Molecular Ecology (2013) 22, 3208–3210
NEWS AND VIEWS
COMMENT
Conserving genetic diversity in the
honeybee: Comments on Harpur et al.
(2012)
A,* RODOLFO JAFFE
,†‡
PILAR DE LA RU
~
IRENE MUNOZ,* JOSE SERRANO,* ROBIN
F . A . M O R I T Z § ¶ and F . B E R N H A R D K R A U S §
*Dpto. de Zoologıa y Antropologıa Fısica, Facultad de
Veterinaria, Universidad de Murcia, 30100 Murcia, Spain;
†Instituto de Bioci^encias, Universidade de S~ao Paulo, Rua do
Mat~ao 321, 05508-900 S~ao Paulo-SP, Brazil; ‡Departamento
de Ci^encias Animais, Universidade Federal Rural do Semiarido,
Av. Francisco Mota, 572, Bairro Costa e Silva, 59625-900
Mossoro-RN, Brazil; §Molecular Ecology Research Group,
Institute of Biology, Martin Luther University, Halle-Wittenberg,
Hoher Weg 4, 06120 Halle (Saale), Germany; ¶Romanian Center
for Bee Biotechnology, University of Agricultural and
Veterinarian Sciences, Calea Manastur 3-5, 400372 Cluj-Napoca,
Romania
Abstract
The article by Harpur et al. (2012) ‘Management increases
genetic diversity of honey bees via admixture’ concludes
that ‘…honey bees do not suffer from reduced genetic
diversity caused by management and, consequently, that
reduced genetic diversity is probably not contributing to
declines of managed Apis mellifera populations’. In the
light of current honeybee and beekeeping declines and their
consequences for honeybee conservation and the pollination
services they provide, we would like to express our concern
about the conclusions drawn from the results of Harpur
et al. (2012). While many honeybee management practices
do not imply admixture, we are convinced that the largescale genetic homogenization of admixed populations could
drive the loss of valuable local adaptations. We also point
out that the authors did not account for the extensive gene
flow that occurs between managed and wild/feral honeybee populations and raise concerns about the data set used.
Finally, we caution against underestimating the importance of genetic diversity for honeybee colonies and highlight the importance of promoting the use of endemic
honeybee subspecies in apiculture.
Keywords: admixture, Apis mellifera, beekeeping, honeybee
conservation
Correspondence: Pilar De la R
ua, Fax: 0034868884906;
E-mail: pdelarua@um.es
Received 5 October 2012; revised 25 January 2013; accepted
2 February 2013
The study by Harpur et al. (2012) measures the degree of
admixture of honeybee populations (Apis mellifera)
exposed to different levels of management. However,
management of honeybees does not necessarily mean
admixture, as many beekeepers around the world exclusively breed bees native to their areas or have long-term
breeding and conservation programmes aiming at avoiding admixture between managed and feral bees (Chapman
et al. 2008; Bouga et al. 2011). Although the authors state
that ‘Management by beekeepers has allowed for honey
bees to admix and produce ‘mongrel’ populations of
greater diversity than that of their progenitors…’, management has also been shown to reduce or at least not to
alter genetic diversity in honeybee populations (see De la
R
ua et al. 2009 and references therein). Central European
populations, for example, are heavily admixed between
the endemic Apis mellifera mellifera and introduced Apis
mellifera carnica from Eastern Europe, a completely different biogeographic lineage (Jensen et al. 2005; Soland-Reckeweg et al. 2009; Rortais et al. 2011). However, Harpur
et al. detected only a low admixture in these populations.
A recent study carried out on Tenerife (Canary Islands)
found that continuous introduction of foreign honeybee
subspecies does not increase genetic diversity of the local
population (Mu~
noz et al. 2012). On another Canary Island
(La Palma), a conservation programme has not affected
genetic diversity of the local bee population, showing that
efforts to select queens with particular mitochondrial haplotypes do not necessarily increase genetic diversity
(Mu~
noz & De la R
ua 2012). Other beekeeping practices,
such as large-scale queen breeding, have also caused a
notorious reduction in genetic diversity in Italian honeybee populations (see Dall’Olio et al. 2007 and references
therein). More importantly, Harpur et al.’s study (2012)
and other studies (Jaffe et al. 2010) found that African
populations harbour the highest genetic diversity, a result
that in our view contradicts the main conclusion of the
study, because Africa hosts a large wild honeybee population with little or no exposure to management practices
(Dietemann et al. 2009).
Whereas we agree that admixture can enhance local
genetic diversity on the short term, it is prudent to acknowledge that it can also lead to a large-scale genetic homogenization of the admixed population and a subsequent loss of
local adaptations. In other words, admixture and gene flow
have caused an increase in within-population variation and
heterozygosity and at the same time, a decrease in amongpopulation variation. This effect is clearly illustrated by the
high population differentiation found among ‘progenitor’
populations (FST > 0.51) compared with the lack of population
© 2013 John Wiley & Sons Ltd
N E W S A N D V I E W S : C O M M E N T 3209
differentiation among managed populations (FST ~ 0).
Admixture will inevitably eliminate the variance among
endemic honeybee subspecies, which, in spite of apiculture,
still occurs throughout Europe (De la R
ua et al. 2009). Native
subspecies are important reservoirs of local adaptations,
ultimately determining the survival and pollination success
of honeybees in the wild. Their extinction thus implies the
loss of a valuable combination of traits shaped by natural
selection over extended periods of time.
Deliberate crossing and the use of non-native honeybees in beekeeping promote the creation of admixed
populations, which introgress into native populations.
The resulting hybrid bees may indeed have a higher
genetic diversity, but will also have lost the combination
of traits, long-shaped by natural selection, that made
them particularly well adapted to their local environment
(Strange et al. 2007; Costa et al. 2012). It is therefore
important to highlight that such beekeeping practices are
detrimental to the conservation of the genetic identity of
endemic honeybee subspecies. This should be kept in
mind by bee breeders that routinely mix different honeybee subspecies to create arguably better bees, following the
aims of the Brother Adam (2000). The following statement
made by Harpur et al. (2012) exactly justifies such breeding
practices: ‘Beekeepers may be, intentionally or unintentionally, selecting hybrid colonies, which tend to have higher
fitness at some colony-level traits’. We believe this statement
is not correct, as most colony traits used for bee breeding
(i.e. colour, posture, swarming behaviour, aggression and
hygienic behaviour, to name a few) are not associated
with hybrid bees at all. Moreover, we believe this statement is misleading, because it promotes the use of hybrid
bees without taking into consideration the negative effects
of it.
Another flawed point in Harpur et al. (2012) is the fact
that the authors fail to account for the extensive gene flow
that occurs between managed and wild/feral honeybee
populations. Although it is true that ‘reduced genetic
diversity is a common feature of domesticated animal and
plant populations (Bruford et al. 2003)’, the authors failed
to mention that honeybees are not fully domesticated animals. In spite of centuries of beekeeping, endemic subspecies-specific genetic footprints can still be identified in
Europe (Jensen et al. 2005; C
anovas et al. 2008; Mu~
noz et al.
2009, 2012; Rortais et al. 2011; Pinto et al. 2012) and Africa
(Dietemann et al. 2009; El-Niweiri & Moritz 2010; Chahbar
et al. 2013), which is exactly why conservation efforts are
meaningful and necessary. Although professional bee
breeders may aim at domestication, the notorious problems
in achieving controlled mating are a huge handicap.
Queens mate in flight typically with uncontrolled drones,
and only few breeders can afford strict control measures
using islands as mating stations or instrumental insemination. In consequence, extensive gene flow usually occurs
between wild/feral and managed honeybee populations,
making the distinction of ‘progenitor’ from ‘managed’ populations difficult. For instance, the authors did find admixture in the ‘progenitor’ populations and hence ‘excluded
© 2013 John Wiley & Sons Ltd
progenitor bees with admixture levels of 10% or greater’ in
subsequent analyses.
An additional weakness of Harpur et al. (2012) is, in our view,
the data set used. While the East European ‘progenitor’ group
is composed of samples from nine colonies (from Germany,
Croatia and Slovenia), the West European ‘progenitor’ group
has 12 (from Poland and Spain). Hence, the ‘progenitor’
groups do not reflect geography, as Poland (grouped in the
West European group) is located east of Germany (grouped
in the East European group). No clarification about this
grouping is given by the authors. In addition, the African
group consists of samples from a single South African subspecies (A. m. scutellata); the managed population from
North America consists of samples from nine colonies from
Ontario, Canada; and the managed population from Europe
consists of samples from six colonies from two locations in
France. We therefore doubt that continent-wide generalizations can be made with this sample set. In the light of the
high diversity of honeybee subspecies occurring throughout
Europe and Africa, we believe that a more exhaustive analyses, employing the same methods as those used by Harpur
et al. (2012) but analysing a more comprehensive data set
(including at least the main European and African subspecies and replicated wild and managed populations), could
yield very different results.
Finally, we would also like to mention that the claim ‘…
reduced genetic diversity is probably not contributing to
declines of managed Apis mellifera populations’ ignores a
substantial body of literature showing the importance of
genetic diversity for social insect colonies. High genetic
diversity has been suggested to increase productivity and
broaden tolerance to environmental changes (Mattila &
Seeley 2007; Oldroyd & Fewell 2007), increase resistance to
pathogens (Schmid-Hempel 1998; Seeley & Tarpy 2007)
and improve task performance through a more efficient
division of labour (Smith et al. 2008). Furthermore, a reduction in genetic diversity at the population level would
increase the risk of inbreeding and diploid male production, with potentially disastrous consequences for honeybee
colonies (Cook & Crozier 1995; Harpur et al. 2013). We
should keep in mind that colony losses (resulting from
CCD and similar phenomena) have primarily occurred in
managed populations (Ellis et al. 2010; Potts et al. 2010a,b;
Dainat et al. 2012), but not at all in wild African populations or feral Africanized populations of South and North
America (Dietemann et al. 2009; Vandame & Palacio 2010;
Moritz et al. 2013). These bees have a higher reproduction
rate and a superior resistance to deadly bee pathogens
such as the Varroa mite. Furthermore, recent work carried
out by colleagues in Europe has shown that local bees have
a higher survival and productivity when compared to
introduced bees living in the same apiary (Costa et al.
2012). These findings thus highlight the importance of preventing the mixing of different honeybee subspecies and
more strongly foster the use of endemic honeybee subspecies in apiculture, a strategy that in our view will turn out
to a win-win situation for both in apiculture and
conservation.
3210 N E W S A N D V I E W S : C O M M E N T
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P.R. and I.M. belong to the Evolution and Animal Phylogeny
Research Group at the University of Murcia headed by J.S., R.J.
is a FAPESP postdoctoral fellow at the University of S~
ao Paulo.
F.B.K. is postdoctoral researcher at the Molecular Ecology
Research Group, Martin Luther University, Halle-Wittenberg.
R.F.A.M. is the head of this group. Their main lines of research
include population ecology, population genetics and conservation of insects, including honeybees, stingless bees and bumblebees.
doi: 10.1111/mec.12333
© 2013 John Wiley & Sons Ltd