See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/237004340

Genetic diversity affects colony survivorship in commercial honey bee

colonies

Article  in  The Science of Nature · June 2013

DOI: 10.1007/s00114-013-1065-y · Source: PubMed

CITATIONS READS

37 358

3 authors, including:

David R. Tarpy Dennis VanEngelsdorp

North Carolina State University University of Maryland, College Park
161 PUBLICATIONS   4,458 CITATIONS    157 PUBLICATIONS   7,703 CITATIONS   

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

COLOSS Bee book View project

Queen reproductive quality and colony health in honey bees View project

All content following this page was uploaded by David R. Tarpy on 15 June 2014.

The user has requested enhancement of the downloaded file.

Naturwissenschaften (2013) 100:723–728
DOI 10.1007/s00114-013-1065-y
ORIGINAL PAPER
Genetic diversity affects colony survivorship in commercial
honey bee colonies
David R. Tarpy & Dennis vanEngelsdorp & Jeffrey S. Pettis
Received: 7 March 2013 / Revised: 16 May 2013 / Accepted: 22 May 2013 / Published online: 1 June 2013
# Springer-Verlag Berlin Heidelberg 2013
Abstract Honey bee (Apis mellifera) queens mate with
unusually high numbers of males (average of approximately
12 drones), although there is much variation among queens.
One main consequence of such extreme polyandry is an
increased diversity of worker genotypes within a colony,
which has been shown empirically to confer significant
adaptive advantages that result in higher colony productivity
and survival. Moreover, honey bees are the primary insect
pollinators used in modern commercial production agricul-
ture, and their populations have been in decline worldwide.
Here, we compare the mating frequencies of queens, and
therefore, intracolony genetic diversity, in three commercial
beekeeping operations to determine how they correlate with
various measures of colony health and productivity, partic-
ularly the likelihood of queen supersedure and colony sur-
vival in functional, intensively managed beehives. We found
the average effective paternity frequency (me) of this popu-
lation of honey bee queens to be 13.6±6.76, which was not
significantly different between colonies that superseded
their queen and those that did not. However, colonies that
were less genetically diverse (headed by queens with me ≤7.0)
were 2.86 times more likely to die by the end of the study
Communicated by: Sven Thatje
D. R. Tarpy (*)
Department of Entomology, North Carolina State University,
Campus Box 7613, Raleigh, NC 27695-7613, USA
e-mail: david_tarpy@ncsu.edu
D. vanEngelsdorp
Department of Entomology, University of Maryland, 3136 Plant
Sciences Building,
College Park, MD 20742-4454, USA
e-mail: Dennis.vanEngelsdorp@gmail.com
J. S. Pettis
USDA–ARS Bee Research Laboratory, Bldg. 306 BARC-E,
Beltsville, MD 20705, USA
e-mail: Jeff.Pettis@ars.usda.gov
when compared to colonies that were more genetically diverse
(headed by queens with me >7.0). The stark contrast in colony
survival based on increased genetic diversity suggests that
there are important tangible benefits of increased queen mat-
ing number in managed honey bees, although the exact mech-
anism(s) that govern these benefits have not been fully
elucidated.
Keywords Genetic diversity . Social insects . Genotyping .
Supersedure . Colony mortality
Introduction
Insect pollinators are important in both natural and
agroecosystems. It is of great concern, therefore, that there
have been documented widespread and drastic declines in
their populations worldwide (Biesmeijer et al. 2006;
vanEngelsdorp and Meixner 2010). Western honey bees
(Apis mellifera L.) are the predominant insect pollinator
for many crops and are, hence, critical to agricultural econ-
omies (National Research Council 2007; Gallai et al. 2009).
Understanding the governing factors of increased colony
mortality is, therefore, of fundamental concern.
In the US, the majority of the active pollination by honey
bees is done by large-scale, migratory beekeeping opera-
tions that transport their beehives in and out of blooming
crops over the course of a growing season. While actively
managed (sometimes intensively so), honey bees are not
domesticated in the strict sense and are, therefore, subject
to many environmental and ecological factors (Harpur et al.
2012; Oldroyd 2012). The susceptibility to multiple envi-
ronmental stressors, ranging from parasites and pathogens to
foraging constraints, makes understanding the biological
mechanisms that govern colony function a particularly in-
sightful approach to elucidating factors that result in poor
health. Central to colony function is the single queen of a
724
honey bee colony, the mother to tens of thousands of daugh-
ter workers sired from the stored sperm from her one to two
dozen mates (Winston 1987). Such extreme multiple mating
(polyandry) early in a queen's lifetime has profound ramifi-
cations on the resultant intracolony genetic diversity of the
colony's workforce that, in turn, has been shown to influ-
ence a wide variety of colony phenotypes (see below). It is
yet unclear, however, if genetic diversity within colonies has
any bearing on actively managed colonies in commercial
beekeeping operations.
Aside from supplying enough sperm for her egg-laying
lifetime, one main consequence of polyandry is an increased
diversity of the genotypes of workers within a colony. This
increased intracolony genetic diversity has been shown em-
pirically to confer significant adaptive advantages, including
homeostatic stability (Oldroyd et al. 1992; Fuchs and
Schade 1994; Jones et al. 2004; Mattila and Seeley 2007;
reviewed by Oldroyd and Fewell 2007), reduced risk of
brood pathogens (Palmer and Oldroyd 2003; Tarpy 2003;
Seeley and Tarpy 2007), and moderated heterozygosity at
the sex locus (Page 1980; Tarpy and Page 2002), all of
which result in higher colony productivity and survival.
Much of this benefit is achieved within the first few matings
by queens, as average genetic diversity within colonies is a
nonlinear function of mating number, and 83 % of the total
possible genetic variation arises within an effective paternity
frequency of 7.0 (Fig. 1). Nonetheless, it follows that
hyperpolyandry and the resultant increased colony genetic
diversity may have significant effects on managed queen
and colony health, as it lies at the interface between parasite
prevalence, colony fitness, and queen reproductive success.
In this study, we compare the mating frequencies, and
therefore the intracolony genetic diversity, of queens in three
commercial beekeeping operations to determine how they
correlate with various measures of colony health and sur-
vival. The study was conducted in conjunction with a larger
Fig. 1 The effect of extreme 1.00
polyandry on colony genetic
diversity. As the effective
paternity frequency (me) of a
queen's brood increases, the 0.75
average genetic relatedness
among nestmates (G)
asymptotically decreases as a
function of 0.25+(2me)−1. As 0.50
mating number increases and
genetic relatedness decreases,
the total intracolony genetic
diversity asymptotically 0.25
increases from 0 % of its
maximum at me =1 (G=0.75) to
100 % at me =∞ (G=0.25). At
an effective paternity of 7.0, a 0.00
full 83 % of the total possible
1 7
increased genetic diversity is
achieved Effective paternity frequency (me) of the colony
Naturwissenschaften (2013) 100:723–728
longitudinal study (vanEngelsdorp et al. 2013) that mea-
sured overall colony phenotype in an effort to temporally
assign predictive associations during colony collapse events.
The current study, however, took a predictive descriptive
approach to determine the consequence of established colo-
ny diversity on subsequent colony phenotypes. Understand-
ing how a colony's “sociogenome” (sensu Linksvayer et al.
2009) may influence colony productivity in a “real-world”
context may provide insights into the causes of the decline
in colony health and mechanisms by which to mitigate it. In
doing so, this study investigates the largest number of honey
bee colonies to date for their phenotypic effects of
intracolony genetic diversity.
Materials and methods
As detailed in vanEngelsdorp et al. (2013), we monitored 81
colonies operated by three different migratory beekeepers
between March 2007 through to January 2008. The selected
colonies were a subset of large commercial beekeeping
operations that trucked their colonies north and south along
the eastern United States to pollinate crops or produce
honey (or both) on a diverse variety of crops and natural
vegetation in several states. We divided the colonies in
Operation 1 (OP1) into two groups. The first set of colonies
(OP1pac) were established from 4-lb. packages of bees
(~12,000 adult workers) imported from Australia in Febru-
ary 2007. The packages were installed into previously used
bee equipment from colonies that had died in the previous
3 months with symptoms indicative of Colony Collapse
Disorder (vanEngelsdorp et al. 2009). Of the 19 packages
successfully installed, 10 colonies were headed by Austra-
lian queens, while the remaining nine were headed by
queens produced commercially in Hawaii. The second set
of colonies (n=20) in Operation 1 (OP1est) were randomly
Proportion
maximum diversity
86% increase of
minimum diversity
Average intracolony
genec diversity (G)
13 19 25 31 37
Naturwissenschaften (2013) 100:723–728
selected established colonies that had survived the previous
winter, did not show symptoms of CCD, and were typical of
the bees surviving in that beekeeper's operation. Colonies in
both of the other two operations (OP2, n=24; and OP3, n=18)
were also established colonies that had survived the previous
winter in their respective operations. These two later opera-
tions had not experienced CCD-like symptoms prior to the
survey's initiation.
During the first inspection, we collected samples of adult
bees, placed them on dry ice until storage at −80 °C was
possible, and later genotyped the workers to infer queen
mating number (see below). During the first inspection, we
found the queen in each colony, marked her with colored
paint, and clipped one pair of her wings to help identify her
presence during subsequent inspections. For each subse-
quent inspection, we attempted to locate the marked queen
to verify that she was the mother of the genotyped workers.
In cases where the queen was not observed directly, we
noted the evidence of her presence (i.e., ample eggs and
young larvae). We also noted instances that suggested the
queen had been replaced or was in the process of being
superseded (e.g., mature queen replacement cells and the
presence of unmarked virgin queens). We inspected all
colonies, on average, every 50 days over the course of
1 year. During these inspections, we conducted colony
strength measures (adult worker population, brood area
and quality, and queen condition), acquired samples to de-
termine the prevalence of various parasites (Varroa
destructor and Nosema species), and noted overt symptoms
of various brood and adult diseases (chalkbrood, European
and American foulbrood, Idiopathic Brood Disease Syn-
drome, and Deformed wing virus (DWV) and Sacbrood
(SBV) (reported in vanEngelsdorp et al. 2013).
Laboratory analyses
We extracted the DNA from 30 to 45 adult workers from each
colony using Puregene® DNA extraction kits (Gentra Sys-
tems, Inc.) according to manufacturer's specifications for an-
imal tissue. Specifically, we extracted DNA from each ani-
mal's gaster and performed PCR at eight microsatellite loci to
infer the paternal genotype of each worker. We performed two
separate multiplex reactions, each with four microsatellite
primer sets that have been published previously (Estoup et
al. 1994, 1995; Solignac et al. 2003; see Tarpy et al. 2010;
Delaney et al. 2011). We excluded microsatellite A76 from
our analyses, since it did not provide consistent PCR products.
Using the program Colony 1.2 (Wang 2004), we then used the
allelic data to assign worker paternity and calculate the num-
ber of subfamilies in each colony.
We excluded any worker from a colony that did not
follow Mendelian inheritance, as these individuals were
likely foreign bees that had “drifted” from nearby beehives.
725
We then calculated the observed paternity number (No) of
each queen by simply tabulating the number of different
drone fathers that were represented among her sampled
offspring as well as the effective paternity frequency (me)
according to Nielsen et al. (2003) to account for unequal
representation of drone fathers among the offspring. To
quantify our degree of certainty for these estimates, we
calculated the nondetection error according to Boomsma
and Ratnieks (1996) to account for limited allelic diversity
within each commercial population as well as the 95 % CI
around each individual estimate of me following Tarpy and
Nielsen (2002) to account for sampling error at finite sample
sizes within each colony.
Statistical analyses
We used one-way ANOVA to compare mating frequency
among the colonies headed by queens from different queen
sources. We employed a t test for comparisons of effective
paternity frequencies between colonies that superseded and
those that did not. We used standard regression to determine
the relationship between effective paternity frequency and
queen longevity and other colony health measures that gen-
erated continuous data (e.g., colony population and varroa
mite prevalence). Finally, we calculated the relative risk
associated with an effective mating frequency of 7 or fewer
and colony survival over the entire course of the study, the
significance of which was determined using the Fisher's
exact test (see vanEngelsdorp et al. 2013b). All analyses
were performed using JMP statistical package (SAS 2007).
Results
We successfully genotyped 3,098 workers belonging to 79
colonies (39.2±3.31 workers per colony), a total that ex-
cludes a large number of “drifters” that were determined to
be of different maternal origins from the sampled colonies.
Overall, we found the average observed mating number (No)
of the queens to be 14.7±4.31. Accounting for unequal
paternal representation within each sample, we found the
average effective paternity frequency (me) to be 13.6±6.76
(95 % CI 3.6±1.61) subfamilies. These estimates are well
within the expected range of A. mellifera mating frequencies
(Tarpy et al. 2004).
Effective paternity frequency and queen source
The queens heading colonies that were successfully geno-
typed at the start of this study represented five different
sources: the stock usually produced or purchased by the
cooperating beekeepers (OP1est: n=20, OP2: n=24, and
OP3: n=17) and the stock introduced with installed
726 Naturwissenschaften (2013) 100:723–728

Table 1 Comparisons of different measures of colony phenotype with
effective paternity frequency (me). Standard regression analyses on the
continuous variable of me with each variable resulted in no statistically
significant relationships with the prevalence of poor brood patterns,
chalkbrood disease, deformed wing virus (DWV), idiopathic brood disease
syndrome (IBDS), sacbrood virus (SBV), queen events (e.g., supersedure),
varroa mites, and nosema. The relative risk analyses calculate the increased
likelihood of each factor for colonies headed by queens with me ≤7.0 versus
those with me >7.0. RR for varroa and nosema could not be calculated
because they were ubiquitous in all colonies through the course of the study

Variable Regression analysis (continuous) Relative risk analysis (discrete)

Prevalence (mean %±SE) r2 P Relative risk (95 % CI) P

Poor pattern 0.29±0.027 +0.0001 0.98 0.97 (0.66–1.43) 0.58

Chalkbrood 0.18±0.03 −0.004 0.55 0.96 (0.47–1.98) 0.97
DWV 0.06±0.012 +0.001 0.77 0.58 (0.15–2.20) 0.32
IBDS 0.048±0.011 −0.016 0.27 0.74 (0.19–2.84) 0.49
SBV 0.19±0.229 +0.017 0.24 0.79 (0.11–5.91) 0.65
Queen event 0.13±0.0.02 −0.005 0.52 0.59 (0.21–1.66) 0.89
Varroa 0.30±0.022 −0.012 0.32 n.a. n.a.
Nosema 0.50±0.024 −0.006 0.46 n.a n.a.

packages (Hawaii: n=9, Australian: n=9). We found no
difference in the effective paternity frequency among these
different sources of queens (F4,74 =0.64, P=0.635).
Effective paternity frequency and queen supersedure
A total of 31 (39.2 %) of the genotyped colonies superseded
their queen at least once over the course of the study.
Effective paternity frequency was not different between
colonies that superseded their queens as compared to those
that did not (t77 =−0.91, P=0.18). The queens that were
superseded over the course of the study lived an average
of 76.6±13.23 days. Effective paternity frequency was not
Less diverse
(me < 7.0)
More diverse
(me > 7.0)
n =2
Colony longevity (months alive)
correlated with the estimated time it took for queens to
supersede (r2 =0.09, P=0.09), but we found a negative cor-
relation between effective paternity frequencies of supersed-
ed queens and their survival (t29 =−2.40, p<0.05).
When we excluded data collected after colonies were
found to have superseded (as to correlate measured colony
phenotypes with effective paternity of the genotyped
queens), we found no evidence of consistent relationships
between effective paternity frequency and the incidence of
disease or colony size measures over the entire data set,
during any specific inspection, or at the time of initial
inspection (Table 1; see vanEngelsdorp et al. 2013 for de-
tails). However, there was no empirical control of pathogen
exposure among the colonies, as they were not inoculated
with disease, and overall incidence was low for most mea-
n = 28
sured parasites and pathogens because of control measures

Colony lived
taken by the beekeepers. As such, we found no evidence of
increased/decreased relative risk for the occurrence of dis-
ease and effective mating number (Table 1).
Colony died
Effective paternity frequency and colony survival

The number of effective matings did not differ between colo-

n =9
Effective paternity frequency (me)
Fig. 2 Measured influence of genetic diversity (as measured by effec-
tive paternity frequency) on colony longevity. As queen mating num-
ber increases (x axis), the associated longevity of her colony (y axis)
increases logarithmically (yellow line). Parsing the measured colonies
into categories that were either genetically diverse (me >7.0; unshaded)
or less diverse (me ≤7.0; blue shaded) compared to those that survived
(unshaded) or died (red shaded) over the course of the experiment,
there was a significant of increased genetic diversity on survival; more
genetically diverse colonies were 2.86 times more likely to survive
compared to less diverse colonies
n = 39 nies that survived versus those that did not for the entirety of
the study (t77 =0.68, P=0.496). However, there was a positive,
albeit nonsignificant, trend between effective paternity fre-
quency and the survival (in months) of experimental colonies
(Fig. 2), where there was a nonlinear (logistic) effect of queen
mating number on how long her resultant colony survived
(r2 =0.046, P=0.06). Most importantly, colonies headed with
queens that had an effective mating of 7.0 or less were 2.86
times more likely to die by the end of this study when
compared to colonies headed by queens with an effective
paternity greater than 7.0 (Relative Risk (RR)=2.86; (95 %
CI 0.79–10.40); Fisher's exact test P<0.05).
Naturwissenschaften (2013) 100:723–728
Discussion
vanEngelsdorp et al. (2008) report the survey results from
305 beekeeping operations in the US accounting for 13.3 %
of the managed honey bee colonies nationwide. In that
survey, beekeepers self-reported that starvation (28 %),
varroa mites (24 %), and symptoms consistent with Colony
Collapse Disorder (9 %) were significant suspected factors
in colony losses. However, the primary perceived problem
for beekeepers was “poor queens” (31 %). Arguably, the
single most important attribute of a queen's “quality” is how
well she is mated. Previous findings suggest that most
commercially produced queens do not exhibit low mat-
ing frequencies (see also Delaney et al. 2011; Tarpy et
al. 2012), but our observed distinction between colonies
of low and high genetic diversity provides increased
emphasis on ensuring that beekeepers are provided with
sufficiently mated queens.
Neumann and Moritz (2000) correlated the mating num-
bers of queens and the levels of varroa mites in their colo-
nies, and they found no significant relationship between the
two. In the present study, we found a significant negative
nonlinear correlation between varroa and mating number
during 1 month's measurements, although this effect was
not persistent through the course of the study (Table 1).
Thus, while previous findings have shown strong effects
of manipulated genetic diversity on the prevalence of vari-
ous brood diseases (Palmer and Oldroyd 2003; Tarpy 2003;
Tarpy and Seeley 2006; Seeley and Tarpy 2007), it is
unclear if there is a similar relationship with adult parasites
at natural levels of genetic diversity.
Richard et al. (2007) showed that mating number affects
queen attractiveness to workers and their pheromone pro-
files. This suggests that supersedure rates might increase
with poorly mated queens (see also Niño et al. 2012). Our
data are not consistent with this prediction at natural mating
levels (as opposed to instrumentally inseminated queens
with artificially low mating numbers). In fact, we found a
negative correlation between effective paternity frequencies
of superseded queens and their survival. This potential as-
sociation is fairly enigmatic, and any inferences drawn from
it would be highly speculative, but it could suggest that there
are indirect costs to increased mating number such as sex-
ually transmitted diseases or trade-offs at different levels of
selection. For example, larger queens have a greater capac-
ity for sperm storage and mate with more drones and selec-
tively favored at the colony level, but larger queens may
also be selected against at the individual level by increased
susceptibility to disease or environmental contaminants.
Nonetheless, while the difference between single- versus
multiple-inseminated queens might show an effect on queen
physiology and attractiveness to workers, this does not
appear to translate to different rates of supersedure within
727
the range of naturally mated queens in active beekeeping
operations.
The theoretical threshold of effective paternity frequency
of 7.0 is somewhat arbitrary, as any other threshold could be
chosen for means of comparison. As Page (1980) noted, and
further expanded by Palmer and Oldroyd (2000) among
others, a mating frequency of 6 is the inflection point of
average intracolony relatedness (see Fig. 1). However, in the
current study, this cutoff point of 7 was found to be partic-
ularly relevant with respect to colony survival. It would be
interesting to verify if this level of genetic diversity holds
some bearing on other concrete, measureable phenotypes
such as disease prevalence or colony homeostasis.
In conclusion, we do not find consistently strong effects
of effective mating frequency on the specific measures of
colony health and productivity in honey bees managed in
commercial settings. However, we did detect a striking
effect of a threshold effective paternity frequency (me =7)
on overall colony survival. This suggests that, even in the
noisiest, least-controlled experimental environment (i.e.,
functioning migratory commercial beekeeping operations),
intracolony genetic diversity as a consequence of queen
multiple mating has a detectable and positive impact on
overall colony phenotype and longevity. Future efforts
should focus on the mechanism(s) by which this benefit is
manifest.
Acknowledgments We thank the three participating beekeepers for
their assistance in this project as well as Michael Andree, Karen
Roccasacca, Linda Wertz, and Nishit Patel and Nathan Rice for help
in collecting and processing samples. We would like to thank Joel
Caren, John Harman, Deborah Delaney, Winnie Lee, Flora Lee,
Mithun Patel, and Matt Mayer for their help in DNA extractions and
PCR analyses. This study was supported by the National Research
Initiative of the USDA Cooperative State Research, Education and
Extension Service, grant number 2007–02281, USDA-ARS as well
as by grants from the North Carolina Department of Agriculture and
Consumer Services and the National Honey Board.
References
Biesmeijer JC, Roberts SPM et al (2006) Parallel declines in pollina-
tors and insect-pollinated plants in Britain and the Netherlands.
Science 313(5785):351–354
Boomsma JJ, Ratnieks FL (1996) Paternity in eusocial Hymenoptera.
Philos Trans R Soc Lond B 351:947–975
Delaney DA, Keller JJ et al (2011) The physical, insemination, and
reproductive quality of honey bee queens (Apis mellifera).
Apidologie 42:1–13
Estoup A, Solignac M et al (1994) Precise assessment of the number of
patrilines and of genetic relatedness in honeybee colonies. Proc R
Soc Lond B 258:1–7
Estoup A, Garnery L et al (1995) Microsatellite variation in honey bee
(Apis mellifera L.) populations: hierarchical genetic structure and
test of the infinite allele and stepwise mutation models. Genetics
140:679–695
728
Fuchs S, Schade V (1994) Lower performance in honeybee colonies of
uniform paternity. Apidologie 25(2):155–168
Gallai N, Salles JM et al (2009) Economic valuation of the vulnerabil-
ity of world agriculture confronted with pollinator decline. Ecol
Econ 68(3):810–821
Harpur BA, Minaei S et al (2012) Management increases genetic
diversity of honey bees via admixture. Mol Ecol 21(18):4414–
4421
Jones JC, Myerscough MR et al (2004) Honey bee nest thermoregula-
tion: diversity promotes stability. Science 305(5682):402–404
Linksvayer TA, Fondrk MK et al (2009) Honeybee social regulatory
networks are shaped by colony-level selection. Am Nat 173(3):
E99–E107
Mattila HR, Seeley TD (2007) Genetic diversity in honey bee colonies
enhances productivity and fitness. Science 317(5836):362–364
National Research Council (2007) Status of pollinators in North
America. National Academy of Sciences, Washington, D.C
Neumann P, Moritz RFA (2000) Testing genetic variance hypotheses
for the evolution of polyandry in the honeybee (Apis mellifera L.).
Insect Soc 47(3):271–279
Nielsen R, Tarpy DR et al (2003) Estimating effective paternity num-
ber in social insects and the effective number of alleles in a
population. Mol Ecol 12(11):3157–3164
Niño EL, Malka O et al (2012) Effects of honey bee (Apis mellifera L.)
queen insemination volume on worker behavior and physiology. J
Insect Physiol 58:1082–1089
Oldroyd BP (2012) Domestication of honey bees was associated with
expansion of genetic diversity. Mol Ecol 21(18):4409–4411
Oldroyd BP, Fewell JH (2007) Genetic diversity promotes homeostasis
in insect colonies. Trends Ecol Evol 22(8):408–413
Oldroyd BP, Rinderer TE et al (1992) Effects of intracolonial genetic
diversity on honey bee (Hymenoptera: Apidae) colony perfor-
mance. Ann Entomol Soc Am 85:335–343
Page RE Jr (1980) The evolution of multiple mating behavior by honey
bee queens (Apis mellifera). Genetics 96(1):263–273
Palmer KA, Oldroyd BP (2000) Evolution of multiple mating in the
genus Apis. Apidologie 31(2):235–248
Palmer KA, Oldroyd BP (2003) Evidence for intra-colonial genetic
variance in resistance to American foulbrood of honey bees (Apis
mellifera): further support for the parasite/pathogen hypothesis for
the evolution of polyandry. Naturwissenschaften 90(6):265–268
Richard F-J, Tarpy DR, Grozinger CM (2007) Effects of Insemination
Quantity on Honey Bee Queen Physiology. PLoS ONE 2(10):
e980. doi:10.1371/journal.pone.0000980
Seeley TD, Tarpy DR (2007) Queen promiscuity lowers disease within
honeybee colonies. Proc R Soc B Biol Sci 274(1606):67–72
View publication stats
Naturwissenschaften (2013) 100:723–728
Solignac M, Vautrin D et al (2003) Five hundred and fifty microsatel-
lite markers for the study of the honeybee (Apis mellifera L.)
genome. Mol Ecol Notes 3(2):307–311
Tarpy DR (2003) Genetic diversity within honeybee colonies prevents
severe infections and promotes colony growth. Proc R Soc Lond
Ser B 270(1510):99–103
Tarpy DR, Nielsen DI (2002) Sampling error, effective paternity, and
estimating the genetic structure of honey bee colonies
(Hymenoptera: Apidae). Ann Entomol Soc Am 95(4):513–528
Tarpy DR, Page RE Jr (2002) Sex determination and the evolution of
polyandry in honey bees (Apis mellifera). Behav Ecol Sociobiol
52(2):143–150
Tarpy DR, Seeley TD (2006) Lower disease infections in honeybee
(Apis mellifera) colonies headed by polyandrous vs. monandrous
queens. Naturwissenschaften 93(4):195–199
Tarpy DR, Nielsen R et al (2004) A scientific note on the revised
estimates of effective paternity frequency in Apis. Insect Soc
51(2):203–204
Tarpy DR, Caren JR et al (2010) Mating frequencies of Africanized
honey bees in the south western USA. J Apic Res 49(4):302–
310
Tarpy DR, Keller JJ et al (2012) Assessing the mating “health” of
commercial honey bee queens. J Econ Entomol 105(1):20–25
vanEngelsdorp D, Evans JD, Saegerman C, Mullin C, Haubruge E,
Nguyen BK, Frazier M, Frazier J, Cox-Foster D, Chen Y,
Underwood R, Tarpy DR, Pettis JS (2009) Colony Collapse
Disorder: A Descriptive Study. PLoS ONE 4(8):e6481. doi:10.1371/
journal.pone.0006481
vanEngelsdorp D, Lengerich E et al (2013b) Standard methods for Apis
mellifera pest and pathogen research. J Apic Res 51: doi:10.3896/
IBRA.1.51.5.08
vanEngelsdorp D, Meixner MD (2010) A historical review of
managed honey bee populations in Europe and the United
States and the factors that may affect them. J Invertebr
Pathol 103:S80–S95
vanEngelsdorp D, Hayes J et al (2008) A survey of honey bee colony
losses in the U.S., fall 2007 to spring 2008. PLoS One. doi:10.1371/
journal.pone.0004071
vanEngelsdorp D, Tarpy DR et al (2013) Idiopathic brood disease
syndrome and queen events as precursors of colony mortality in
migratory beekeeping operations in the Eastern United States.
Prev Vet Med 108:225–233
Wang JL (2004) Sibship reconstruction from genetic data with typing
errors. Genetics 166(4):1963–1979
Winston ML (1987) The biology of the honey bee. Harvard University
Press, Cambridge