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Reproductive Isolation Among Species of the Genus Apis

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Reproductive Isolation Among Species of the Genus Apis Apidologie 31 (2000) 313–339 313 © INRA/DIB-AGIB/EDP Sciences Review article Reproductive isolation among species of the genus Apis Nikolaus KOENIGER*, Gudrun KOENIGER Institut für Bienenkunde, (Polytechnische Gesellschaft), Fachbereich Biologie der J.-W. Goethe Universität Frankfurt am Main, Karl-von-Frisch Weg 2, 61440 Oberursel, Germany (Invited paper) Abstract – In the 1960s, research on reproductive isolation in honeybees started with the pioneering work on Apis cerana and A. mellifera of F. Ruttner. Since then, the number of recognised Apis species increased from four to nine, and data on reproductive isolation played a key role in this development. In this paper, we discuss the behavioural mating barriers (mating season, mating place, sexual signals, daily mating periods), copulatory barriers (size, genitalia, mating sign) and physiological barriers (sperm transfer, sperm storage) and postzygotic barriers (fertilisation, development, hybrids). Allopatric A. mellifera and allopatric populations of the other species had a uniform mating period dur- ing the afternoon hours. Sympatric honeybee species were separated mainly by different daily mat- ing periods. The mating period differed between populations of the same species from different regions. The sequence of the mating periods, however, described from Sri Lanka, Thailand and Sabah (Borneo) followed the same pattern and showed a taxonomic and size correlation: the dwarf bees (A. andreniformis and/or Apis florea) occupied the first position shortly after noon. The next mat- ing period was occupied by cavity-dwelling bees and at sunset, A. dorsata drones flew out for mat- ing. In addition, in the honeybee species that have been studied, various non behavioural mating barriers have been demonstrated. reproductive isolation / Apis / mating behaviour / genitalia / hybrid 1. INTRODUCTION systematics [8, 23, 50]. In spite of these dif- ferences, however, traditional definitions Among evolutionary biologists, defini- acknowledge the central importance of tions of ‘what a species is’ are highly reproductive isolation. Effective barriers to diverse. Furthermore, different species con- gene flow between populations prevent any cepts have had a considerable influence on possibility of subsequent reintegration. Thus * Correspondence and reprints E-mail: [email protected] This work is dedicated to the memory of the late Friedl Ruttner, whose unfailing enthusiasm for research on honeybee reproduction has been an inspiration to us. 314 N. Koeniger, G. Koeniger achieving reproductive isolation becomes barriers operate early, and prevent the phys- an evolutionary ‘key event’ which marks a ical contact between queen and drone; point of independent genetic development ii) copulatory barriers operate during the and divergence. process of copulation (from the first con- In honeybees, research into reproductive tact to the separation of the queen and the isolation has had a relatively recent start. drone). These mechanisms prevent sperm The Western honeybee species Apis melli- transfer to the queen; iii) physiological bar- fera L. with its wide, natural distribution in riers operate after copulation. These barriers Europe, in the Middle East and Africa, and block the path of the sperm from the queen’s its successful introduction into the Americas oviduct into the spermatheca and further to and Australia has dominated scientific inter- the fertilisation of the egg; iv) postzygotic est. Since the start of modern beekeeping barriers disturb normal development, result- in Europe [10] about 150 years ago, numer- ing in the death or in the infertility of hybrids. ous honeybee colonies and queens have been imported from various places (Africa, the Middle East, the Mediterranean islands). 2. BEHAVIOURAL BARRIERS These exotic bees, crossed with the local population, resulted in multiple hybrids, all 2.1. Reproductive isolation due to of them fertile between one another without seasonally different mating periods any apparent limitation [74]. This ‘absence’ of reproductive isolation lasted until 1965, Monogyny is one of the basic features of when A. cerana Fabricius colonies from the honeybee colony. This links the rearing China were imported into Germany, and the of new queens to the process of colony mul- first pioneering research on reproductive tiplication [69]. In other words, the mating isolation among honeybees was initiated by season in honeybees is inevitably linked to F. Ruttner. the swarming season. Reproductive swarm- Traditionally, isolation mechanisms are ing depends on favourable environmental categorised according to their temporal rela- conditions. Specifically, ample pollen and tion to fertilisation as prezygotic − or postzy- nectar must be available for two reasons: to gotic barriers [50]. To accommodate the produce enough bees before colony fission, special mating biology of honeybees and and to support the swarms which do not the complicated process of multiple mating have combs or any honey storage at the in the genus Apis [27], we divided the beginning [84]. For survival, a new swarm prezygotic phase into three subgroups of needs more or less immediate access to nec- isolating factors. The following definitions tar and pollen for comb building and brood apply to this paper (Tab. I): i) behavioural rearing. Otherwise the natural mortality of Table I. Categories of mating barriers and ‘factors’ which may cause reproductive isolation in the genus Apis. Behavioural Copulatory Physiological Postzygotic barriers barriers barriers barriers (prezygotic) (prezygotic) (prezygotic) Mating season Size Sperm transfer Fertilisation Mating places Genitalia Sperm storage Hybrids Sexual signals Mating sign Daily mating periods Reproductive isolation among species of the genus Apis 315 workers cannot be compensated and later During mating flights, A, mellifera drones the swarm (new colony) is reduced to congregate in the open air above their drone beyond the critical threshold. Therefore, the congregation area [106] where they remain, mating season in honeybee populations flying in wide loops until they return to the depends on seasonal blooming cycles. This colony to feed [75]. Congregation areas usu- holds true for allopatric A. mellifera in ally have a diameter of 30–200 m. More Africa and Europe [74], and for populations recently, the area above which the drones of sympatric Asian species. Accordingly, flew was measured by radar as 1 600 m2 in Sri Lanka [39], in Thailand [67] and in [48]. Nonetheless, a congregation area has a Borneo [44] all sympatric Apis species pro- limited spatial extension and A. mellifera duced drones simultaneously. We assume, drones are not attracted by a queen flying because of the uniform mode of colony mul- outside the area [75]. Depending on weather tiplication by swarming within the genus, conditions, A. mellifera drone populations that there is not much ‘evolutionary flexi- fly at a preferential height above the ground bility’ to change the reproductive season that varies from 5–40 m above the ground. between sympatric honeybee species. Within a single drone congregation area, A. mellifera ligustica drones and A. mellifera carnica drones showed a distinct difference 2.2. Reproductive isolation due in vertical distribution: A. m. ligustica drones to different mating places were more frequently caught at lower alti- tudes (4 m above ground), while A. m. car- Among the Apoidea we find an impres- nica drones preferred to fly at higher alti- sive variability of locations where mating tudes [29]. Virgin queens that mated with occurs. Several solitary species mate at the that mixed drone population subsequently nesting sites. Often the males emerge earlier produced significantly more ‘pure’ worker and assemble (and compete) at the nesting offspring: Thus, A. m. ligustica queens sites where they mate with freshly emerging mated more often with A. m. ligustica drones females. In the case of species-specific nest- and A. m. carnica queens mated preferably ing sites, such behaviour would serve as a with A. m. carnica drones. The above dif- mating barrier. Other Apoidea mate on flow- ferences between cruising altitudes of A. m. ers which, in the case of oligolectic bees, ligustica and A. m. carnica drones were dis- may lead to the ‘rendezvous’ of conspecific cussed as a mechanism of assortative mating mates [1]. Another example of spatial dif- (i.e., incomplete reproductive isolation) [29]. ferentiation of mating places comes from Assortative mating has been reported to sympatric Bombus species. The males build occur in a mixed population of A. m. ligus- an odour track by deposition of pheromones tica and A. m. scutellata in South America which attract virgin queens. The altitude [25]. (height) of these odour tracks is different, Since virgin queens commence their mat- ranging from the ground to the canopy [20]. ing flights significantly later than drones, Thus spatial separation seems to work in the congregation of drones is formed irre- favour of reproductive isolation. spective of the presence of a queen [29, 79]. In discussing the genus Apis, we shall The same drone congregation area was vis- start with a short description and review of ited by A. mellifera drones each season for the drone congregation areas of honeybee more than 30 years ([29]; Pechhacker, species. This is intended to lay the basis for unpubl. data). Near Selbourne (England) a the question of whether or not a spatial sep- drone congregation area has been recorded aration of
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