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: [email protected]
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 References Adam B (2000) In Search of the Best Strains of Bees. Peacock Press, Texas. Bouga M, Alaux C, Bienkowska M et al. (2011) A review of methods for discrimination of honey bee populations as applied to European beekeeping. Journal of Apicultural Research, 50, 51–84. Bruford MW, Bradley DG, Luikart G (2003) DNA markers reveal the complexity of livestock domestication. Nature Reviews: Genetics, 4, 900–910. C anovas F, De la R ua P, Serrano J, Galian J (2008) Geographic patterns of mitochondrial DNA variation in Apis mellifera iberiensis (Hymenoptera: Apidae). Journal of Zoological Systematics and Evolutionary Research, 46, 24–30. Chahbar N, Mu~ noz I, Dall’Olio R, De la R ua P, Serrano J, Doumandji S (2013) Population structure of North African honey bees is influenced by both biological and anthropogenic factors. Journal of Insect Conservation, 17, 385–392. Chapman NC, Lim J, Oldroyd BP (2008) Population genetics of commercial and feral honey bees in Western Australia. Journal of Economic Entomology, 101, 272–277. Cook JM, Crozier RH (1995) Sex determination and population biology in the Hymenoptera. Trends in Ecology & Evolution, 10, 281–286. Costa C, Lodesani M, Bienefeld K (2012) Differences in colony phenotypes across different origins and locations: evidence for genotype by environment interactions in the Italian honeybee (Apis mellifera ligustica)? Apidologie, 43, 634–642. Dainat B, Evans JD, Chen YP, Gauthier L, Neumann P (2012) Predictive markers of honey bee colony collapse. PLoS ONE, 7, e32151. Dall’Olio R, Marino A, Lodesani M, Moritz RFA (2007) Genetic characterization of Italian honeybees, Apis mellifera ligustica, based on microsatellite DNA polymorphisms. Apidologie, 38, 207– 217. De la R ua P, Jaffe R, Dall’Olio R, Mu~ noz I, Serrano J (2009) Biodiversity, conservation and current threats to European honeybees. Apidologie, 40, 263–284. Dietemann V, Pirk CWW, Crewe R (2009) Is there a need for conservation of honeybees in Africa? Apidologie, 40, 285–295. Ellis JD, Evans JD, Pettis J (2010) Colony losses, managed colony population decline, and Colony Collapse Disorder in the United States. Journal of Apicultural Research, 49, 134–136. El-Niweiri MAA, Moritz RFA (2010) The impact of apiculture on the genetic structure of wild honeybee populations (Apis mellifera) in Sudan. Journal of Insect Conservation, 14, 115–124. Harpur BA, Minaei S, Kent CF, Zayed A (2012) Management increases genetic diversity of honey bees via admixture. Molecular Ecology, 21, 4414–4421. Harpur BA, Sobhani M, Zayed A (2013) A review of the consequences of complementary sex determination and diploid male production on mating failures in the Hymenoptera. Entomologia Experimentalis et Applicata, 146, 156–164. Jaffe R, Dietemann V, Allsopp MH et al. (2010) Estimating the density of honeybee colonies across their natural range to fill the gap in pollinator decline censuses. Conservation Biology, 24, 583– 593. Jensen AB, Palmer KA, Boomsma JJ, Pedersen BV (2005) Varying degrees of Apis mellifera ligustica introgression in protected populations of the black honeybee, Apis mellifera mellifera, in northwest Europe. Molecular Ecology, 14, 93–106. Mattila HR, Seeley TD (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science, 317, 362–364.
Moritz RFA, Kraus FB, Huth-Schwarz A et al. (2013) Number of honeybee colonies in areas with high and low beekeeping activity in Southern Mexico. Apidologie, 44, 113–120. Mu~ noz I, De la R ua P (2012) Temporal analysis of the genetic diversity in a honey bee mating area of an island population (La Palma, Canary Islands, Spain). Journal of Apicultural Science, 55, 141–148. Mu~ noz I, Dall′Olio R, Lodesani M, De la R ua P (2009) Population genetic structure of coastal Croatian honeybees (Apis mellifera carnica). Apidologie, 40, 617–626. Mu~ noz I, Madrid-Jimenez MJ, De la R ua P (2012) Temporal genetic analysis of an introgressed island honey bee population (Tenerife, Canary Islands, Spain). Journal of Apicultural Research, 51, 144–146. Oldroyd BP, Fewell JH (2007) Genetic diversity promotes homeostasis in insect colonies. Trends in Ecology & Evolution, 22, 408–413. Pinto MA, Mu~ noz I, Ch avez-Galarza J, De la R ua P (2012) The Atlantic side of the Iberian Peninsula: a hot-spot of novel African honey bee maternal diversity. Apidologie, 43, 663–673. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010a) Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution, 25, 345–353. Potts SG, Roberts SPM, Dean R et al. (2010b) Declines of managed honey bees and beekeepers in Europe. Journal of Apicultural Research, 49, 15–22. Rortais A, Arnold G, Alburaki M, Legout H, Garnery L (2011) Review of the DraI COI–COII test for the conservation of the black honeybee (Apis mellifera mellifera). Conservation Genetics Resources, 3, 383–391. Schmid-Hempel P (1998) Parasites in Social Insects. Princeton University Press, Princeton. Seeley TD, Tarpy DR (2007) Queen promiscuity lowers disease within honeybee colonies. Proceedings of the Royal Society of London B Biological Sciences, 274, 67–72. Smith CR, Toth AL, Suarez AV, Robinson GE (2008) Genetic and genomic analyses of the division of labour in insect societies. Nature Reviews: Genetics, 9, 735–748. Soland-Reckeweg G, Heckel G, Neumann P, Fluri P, Excoffier L (2009) Gene flow in admixed populations and implications for the conservation of the Western honey bee, Apis mellifera. Journal of Insect Conservation, 13, 317–328. Strange JP, Garnery L, Sheppard WS (2007) Persistence of the Landes ecotype of Apis mellifera mellifera in southwest France: confirmation of a locally adaptive annual brood cycle trait. Apidologie, 38, 259–267. Vandame R, Palacio M (2010) Preserved honey bee health in Latin America: a fragile equilibrium due to low-intensity agriculture and beekeeping? Apidologie, 41, 243–255.
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
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: [email protected]
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 References Adam B (2000) In Search of the Best Strains of Bees. Peacock Press, Texas. Bouga M, Alaux C, Bienkowska M et al. (2011) A review of methods for discrimination of honey bee populations as applied to European beekeeping. Journal of Apicultural Research, 50, 51–84. Bruford MW, Bradley DG, Luikart G (2003) DNA markers reveal the complexity of livestock domestication. Nature Reviews: Genetics, 4, 900–910. C anovas F, De la R ua P, Serrano J, Galian J (2008) Geographic patterns of mitochondrial DNA variation in Apis mellifera iberiensis (Hymenoptera: Apidae). Journal of Zoological Systematics and Evolutionary Research, 46, 24–30. Chahbar N, Mu~ noz I, Dall’Olio R, De la R ua P, Serrano J, Doumandji S (2013) Population structure of North African honey bees is influenced by both biological and anthropogenic factors. Journal of Insect Conservation, 17, 385–392. Chapman NC, Lim J, Oldroyd BP (2008) Population genetics of commercial and feral honey bees in Western Australia. Journal of Economic Entomology, 101, 272–277. Cook JM, Crozier RH (1995) Sex determination and population biology in the Hymenoptera. Trends in Ecology & Evolution, 10, 281–286. Costa C, Lodesani M, Bienefeld K (2012) Differences in colony phenotypes across different origins and locations: evidence for genotype by environment interactions in the Italian honeybee (Apis mellifera ligustica)? Apidologie, 43, 634–642. Dainat B, Evans JD, Chen YP, Gauthier L, Neumann P (2012) Predictive markers of honey bee colony collapse. PLoS ONE, 7, e32151. Dall’Olio R, Marino A, Lodesani M, Moritz RFA (2007) Genetic characterization of Italian honeybees, Apis mellifera ligustica, based on microsatellite DNA polymorphisms. Apidologie, 38, 207– 217. De la R ua P, Jaffe R, Dall’Olio R, Mu~ noz I, Serrano J (2009) Biodiversity, conservation and current threats to European honeybees. Apidologie, 40, 263–284. Dietemann V, Pirk CWW, Crewe R (2009) Is there a need for conservation of honeybees in Africa? Apidologie, 40, 285–295. Ellis JD, Evans JD, Pettis J (2010) Colony losses, managed colony population decline, and Colony Collapse Disorder in the United States. Journal of Apicultural Research, 49, 134–136. El-Niweiri MAA, Moritz RFA (2010) The impact of apiculture on the genetic structure of wild honeybee populations (Apis mellifera) in Sudan. Journal of Insect Conservation, 14, 115–124. Harpur BA, Minaei S, Kent CF, Zayed A (2012) Management increases genetic diversity of honey bees via admixture. Molecular Ecology, 21, 4414–4421. Harpur BA, Sobhani M, Zayed A (2013) A review of the consequences of complementary sex determination and diploid male production on mating failures in the Hymenoptera. Entomologia Experimentalis et Applicata, 146, 156–164. Jaffe R, Dietemann V, Allsopp MH et al. (2010) Estimating the density of honeybee colonies across their natural range to fill the gap in pollinator decline censuses. Conservation Biology, 24, 583– 593. Jensen AB, Palmer KA, Boomsma JJ, Pedersen BV (2005) Varying degrees of Apis mellifera ligustica introgression in protected populations of the black honeybee, Apis mellifera mellifera, in northwest Europe. Molecular Ecology, 14, 93–106. Mattila HR, Seeley TD (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science, 317, 362–364.
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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
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