contained prepupae, the development stage occurring during the first three days post capping. Thus, removal of infested pupae may be triggered by stimuli in cells with pupae aged 3–5 days post capping.La supresión de la reproducción del ácaro (SMR) es un rasgo de las abejas que les proporciona resistencia ante Varroa destructor. El mecanismo de resistencia en abejas SMR consiste en retirar las pupas infestadas de la cría operculada, por lo que abejas VSH (siglas de higiene sensitiva a la varroa) es un término más adecuado. Este estudio comparó la retirada de cría infestada por abejas VSH y abejas control para determinar si las abejas VSH quitaban pupas infestadas de diferentes edades en proporciones similares. Un par de cuadros infestados que contenían pupas de todas las etapas fueron introducidos en colmenas anfitrionas (seis VSH y seis colmenas control) durante 40 horas. Las abejas VSH retiraron significativamente más pupas de celdas infestadas (55%) (única ó múltiple infestación) que las colmenas control (13%). Las abejas VSH eliminaron considerablemente más (66%) pupas maduras de infestación única de uno a cinco días tras la operculación (cohorte A) que las colmenas control (16%). Los dos tipos de abejas no presentaron diferencias en la retirada de pupas maduras entre los cinco y diez días tras la operculación (cohorte B) (5–22%). Muchas pupas fueron encontradas en celdas desoperculadas al final de la prueba, y la mayor parte de las pupas desoperculadas estaban infestadas por el ácaro. Ninguna de las celdas desoperculadas contuvo pre-pupas, etapa del desarrollo que trascurre durante los primeros tres días tras la operculación. Por lo tanto, la retirada de pupas infestadas se puede activar mediante el estímulo en celdas con pupas de entre 3–5 días tras la operculación.
A time-saving method for determining the duration of the capped stage (sealed brood) of large numbers of colonies is described. The results of 112 colonies covering 22 different origins and hybrids of European honeybee races are presented. Differences up to 9 h between strains and up to 19 h within individual colonies could be detected. Influenced by seasonal effects, the average capped period is about 7 h shorter in early than in late summer. For one group of test colonies (n= 21) the Varroa infestation after 18 months of undisturbed colony and mite population development has been determined. The correlation between the capped period and the susceptibility of the colonies to mites is calculated as r = 0·48. By linear regression, an 8·7% reduction of the final mite infestation is calculated for a 1-h reduction of the capped period. The heritability of the duration of the capped period is estimated with h2 = 0·232. This may be a realistic value for test populations of European honeybee under field conditions.