Factors affecting the dynamics of the honeybee (apis mellifera) hybrid zone of south africa

ABSTRACT Hybrid zones are found wherever two populations distinguishable on the basis of heritable characters overlap spatially and temporally and hybridization occurs. If hybrids have lower

fitness than the parental types a tension zone may emerge, in which there is a barrier to gene flow between the two parental populations. Here we discuss a hybrid zone between two honeybee

subspecies, _Apis mellifera capensis_ and _A. m. scutellata_ and argue that this zone is an example of a tension zone. This tension zone is particularly interesting because _A. m. capensis_

can be a lethal social parasite of _A. m. scutellata_. However, despite its parasitic potential, _A. m. capensis_ appears to be unable to increase its natural range unassisted. We propose

three interlinked mechanisms that could maintain the South African honeybee hybrid zone: (1) low fitness of intercrossed and genetically mixed colonies arising from inadequate regulation of

worker reproduction; (2) higher reproductive success of _A. m. scutellata_ via both high dispersal rates into the hybrid zone and increased competitiveness of males, countered by (3) the

parasitic nature of _A. m. capensis_. SIMILAR CONTENT BEING VIEWED BY OTHERS SHORT-TERM EFFECTS OF CONTROLLED MATING AND SELECTION ON THE GENETIC VARIANCE OF HONEYBEE POPULATIONS Article

Open access 30 March 2021 SERIAL FOUNDER EFFECTS SLOW RANGE EXPANSION IN AN INVASIVE SOCIAL INSECT Article Open access 29 April 2024 SEASONAL VARIATION IN DEFENSE BEHAVIOR IN EUROPEAN AND

_SCUTELLATA_-HYBRID HONEY BEES (_APIS MELLIFERA_) IN SOUTHERN CALIFORNIA Article Open access 07 August 2023 INTRODUCTION Hybrid zones are ‘narrow regions in which genetically distinct

populations meet, mate and produce hybrids’ (Barton and Hewitt, 1985). Hybrid zones usually arise after fragmentation of a panmictic population, which is later rejoined. Depending on the

differences between the formerly isolated sub-populations, the resulting hybrid zone can either be a transient phase ultimately leading to the re-establishment of one interbreeding

population, or the two sub-populations may remain separated. If the parental genotypes have become adapted to different ecological conditions, the frequency of parental genotypes may form a

cline along an ecological gradient (Hewitt, 1988), or may form a ‘mosaic’ pattern across the landscape, reflecting different ecological zones (Harrison and Rand, 1989). Conversely, if the

separating causes are endogenous (that is determined by genetic incompatibilities), a ‘tension’ zone may be formed between the two parental populations, which forms a barrier to gene flow

between the two. Tension zones are maintained by a balance between dispersal of parentals into the zone and selection against hybrids within it (Barton and Hewitt, 1985). Various mechanisms

may reduce the fitness of hybrids relative to their parental types. These include regulatory incompatibilities between transcription factors and the genes that they control (Noor, 2006),

disruption of co-adapted gene complexes (Barton, 2001), chromosomal incompatibilities between parental populations (FelClair et al., 1996) or behavioural mechanisms such as assortative

mating, which prevent hybrids from finding mates or copulating with them (Moore and Price, 1993). When hybrid fitness is lower than the fitness of either parental type, gene flow is impeded

across the tension zone (Barton and Hewitt, 1985). Where they occur, tension zones tend to be found in regions of low population density, where rates of dispersal of the parental genotypes

into the zone are low (Hewitt, 1988). Here we discuss a hybrid zone between two subspecies of honeybee in South Africa: the Cape honeybee, _Apis mellifera capensis_ Escholtz 1821 (hereafter

_capensis_), and the African honeybee, _A. m. scutellata_ Lepeletier 1836 (hereafter _scutellata_). This hybrid zone is particularly interesting because _capensis_ can be a lethal social

parasite of _scutellata_. However, despite its parasitic potential, parasitism by _capensis_ workers has not been observed outside the natural range of _capensis_ without artificial movement

by humans. NATURE OF THE HYBRID ZONE Based on mitochondrial and micorosatellite markers _capensis_ and _scutellata_ populations are indistinguishable (Franck et al., 2001) but are

nevertheless characterized by significant differences in behavioural and morphological traits (see further). The two subspecies are separated by a hybrid zone with _capensis_ confined to the

southernmost part of the country and _scutellata_ throughout the rest of South Africa and to countries to its north (Ruttner, 1988). Although we cannot be certain how _capensis_ and

_scutellata_ originally became separated, we do know that the Cape bee subsequently evolved some extraordinary and unique characteristics. Foremost among these is thelytokous

parthenogenesis, in which unmated workers are able to lay eggs that develop into diploid females (Onions, 1914). This contrasts with all other honeybee species in which unmated workers

produce haploid males via arrhentokous parthenogenesis. The unique ability of _capensis-_workers to produce female offspring has resulted in calls for its conservation. Fears were expressed

that hybridization between _capensis_ and the much larger _scutellata_ population might drive the only thelytokous honeybee race to extinction (Anderson, 1980). Contrary to this expectation,

however, _scutellata_ colonies introduced into the Cape area tend to die out when they are kept in proximity to _capensis_ apiaries (Allsopp, 1993). The cause of the disappearance of

_scutellata_ colonies when in the vicinity of _capensis_ colonies is the ability of _capensis_ workers to parasitize non-_capensis_ colonies by entering them, activating their ovaries and

producing diploid eggs that are reared by the host colony to produce yet more parasitic daughter workers (Allsopp, 1992). Because parasitizing _capensis_ workers rarely, if ever, produce a

new _capensis_ queen an infestation with parasitic _capensis_ workers ultimately leads to the death of the host colony. Yet, despite having the capacity to become a social parasite,

_capensis_ is unable to spread north of the Cape area unless assisted by beekeepers. Instead, a hybrid zone exists in which _capensis_ and _scutellata_ interbreed without causing a breakdown

of the zone or loss of the distinct characteristics of each subspecies (Hepburn and Crewe, 1991). Evidence for interbreeding within the hybrid zone comes from a study that showed that in

queenless colonies within the zone workers produce both males (by arrhenotoky—_scutellata_ type) and females (by thelytoky—_capensis_ type) (Hepburn and Crewe, 1991), demonstrating that such

colonies are the product of a cross between _capensis-_ and _scutellata_-derived genotypes. The clinal gradient of sting pheromone components further shows that the two interbreed within

the hybrid zone (Hepburn et al., 1994). The bulk of the hybrid zone occurs within the semi-arid areas of the Karoo ecotone, an area 100–200 km wide situated between latitudes 31S and 33S,

where densities of wild honeybee colonies are low (Ruttner, 1977). However, the coastal area east of the country likely provides a significant corridor for contact between _capensis_ and

_scutellata_ populations (Ruttner, 1977). Even within the semi-arid areas of the Karoo there is significant contact between the two subspecies due to bee movements via beekeepers (Ruttner,

1977). Moreover, the contemporary Karoo is a fairly recent ecosystem (Tyson, 1987). Until 300 years ago the Karoo was an extensive grassland, almost certainly inhabited by honeybees (as

evidenced by the large number of bee-related place names (Nienaber and Raper, 1983)) and suggesting that there was also significant contact between the two subspecies in historical times.

This raises the question as to how _capensis_ and _scutellata_ remain separated. REPRODUCTIVE BIOLOGY OF HONEYBEES In order to understand how the two subspecies interact and what the likely

effect is of interbreeding within the hybrid zone, we need to discuss reproductive biology of honeybees in some detail. We also need to discuss aspects of the biology of both _capensis_ and

_scutellata_ with respect to their potential ability to increase their range, as well as behaviour that sets them apart from the other subspecies. Honeybee colonies comprise a single mated

queen and 10–50 000 of her worker daughters. Because of haplo-diploidy the queen can choose the sex of her offspring. Eggs that are fertilized produce diploid female offspring (workers and

queens), whereas (except in _capensis_ workers) unfertilized eggs develop as haploid males. In order to mate, a virgin queen flies to drone aggregations on 1–4 successive afternoons, mating

with 6–10 males on each flight (Tarpy and Page, 2000). Large numbers of colonies contribute males to each aggregation. Where more than one subspecies co-occur, assortative mating may occur

via spatial separation of drones of different subspecies within mating aggregations and temporal separation of mating flights (Koeniger et al., 1989). However, queens regularly mate with

drones of different subspecies, resulting in colonies of mixed subspecies paternity. New queens are produced prior to swarming. As soon as the virgin daughter queens are ready to emerge, the

motherqueen and approximately half the workers leave the parental nest to establish a new colony. In the meantime, the first daughter queen to emerge will seek out her pupal or just-emerged

sisters and kill them. There is therefore a fitness premium for being the first virgin to emerge. Honeybee caste determination is primarily based on differential feeding of female larvae;

thus queens are genetically identical to workers. Queen-destined larvae receive larval food that is richer in certain sugars and receive it in greater amounts than do worker-destined larvae

(de Wilde and Beetsma, 1982). Hence, worker larvae can potentially manipulate adult nurse workers by soliciting more larval food and becoming more queen-like as a result (Allsopp et al.,

2003). A queen signals her presence to workers via pheromones. Workers respond to pheromones produced by the queen herself, and to those produced by her brood, in various ways, most notably

by not producing their own offspring (reviewed in Barron et al. (2001)). This means that worker reproduction is normally absent in the presence of a queen and her brood. However, if the

queen is lost and the colony fails to rear a replacement, workers activate their ovaries and lay eggs that produce fully viable offspring. During this period of worker reproduction there is

reproductive competition among workers, and some subfamilies (worker daughters of a particular male) have higher reproductive success than others (Martin et al., 2004). REPRODUCTIVE BIOLOGY

OF _CAPENSIS_—PREDISPOSITIONS TO REPRODUCTIVE PARASITISM Not only is _capensis_ the only honeybee in which the workers are able to produce diploid offspring, its' workers often show

traits that are normally only found in queens. _Capensis_ workers tend to have: (1) a large number of ovarioles (10–20 compared with 3–5 in other subspecies (Ruttner, 1988)); (2) an organ,

the spermatheca, normally used by queens for the storage of sperm which is absent in workers of all other subspecies (Onions, 1914) and (3) in laying workers, a pheromonal bouquet that

resembles that of queens (Wossler, 2002). In addition to laying workers producing queen-like pheromonal bouquets, a _capensis_ queen, and presumably her brood as well (Allsopp et al., 2003),

produce a much greater quantity of pheromone than any other honeybee subspecies (Crewe, 1988). Hereafter we refer to the characteristics unique to _capensis_ workers (thelytoky, high number

of ovarioles, presence of spermatheca and queen-like pheromonal bouquets) as the _capensis_ complex. As a consequence of thelytokous worker reproduction, reproductive competition among

queenless _capensis_ workers is expected to be even stronger than in honeybee subspecies in which workers can only produce males (Greeff, 1996). Because she can lay diploid eggs that are

substantially clones of herself, a _capensis_ worker has the potential to become the mother of the future queen of the colony; and in genetic terms she becomes the new queen herself. As

might be expected, reproductive competition among queenless _capensis_ worker subfamilies is intense. First, larvae of some subfamilies are apparently much more likely to be reared as queens

than larvae of other subfamilies (Moritz et al., 2005). Second, workers of some subfamilies pheromonally prevent other subfamilies from activating their ovaries (Crewe and Velthuis, 1980),

eventually dominating in egg laying and monopolizing the colony's reproductive output (Moritz et al., 1996). _CAPENSIS_ AS A REPRODUCTIVE PARASITE _Capensis_ workers in a colony headed

by a _capensis_ queen mated to _capensis_ drones behave as any other honeybee worker (Allsopp and Hepburn, 1997). However, problems can arise when a _capensis_ worker finds herself in a

_scutellata_ colony. Most likely _capensis_ workers require higher levels of pheromones than are normally required to regulate reproductive division of labour (given that their queen and her

brood elicit higher amounts, see above). As a result, the mixing of _capensis_ with non-_capensis_ genotypes within one colony results in a cascade of events caused by pheromonal imbalances

between the two subspecies (see Neumann and Moritz (2002) for an overview). _Capensis_ infestations recently played havoc in northern South Africa. In 1992 around 400 _capensis_ colonies

were moved into the _scutellata_ zone (Allsopp, 1993). As early as 1993 it was estimated that 50 000 _scutellata_ colonies had died due to the infestation (Greeff, 1997). Microsatellite

studies have shown that this infestation almost certainly arose from a single _capensis_ worker that has multiplied automatically to produce a vast parasitizing population of workers of very

similar genotype (Baudry et al., 2004). One is tempted to presume that this pseudo-clone has special characteristics that favour parasitism. However, records of other outbreaks suggest that

the potential for social parasitism is not unique to this particular pseudo-clone, and that many _capensis_ workers have the potential to form lineages capable of parasitizing _scutellata_

colonies. REPRODUCTIVE BIOLOGY OF _SCUTELLATA_—A PROVEN INVADER The reproductive biology of the _scutellata-_derived ‘Africanized honeybee’ (hereafter AHB) has been extensively studied in

the American neotropics (for an overview and references see Schneider et al., 2004). AHB has been shown to have a strong reproductive advantage over European subspecies. Whether _scutellata_

has the same reproductive advantage over _capensis_ is unknown, but our assumption is that the reproductive biology of AHB is similar to that of _scutellata_ in its native range. AHB

colonies show a greater emphasis on pollen than nectar collection, and this pollen is rapidly converted into brood. AHB colonies produce more brood per adult worker than other honeybee

subspecies, resulting in high growth rates and increased swarm production. Likewise, drone production is high, resulting in a mating advantage of AHB males due to numerical superiority at

drone aggregations. Moreover, AHB drones tend to drift into other colonies, thereby suppressing drone production by the host colony. Male migration from AHB colonies into European ones was

almost certainly an important factor in the displacement of European subspecies in the Americas. During queen rearing (prior to swarming or to replace the mother queen), AHB virgin queens

may have a competitive advantage in colonies that have both AHB and non-AHB parentage. This advantage arises from AHB virgin queens developing faster than queens of other genotypes. Thus, if

a colony has patrilines arising from both _scutellata_ and non_-scutellata_ males, it is more likely that a virgin from a _scutellata_ patriline will inherit the colony because they tend to

emerge first and kill their rivals. WHAT HAPPENS IN _CAPENSIS SCUTELLATA_ HYBRID COLONIES? The term ‘hybrid’ can have several different meanings in the context of a polyandrous insect

colony, so we discuss this issue first. First a hybrid colony can arise if a queen mates with drones of a different subspecies, in which case her workers are F1 hybrids. Hereafter we call

such colonies F1 hybrids. Second, a queen could mate with drones of both her own subspecies and those of another subspecies, in which case there will be a mixture of F1 and parental workers

in the colony. We will call these ‘mixed’ colonies. Finally a colony might arise from intercrosses (crosses between hybrids or between hybrids and parentals) in which case there will be a

variety of worker genotypes present. We refer to these colonies as intercrossed colonies. We know that F1 matings produce viable colonies without signs of reproductive parasitism by

_capensis_ workers (Crewe and Allsopp, 1994; Jordan et al., 2007). Most likely F1 colonies contain sufficient numbers of _capensis_-derived genotypes to prevent the expression of worker

reproduction due to differences in the pheromonal thresholds that regulate reproductive division of labour. However, based on previous work (Allsopp et al., 2003), we strongly suspect that

as soon as colonies contain a mixture of _capensis-_ and _scutellata_-derived subfamilies, as in intercrossed colonies, differences in the pheromonal thresholds lead to misinterpretation of

inter-subspecies signals. Most important in this regard are the pheromonal cues that regulate the feeding of larvae. If _capensis_ and _scutellata_ larvae are cross-fostered into colonies of

the opposite subspecies, _capensis_ larvae are fed more by _scutellata_ nurse workers than when reared by their own sisters (Allsopp et al., 2003). Conversely, _scutellata_ brood receive

less food when fed by _capensis_ nurse workers (Allsopp et al., 2003). Colonies from the hybrid zone (which are presumably intercrossed colonies) feed _capensis_ larvae significantly more

and _scutellata_ larvae significantly less than they do larvae of their own genotype (Allsopp et al., 2003). Furthermore when larvae from intercrossed colonies of the hybrid zone are reared

by _capensis_ nurse workers, they are fed less compared with when they are reared by workers of their own genotype, whereas the opposite is true when the nurse workers are _scutellata_. It

seems that _capensis_ larvae ‘ask’ for more food than _scutellata_ larvae, resulting in _capensis_ larvae being fed more when nursed by _scutellata_ workers. Similarly, _scutellata_ larvae

‘ask’ for less food than _capensis_ larvae, resulting in _capensis_ nurse workers feeding _scutellata_ larvae less then they would feed to _capensis_-larvae. Larvae from colonies of the

hybrid zone show an intermediate response. This means that larvae expressing _capensis_-like traits are likely to receive more food than either _scutellata_ or hybrid larvae, whatever the

average genotype of the colony. When worker larvae are fed an excessive amount of larval food, the resulting workers are more queen-like, showing decreased pupal development time, increased

wet weight and size of spermatheca and reduced pollen combs on the basitarsus (Allsopp et al., 2003). The rearing of such queen-like workers is likely to come at a colony-level cost, for

example when overfed individuals instead of performing worker tasks become reproductively active. A MODEL FOR MAINTENANCE OF THE _CAPENSIS–SCUTELLATA_ HYBRID ZONE If we are correct and

intercrossed colonies suffer from a breakdown of reproductive division of labour, these colonies will show a reduction in fitness relative to F1 and parental colonies. We also predict that

in the north of the zone, close to the _scutellata_ parental population, there is selection towards a _scutellata_ type. This selection primarily arises from the very high rates of

production of swarms and drones by _scutellata_ colonies (Rinderer et al., 1985). Presumably _scutellata_ drones massively outnumber drones of any other genotype (_capensis_ or hybrid) in

the north of the hybrid zone. If queens, of any genotype, are inseminated by rare _capensis_ males, these males are likely to have low reproductive success. First, _scutellata_ spermatozoa

may be more competitive than _capensis_ spermatozoa, and will therefore be overrepresented in offspring (DeGrandi-Hoffman et al., 2003). Second, daughter virgin queens of _scutellata_ males

may develop faster and have superior fighting abilities compared with daughters of _capensis_ males (DeGrandi-Hoffman et al., 1998). Thus daughters of _scutellata_ males are more likely to

inherit colonies after queen replacement or reproductive swarming, driving the northern hybrid population towards the parental _scutellata_ type. In the south of the hybrid zone, we

hypothesize strong selection towards the _capensis_ type due to the capacity of _capensis_ workers to become parasites of non-_capensis_ colonies, particularly intercrossed colonies. Hence,

any colony that does not express the _capensis_ phenotype will be vulnerable to reproductive parasitism by _capensis_ workers originating from _capensis_ colonies. Moving towards the centre

of the zone, colonies that show mixtures of _scutellata_ and _capensis_-like traits are found (Hepburn and Crewe, 1991; Hepburn et al., 1994). We propose that these intercrossed and mixed

colonies have low reproductive success when different workers in a colony differentially express _capensis_ and _scutellata_ traits. This can arise when queens mate with a mixture of

_capensis_ and _scutellata_ drones, and in second and third generation intercrossed colonies. In this case the breakdown of reproductive division of labour arises from within the colony

(contrary to parasitism coming from without), due to the minority _capensis_ genotypes becoming reproductively active. Critical to understanding the genetic architecture of intercrossed

colonies is the mode of inheritance of the _capensis_-complex (thelytoky, high ovariole number, spermatheca and queen-like pheromonal bouquet). Many of the _capensis-_complex traits are

controlled by a single locus (Lattorff et al., 2007), so some intercrossed workers will express the complete suite of _capensis_-complex traits, while other workers, not inheriting this

allele will not. The presence of individuals that do and do not express the _capensis_-complex traits within an intercrossed or mixed colony will not have adverse consequences as long as the

majority of the subfamilies within the colony are of the _capensis_ phenotype (likely in the southern part of the hybrid zone). This is because there will be no pheromonal imbalances

between _capensis_ and non-_capensis_ worker genotypes, and the colony will appear to be a _capensis_ colony. However, when there are only a few subfamilies expressing _capensis_ traits

within an intercrossed or mixed colony (likely towards the centre of the hybrid zone), _capensis_ workers will misinterpret pheromonal signals emitted from their half-sisters, the brood and

possibly the queen (if the queen expresses the _scutellata_ phenotype). These _capensis_ workers are likely to perceive their colony as being queenless and become reproductively active,

ultimately resulting in a dwindling colony and hence a severe reduction in reproductive success. In addition to the locus that influences pheromone production, onset of reproduction and

thelytoky pleiotropically (Lattorff et al., 2007), there is most likely a second locus that influences the amount of food that a worker larva is fed (Jordan et al., 2007). Individuals that

receive more food are more likely to develop queen-like traits, that is, are more likely to become reproductively active, or to be reared as queens. The amount of food a larva receives

depends both on the genotype of the larva as well as the genotype of the nurse worker. Hence, again, this will result in frequency-dependent expression of worker reproduction in intercrossed

and mixed colonies. The presence of _scutellata_ nurse workers and _capensis_ brood within the same colony, will lead to _capensis_ brood being over-fed by _scutellata_ nurse workers,

resulting in reproductively active _capensis_ workers. CONCLUSIONS In this review we have tried to identify possible mechanisms that maintain the _capensis–scutellata_ hybrid zone in South

Africa. We suggest that there is selection to parental _capensis_ on the south margin of the zone caused by parasitism of any colony showing _scutellata_ traits. In the north margin there is

selection to _scutellata_ caused by excessive production of _scutellata_ males and swarms and a selective advantage of fast-developing queens. Within the hybrid zone intercrossed and mixed

colonies suffer intra-colonial reproductive conflicts, which put them at a severe disadvantage relative to either parental type. We have argued that _capensis_ and _scutellata_ remain

separated due to endogenous factors related to reproductive division of labour and that the hybrid zone is thus an example of a tension zone, maintained by a reduced fitness of intercrossed

and mixed colonies. The hypothesis that we propose assumes an essential role of frequency-dependent selection on reproductive division of labour. Such mechanism is not unique. For example

frequency-dependent mechanisms maintain a hybrid zone of flickers where territory defence depends critically on the shaft colour of the males (Moore and Price, 1993). Birds that have the

minority shaft colour are not able to obtain a territory as the majority of males are unimpressed by the colour of the minority males' shafts. Hence, selection favours the majority

genotype when the two co-occur and individuals within the hybrid zone have reduced fitness compared with individuals in populations where only one shaft colour occurs. Frequency dependence

also plays a role in the Australian frogs _Litoria_ sp. and _Geocrinia_ sp. where females are attracted to the males' advertisement calls (Littlejohn and Watson, 1985) and use call

frequency to discriminate between males of their own species. However, because of clinal variation in call frequency, call frequencies of sympatric individuals overlap more than the

frequencies of individuals outside this zone. As a result females within the hybrid zone are not able to discriminate between males of their own species and those of the sympatric species

resulting in interspecific matings. Honeybees have often served as a model species for investigating questions of general relevance. For example, after its introduction into Brazil in 1956,

_scutellata_ colonized much of the Americas in less than 50 years and therefore provided a unique opportunity to study the factors that determine the success of an invading subspecies

(Schneider et al., 2004). Because of the amenability of honeybees to experimental manipulation, the _capensis–scutellata_ hybrid zone provides a fascinating system for studying factors that

maintain the separation of two social insect subspecies. Our tension zone hypothesis can be tested by constructing colonies comprising different proportions of _capensis_ and _scutellata_

patrilines and determining the colony's relative survival and reproductive success. We can also test some of the other assumptions that we have made, for example the higher reproductive

success of _scutellata_ in the north of the hybrid zone. Although we suspect that the _capensis–scutellata_ hybrid zone is maintained by endogenous factors only, the effect of ecological

factors could potentially be studied by performing reciprocal transplant experiments (for example Bronson et al., 2003; Buggs and Pannell, 2007) provided it is possible to prevent

experimental colonies from being parasitized by _capensis_. In fact an alternative hypothesis for the stability of the _capensis_–_scutellata_ hybrid zone argues that it is maintained by

ecological factors only (Hepburn and Crewe, 1991). Hence, further research will enable us to disentangle the exact biological mechanisms that keep the honeybees of South Africa apart.

REFERENCES * Allsopp MH (1992). The _Capensis_ calamity. _S Afr Bee J_ 64: 52–57. Google Scholar  * Allsopp MH (1993). Summarized overview of the _Capensis_ problem. _S Afr Bee J_ 65:

127–136. Google Scholar  * Allsopp MH, Calis JNM, Boot WJ (2003). Differential feeding of worker larvae affects caste characters in the Cape honey bee, _Apis mellifera capensis_. _Behav Ecol

Sociobiol_ 54: 555–561. Article  Google Scholar  * Allsopp MH, Hepburn HR (1997). Swarming, supersedure and the mating system of a natural population of honey bees (_Apis mellifera

capensis_). _J Apic Res_ 36: 41–48. Article  Google Scholar  * Anderson RH (1980). Cape honey-bee sanctuaries. _S Afr Bee J_ 52: 5–9. Google Scholar  * Barron AB, Oldroyd BP, Ratnieks FLW

(2001). Worker reproduction in honey-bees (Apis) and the anarchistic syndrome: a review. _Behav Ecol Sociobiol_ 50: 199–208. Article  Google Scholar  * Barton NH (2001). The role of

hybridization in evolution. _Mol Ecol_ 10: 551–568. Article  CAS  Google Scholar  * Barton NH, Hewitt GM (1985). Analysis of hybrid zones. _Ann Rev Ecol Syst_ 16: 113–148. Article  Google

Scholar  * Baudry E, Kryger P, Allsopp MH, Koeniger N, Vautrin D, Mougel F _et al_. (2004). Whole-genome scan in thelytokous-laying workers of the Cape honeybee (_Apis mellifera capensis_):

central fusion, reduced recombination rates and centromere mapping using half-tetrad analysis. _Genetics_ 167: 243–252. Article  CAS  Google Scholar  * Bronson CL, Grubb TC, Braun MJ (2003).

A test of the endogenous and exogenous hypotheses for the maintenance of a narrow avian hybrid zone. _Evolution_ 57: 630–637. Article  CAS  Google Scholar  * Buggs RJA, Pannell JR (2007).

Ecological differentiation and diploid superiority across a moving ploidy contact zone. _Evolution_ 61: 125–140. Article  Google Scholar  * Crewe RM (1988). Natural history of honey-bee

mandibular gland secretions: development of analytical techniques and the emergence of complexity. In: Needham GR, Page RE, Delfinado-Baker M, Bowman C (eds). _Africanized Honey Bees and Bee

Mites_. Ellis Horwood: Chichester. pp 149–158. Google Scholar  * Crewe RM, Allsopp MH (1994). Sex and the single queen: recent experiments with _capensis_ and _scutellata_ queens. _S Afr

Bee J_ 66: 58–62. Google Scholar  * Crewe RM, Velthuis HHW (1980). False queens: a consequence of mandibular gland signals in worker honeybees. _Naturwissenschaften_ 67: 467–469. Article 

Google Scholar  * DeGrandi-Hoffman G, Tarpy DR, Schneider SS (2003). Patriline composition of worker populations in honeybee (_Apis mellifera_) colonies headed by queens inseminated with

semen from African and European drones. _Apidologie_ 34: 111–120. Article  Google Scholar  * DeGrandi-Hoffman G, Watkins JC, Collins AM, Loper GM, Martin JH, Arais M _et al_. (1998). Queen

developmental time as a factor in the Africanization of European honey bee (Hymenoptera: Apidae) populations. _Ann Entomol Soc Am_ 91: 52–58. Article  Google Scholar  * de Wilde J, Beetsma J

(1982). The physiology of caste development in social insects. _Advances in Insect Physiology_ 16: 167–246. Article  CAS  Google Scholar  * FelClair F, Lenormand T, Catalan J, Grobert J,

Orth A, Boursot P _et al_. (1996). Genomic incompatibilities in the hybrid zone between house mice in Denmark: evidence from steep and non-coincident chromosomal clines for Robertsonian

fusions. _Genet Res_ 67: 123–134. Article  CAS  Google Scholar  * Franck P, Garnery L, Loiseau A, Oldroyd BP, Hepburn HR, Solignac M _et al_. (2001). Genetic diversity of the honeybee in

Africa: microsatellite and mitochondrial data. _Heredity_ 86: 420–430. Article  CAS  Google Scholar  * Greeff JM (1996). Effects of thelytokous worker reproduction on kin-selection and

conflict in the Cape honeybee, _Apis mellifera capensis_. _Phil Trans R Soc Lond B_ 351: 617–625. Article  Google Scholar  * Greeff JM (1997). The Cape honeybee and her way north: an

evolutionary perspective. _S Afr J Sci_ 93: 306–308. Google Scholar  * Harrison RG, Rand DM (1989). Mosaic hybrid zones and the nature of species boundaries. In: Otte D, Endler JA (eds).

_Speciation and Its Consequences_. Sinauer: Sunderland, MA. pp 111–133. Google Scholar  * Hepburn HR, Crewe RM (1991). Portrait of the Cape honeybee, _Apis mellifera capensis_. _Apidologie_

22: 567–580. Article  Google Scholar  * Hepburn HR, Jones GE, Kirby R (1994). Introgression between _Apis mellifera capensis_ Escholtz and _Apis mellifera scutellata_ Lepeletier: the sting

pheromones. _Apidologie_ 25: 557–565. Article  Google Scholar  * Hewitt GM (1988). Hybrid zones—natural laboratories for evolutionary studies. _Trend Ecol Evol_ 3: 158–167. Article  CAS 

Google Scholar  * Jordan LA, Allsopp MH, Beekman M, Wossler TC, Oldroyd BP (2007). Inheritance of traits associated with reproductive potential in _Apis mellifera capensis_ and _A. m.

scutellata_ workers. _J Hered_ (submitted). * Koeniger G, Koeniger N, Pechhacker H, Ruttner F, Berg S (1989). Assortative mating in a mixed population of European honeybees, _Apis mellifera

ligustica_ and _Apis mellifera carnica_. _Insectes Soc_ 36: 129–138. Article  Google Scholar  * Lattorff HMG, Moritz RFA, Crewe RM, Solignac M (2007). Control of reproductive dominance by

the thelytoky gene in honeybees. _Biol Lett_ 3: 292–295. Article  CAS  Google Scholar  * Littlejohn MJ, Watson GF (1985). Hybrid zones and homogamy in Australian frogs. _Ann Rev Ecol Syst_

16: 85–112. Article  Google Scholar  * Martin CG, Oldroyd BP, Beekman M (2004). Differential reproductive success among subfamilies in queenless honeybee (_Apis mellifera_ L.) colonies.

_Behav Ecol Sociobiol_ 56: 42–49. Article  Google Scholar  * Moore WS, Price JT (1993). Nature of selection in the northern flicker hybrid zone and its implications for speciation theory.

In: Harrison RG (ed). _Hybrid Zones and The Evolutionary Process_. Oxford University Press: Oxford. pp 196–225. Google Scholar  * Moritz RFA, Kryger P, Allsopp MH (1996). Competition for

royalty in bees. _Nature_ 384: 31. Article  CAS  Google Scholar  * Moritz RFA, Lattorff HMG, Neumann P, Kraus FB, Radloff SE, Hepburn HR (2005). Rare royal families in honeybees, _Apis

mellifera_. _Naturwissenschaften_ 92: 488–491. Article  CAS  Google Scholar  * Neumann P, Moritz RFA (2002). The Cape honeybee phenomenon: the sympatric evolution of a social parasite in

real time? _Behav Ecol Sociobiol_ 52: 271–281. Article  Google Scholar  * Nienaber GS, Raper PE (1983). _Hottentot (Khoekhoen) Place Names. Southern African Place Names: 1_. Butterworth

Publishers: Durban. Google Scholar  * Noor MAF (2006). Speciation genetics: evolving approaches. _Nat Rev Genet_ 7: 851–861. Article  CAS  Google Scholar  * Onions GW (1914). South African

‘fertile worker bees’. _Agric J Univ S Afr_ 7: 44–46. Google Scholar  * Rinderer TE, Hellmich RL, Danka RG, Collins AM (1985). Male reproductive parasitism: a factor in the Africanization of

European honeybee populations. _Science_ 228: 1119–1121. Article  CAS  Google Scholar  * Ruttner F (1977). The problem of the Cape bee (_Apis mellifera capensis_ Escholtz):

parthenogenesis—size of population—evolution. _Apidologie_ 8: 281–294. Article  Google Scholar  * Ruttner F (1988). _Biogeography and Taxonomy of Honey Bees_. Springer-Verlag: Berlin. Book 

Google Scholar  * Schneider SS, Degrandi-Hoffman G, Smith DR (2004). The African honey bee: factors contributing to a successful biological invasion. _Annu Rev Entomol_ 49: 351–376. Article

  CAS  Google Scholar  * Tarpy DR, Page RE (2000). No behavioral control over mating frequency in queen honey bees (_Apis mellifera_ L.): implications for the evolution of extreme polyandry.

_Am Nat_ 155: 820–827. Article  CAS  Google Scholar  * Tyson PD (1987). _Climatic Change and Variability in Southern Africa_. Oxford University Press: Cape Town. Google Scholar  * Wossler

TC (2002). Pheromone mimicry by _Apis mellifera capensis_ social parasites leads to reproductive anarchy in host _Apis mellifera scutellata_ colonies. _Apidologie_ 33: 139–163. Article  CAS

  Google Scholar  Download references ACKNOWLEDGEMENTS We thank Bill Hughes, Christian Peeters, Graham Thompson and other members of the Social Insects Lab for discussions and constructive

comments. We also thank the anonymous referees for their comments. Johan Calis is thanked for sharing his ideas and providing us with unpublished data at a very early stage of this

manuscript. MB and BPO are supported by the Australian Research Council. TCW is supported by the National Research Foundation. Additional financial support was obtained from a University of

Sydney Senior International Research Fellowship to MB. Because the number of references was limited to 40, we apologize to all our colleagues who we should have cited but could not. AUTHOR

INFORMATION AUTHORS AND AFFILIATIONS * Behaviour and Genetics of Social Insects Lab, School of Biological Sciences A12, University of Sydney, Sydney, Australia M Beekman & B P Oldroyd *

Honeybee Research Section, ARC-Plant Protection Research Institute, Stellenbosch, South Africa M H Allsopp * Department of Botany and Zoology, DST-NRF Centre of Excellence for Invasion

Biology, University of Stellenbosch, Matieland, South Africa T C Wossler Authors * M Beekman View author publications You can also search for this author inPubMed Google Scholar * M H

Allsopp View author publications You can also search for this author inPubMed Google Scholar * T C Wossler View author publications You can also search for this author inPubMed Google

Scholar * B P Oldroyd View author publications You can also search for this author inPubMed Google Scholar CORRESPONDING AUTHOR Correspondence to M Beekman. RIGHTS AND PERMISSIONS Reprints

and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Beekman, M., Allsopp, M., Wossler, T. _et al._ Factors affecting the dynamics of the honeybee (_Apis mellifera_) hybrid zone of South

Africa. _Heredity_ 100, 13–18 (2008). https://doi.org/10.1038/sj.hdy.6801058 Download citation * Received: 21 February 2007 * Revised: 31 July 2007 * Accepted: 03 August 2007 * Published: 12

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shareable link Sorry, a shareable link is not currently available for this article. Copy to clipboard Provided by the Springer Nature SharedIt content-sharing initiative KEYWORDS * _Apis

mellifera capensis_ * _A. m. scutellata_ * hybridization * reproductive division of labour * social parasitism * thelytoky