The Darwin cure for apiculture? Natural selection and managed honey bee health

Abstract

Recent major losses of managed honeybee, Apis mellifera, colonies at a global scale have resulted in a multitude of research efforts to identify the underlying mechanisms. Numerous factors acting singly and/or in combination have been identified, ranging from pathogens, over nutrition to pesticides. However, the role of apiculture in limiting natural selection has largely been ignored. This is unfortunate, because honeybees are more exposed to environmental stressors compared to other livestock and management can severely compromise bee health. Here, we briefly review apicultural factors that influence bee health and focus on those most likely interfering with natural selection, which offers a broad range of evolutionary applications for field practice. Despite intense breeding over centuries, natural selection appears to be much more relevant for the health of managed A. mellifera colonies than previously thought. We conclude that sustainable solutions for the apicultural sector can only be achieved by taking advantage of natural selection and not by attempting to limit it.

Full text

Evoluonary Applicaons 2016; 1–5
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wileyonlinelibrary.com/journal/eva
Received: 3 June 2016
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Accepted: 6 November 2016
DOI: 10.1111/eva.12448
PERSPECTIVE
The Darwin cure for apiculture? Natural selecon and managed
honeybee health
Abstract
Recent major losses of managed honeybee, Apis mellifera, colonies at a
global scale have resulted in a multude of research eorts to idenfy
the underlying mechanisms. Numerous factors acng singly and/or in
combinaon have been idened, ranging from pathogens, over nu-
trion to pescides. However, the role of apiculture in liming natu-
ral selecon has largely been ignored. This is unfortunate, because
honeybees are more exposed to environmental stressors compared
to other livestock and management can severely compromise bee
health. Here, we briey review apicultural factors that inuence bee
health and focus on those most likely interfering with natural selec-
on, which oers a broad range of evoluonary applicaons for eld
pracce. Despite intense breeding over centuries, natural selecon
appears to be much more relevant for the health of managed A. mel-
lifera colonies than previously thought. We conclude that sustainable
soluons for the apicultural sector can only be achieved by taking ad-
vantage of natural selecon and not by aempng to limit it.
1 | INTRODUCTION
The western honeybee, Apis mellifera, is one of the most economically
important insects, providing essenal pollinaon services for human
food security as well as valuable hive products for the apicultural sec-
tor (Klein et al., 2007; Morse & Calderone, 2000). Therefore, major
losses of managed A. mellifera colonies at a global scale (e.g., van
Engelsdorp & Meixner, 2010; vanEngelsdorp, Hayes Jr., Underwood,
Caron, & Pes 2011; Neumann & Carreck, 2010; Pirk, Human, Crewe,
& vanEngelsdorp, 2014) have resulted in a multude of naonal and
internaonal research eorts to idenfy underlying mechanisms
(Moritz et al., 2010; Pos et al., 2011; Vanbergen et al., 2012; among
many others). Numerous factors acng singly and/or in combinaon
have been idened, ranging from pathogens, over nutrion to pes-
cides (see Pos et al., 2010 for an overview). However, the role of
apiculture as another stressor has received far less aenon, although
management can severely compromise bee health. In parcular, the
role of common beekeeping pracces in liming natural selecon as a
potenal major factor governing managed honeybee health has been
completely ignored so far. This is kind of surprising, because it is well
known that honeybees are more exposed to environmental stressors
compared to other livestock. As natural selecon is the key mechanism
of evoluon, it will enable any given stock of managed honeybees,
irrespecve of habitat (agro- ecosystems, nature reserves, etc.) and/or
genec background (endemic, imported, “pure” breeding lines, hybrids
[e.g., Buckfast], etc.) to adapt to each and every stressor as long as
the ability to cope with the stressor has a genec basis so that the
respecve heritable traits can change in this populaon over me.
Although domescaon always interferes by denion with natural
selecon and apicultural selecon has existed for decades, if not cen-
turies (Crane, 1999), we here argue that beekeeping interference with
natural selecon in combinaon with globalizaon of industrialized
apiculture may have now reached levels, where ill eects are inevita-
ble at the colony level. Such ill eects have previously and repeatedly
been reported in populaons of managed honeybees (see review by
van Engelsdorp & Meixner, 2010), but the role of natural selecon has
not been considered in this regard. Even though comparisons with
historical data sets remain notoriously dicult, it appears as if the
factors compromising managed honeybee health may have reached
higher levels compared to the past (invasive pests, vectored viruses,
prophylacc pescide usage, starvaon, etc., reviewed by Pos et al.,
2010). Indeed, globally standardized survey data from the COLOSS
network over the past 8 years (www.coloss.org) suggest unsustainable
high losses repeatedly in many regions globally. Here, we therefore
briey review apicultural factors governing honeybee health and focus
on those probably interfering with natural selecon (Figure 1), which
oers a broad range of evoluonary applicaons for eld pracce.
It is evident that the beekeeper is the most crucial (mul)factor
driving managed honeybee health. Indeed, beekeepers play the key
role in spread as well as diagnosis and control of new and estab-
lished diseases (Munelli, 2011; Neumann, Pes, & Schäfer, 2016;
Rosenkranz, Aumeier, & Ziegelmann, 2010), for example, treang
against ectoparasic mites, Varroa destructor (Rosenkranz et al.,
2010), not only prevents host–parasite coevoluon, but may also add
to the exposure to pescides thereby possibly compromising colony
health (Boncrisani et al., 2012). In general, the high density of col-
onies at apiaries promotes disease transmission and impact (Seeley
& Smith, 2015) and the large hives compared to natural nests may
also have a detrimental impact on colony survival (Lous, Smith, &
Seeley, 2016). During roune colony inspecons, beekeepers fre-
quently break the natural propolis envelope of colonies, which may
This is an open access arcle under the terms of the Creave Commons Aribuon License, which permits use, distribuon and reproducon in any medium,
provided the original work is properly cited.
© 2016 The Authors. Evoluonary Applicaons published by John Wiley & Sons Ltd

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NEUMANN AND BLACQUIÈRE
compromise social immunity (Simone- Finstrom, Evans, & Spivak,
2009). Apiculture also governs bee nutrion, for example, by placing
staonary apiaries in areas with bad forage or by choosing the forage
for the bees in migratory beekeeping. The alternaon of honey/pol-
len ows with poor forage periods is indeed a challenge to the colo-
nies to adapt to normal seasonality (Bretagnolle & Gaba, 2015) and
may aect resilience to diseases. Replacing diverse honey stores with
low- quality sugar water may also impact health (Erler, Denner, Bobis,
Forsgren, & Moritz, 2014; Wheeler & Robinson, 2014), and unmely
and/or insucient feeding of honey- depleted colonies for overwin-
tering is an obvious key reason for mortality (vanEngelsdorp et al.,
2011). Finally, due to the potenal role of endosymbionts and the
enre associated microbiome of honeybees (Aebi & Neumann, 2011;
Engel et al., 2016), treatment of colonies with acaricides (Kakumanu,
Reeves, Anderson, Rodrigues, & Williams, 2016), anbiocs, and even
sugar feeding may interfere with natural populaon dynamics of such
associated prokaryotes. All these factors have received at least some
aenon for improving bee health in the past. However, the limita-
on of natural selecon by beekeepers has so far been ignored for
migaon measures.
While treatment against disease is helpful, it nevertheless prevents
natural selecon for improved host resistance and tolerance (Fries &
Bommarco, 2007; Råberg, Graham, & Read, 2009). In parcular, the
common pracce of removing male sexuals (=drone brood) to con-
trol V. destructor (Rosenkranz et al., 2010), basically castrates colonies,
thereby prevenng that well- adapted ones spread their genes in the
populaon. This seems signicant because recent evidence suggests
substanal local adaptaons of honeybees enhancing colony survival
(Büchler et al., 2014) and reducing pathogen loads (Francis et al.,
2014). In this regard, the situaon in Europe is dierent to areas,
in which European honeybees have been imported. Indeed, several
local subspecies can be dierenated in Europe using morphometric
or genec makers (Miguel, Iriondo, Garnery, Sheppard, & Estonba,
2007; Miguel et al., 2011; Runer, 1988). The compeon of intro-
duced honeybees with such endemic honeybees and other pollinators
is plausible (see Moritz, Härtel, & Neumann, 2005; for a review), but
this is not a focus of this arcle. Indeed, we here argue about natural
selecon and managed honeybee health and not about conservaon
of endangered honeybee subspecies. Clearly, each honeybee subspe-
cies deserves to be protected in its own rights and local adaptaons
are most likely (e.g., endemic A. m. mellifera in France, Strange, Garnery,
& Sheppard, 2007). We cannot and do not want to queson this ob-
vious nature conservaon issue, especially because adapted traits of
endemic subspecies may be lost due to introgression of foreign ones
(Meixner et al., 2010). However, the well- jused ongoing nature con-
servaon eorts (mainly in Europe) and our suggeson to take advan-
tage of natural selecon to improve the health of managed honeybee
colonies globally are basically two dierent things. For a funconal
global apiculture, the health of any given colony seems to be more
relevant than conservaon eorts for specic subspecies in Europe or
elsewhere. This is especially true, because there are nowadays more
managed colonies of European honeybees outside of Europe than in
Europe itself (FAO data: hp://faostat.fao.org/). For example, suscep-
bility to infecon by the endoparasic microsporidian Nosema cer-
anae is not linked to honeybee taxa, but results from the variability
between colonies, and those dierences are probably linked to genec
variaons (Fontbonne et al., 2013).
These genotype–environment interacons, including immuno-
priming of eggs by the queen in response to pathogens in the hive
(Salmela, Amdam, & Freitak, 2015), are rounely and constantly dis-
rupted when queens or colonies are moved over large distances, for
example, from Southern Italy to Finland, as part of internaonal api-
cultural trade. Indeed, the industrial producon of tens of thousands
of queens annually, which are nowadays exported at a connental and
even global scale (Lodesani & Costa, 2003), clearly interferes with any
local adaptaons. Therefore, “think globally, but breed locally” appears
an adequate suggeson for honeybee breeders to take advantage of
natural selecon and to foster local adaptaons.
In arcial inseminaon, breeders choose drones (=male sexuals)
of the right age, which obviously have not made it yet to drone con-
gregaon areas and may thus not have the full reproducve potenal.
At isolated mang apiaries, only few drone- producing colonies are
provided, which are oen headed by sister queens, thereby clearly
liming the full potenal of the highly polyandrous mang system of
honeybees to generate subfamilies with ample genotypic diversity and
respecve derived benets (Oldroyd & Fewell, 2007; Mala & Seeley,
2007; Tarpy, vanEngelsdorp, & Pes, 2013). The equal number of mat-
ings of wild and managed queens (Tarpy, Delaney, & Seeley, 2015)
suggests that the system has evolved to provide opmal genec vari-
aon of colonies, but will fail to deliver with closer genec similarity
of the drones and reduced mate numbers. A recent study showed that
honeybee colonies, which were made hyperpolyandrous arcially
(30 or 60 mangs), had improved performance (Delaplane, Pietravalle,
Brown, and Budge (2015), thereby suggesng that genec diversity
of A. mellifera has already been lost and thus drone mates may be too
genecally similar by now.
The buildup of a stable host–parasite relaonship is strongly fa-
vored by vercal transmission of the parasite (Fries & Camazine, 2001)
and is unlikely to occur when horizontal transmission is the predom-
inant route (Schmid- Hempel, 2011). Indeed, shis from vercal to
FIGURE1 Apiculture and natural selection as a joint framework
for the health of managed honeybee colonies. Specific beekeeping
methods, which are likely to interfere with natural selection (=orange
area), and possible impact on natural selection (=green area) are
shown with an ongoing colony inspection in the center

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NEUMANN AND BLACQUIÈRE
horizontal transmission are known to increase pathogen virulence
(Woolhouse, Haydon, & Ana, 2005). However, the common pracce
in commercial beekeeping in most countries to rounely requeen col-
onies annually or every 2 years limits the full adapve potenal of ver-
cal transmission. Aer requeening, parasites are confronted not only
with an enrely new queen genotype, but also with novel genotypes
of the drones, the queens have mated with (assuming natural queen
mang at apiaries and unrelated drone/queen sources). This may have
caused shis from vercal to horizontal transmission with respecve
consequences for the virulence of honeybee parasites.
Commercial breeders select against swarming, defensive behavior,
and propolis usage, thereby probably compromising colony defense
and social immunity (Meunier, 2015). Indeed, in Africa, where the
majority of honeybee colonies are not kept by man and where bee-
keepers are mostly side users not interfering with natural swarm-
ing, queen rearing etc., the virtually nonbred local subspecies have
less desirable beekeeping traits, but a superior health compared to
European ones (Pirk, Strauss, Yusuf, Démares, & Human, 2016). This
supports the noon of a trade- o scenario between commercially
desired traits and bee health. In parcular, queen failure is one of the
foremost menoned causes of honeybee losses (vanEngelsdorp et al.,
2011; Pes, Rice, Joselow, vanEngelsdorp, & Chaimanee, 2016) and
may also be linked to breeding, because queen breeders usually ig-
nore choices made by colonies and choose larvae based on right age
alone. The natural reproducve cycle of a colony, incl. hormonal and
nutrional aspects, determines ming and development of drones and
new queens and oen lays outside of the me window for commercial
queen rearing. Moreover, during emergency queen rearing, the choice
of the bees is not at random; instead, subfamilies, which are rare in the
work force, are signicantly more likely to end up as queens (Moritz
et al., 2005). As such royal subfamilies are rare, human choice of lar-
vae based on appropriate age alone is likely to miss those and instead
oers only subopmal choices for the bees. Moreover, breeding for V.
destructor- resistance over >20 years has sll not resulted in survival of
untreated colonies, but natural selecon has delivered mulple mes
(Locke, 2016; Rosenkranz et al., 2010), thereby suggesng that breed-
ers should choose traits favored by natural selecon. This suggests
fundamental conceptual aws in both commercial honeybee queen
rearing and breeding. As the tness of a honeybee colony clearly is
the number of surviving swarms as well as the number of successfully
mang drones (all other traits are only tokens of tness), the selecon
by beekeepers for low swarming tendency of colonies and removal of
drone brood, mainly to combat mites V. destructor, remain probably
the key factors in liming natural selecon.
There is amplitude of hypothesis- driven research avenues to test
our claims. For example, the possible role of subopmal choices made
by queen breeders for the recent queen- related problems (vanEngels-
dorp et al., 2011; Pes et al., 2016) could be invesgated by compar-
ing the performance of honeybee queens natural chosen by the bees
themselves with graed ones in populaons, which sll have ample
genec diversity (e.g., in Africa). Similarly, given that natural selecon
plays the key role for survival of otherwise deadly V. destructor mite
infestaons, the famous “Bond experiment” (Locke & Fries, 2011)
conducted in other countries should almost always result in at least
some surviving colonies.
2 | CONCLUSIONS
It is obvious that taking into account natural selecon will not solve
all of the various problems for apiculture, but instead we consider it
to be a main issue in itself at the moment. As natural selecon is the
dierenal survival and reproducon of individuals due to dierences
in phenotype, future eorts to enhance managed honeybee health
should take into account the central role of apiculture in liming natu-
ral selecon and compromising colony health via adjusted keeping and
breeding of local bees. Here lies a great opportunity for beekeeping in
several countries, where economic constraints are no longer leading
as beekeeping has become a hobby sector, with dispersed and small
apiaries being the rule. Sustainable soluons for the apicultural sector
can only be achieved by taking advantage of natural selecon and not
by aempng to limit it.
ACKNOWLEDGEMENTS
PN acknowledges the Vinetum foundaon and TB the Dutch Ministry
of Economic Aairs (Project BO 20- 003- 023) for nancial support.
DATA ARCHIVING STATEMENT
We will not be archiving data because this manuscript does not have
associated data.
Keywords
Apis mellifera, beekeeping, honeybee, natural selecon
Peter Neumann1
Tjeerd Blacquière2
1Instute of Bee Health, Vetsuisse Faculty, University of Bern, Bern,
Switzerland
2Bees@wur, Bio-interacons and Plant Health, Wageningen UR,
Wageningen, The Netherlands
Correspondence
Peter Neumann, Instute of Bee Health, Vetsuisse Faculty, University of
Bern, Bern, Switzerland.
Email: peter.neumann@vetsuisse.unibe.ch
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