Original Article printed in
American Bee Journal (1995) 26: 467-75

Queen Development Time and

the Africanization of European Honey Bees



by GLORIA DeGRANDI-HOFFMAN and JOSEPH C. WATKINS'

Carl Hayden Bee Research Center, USDA-ARS, 2000 East Allen Road

Tucson AZ 85719



Organisms that inhabit an area thrive because they have become well adapted to the 

environmental conditions that surround them. The general rule is that the distinguishing 

characteristics of a species change very slowly over time. Suppose an individual of a 

particular species migrates into a territory in which that same species is established. If the 

migrant individual is similar to the current inhabitants, then the small differences in traits 

that the new arrival might bring will mix into the population and the distinguishing traits 

will rarely, if ever, be seen. On the other hand, if the immigrant has distinctive genetic 

characteristics, it often cannot compete for survival and reproduction with the resident 

population. Thus, these distinguishing characteristics are rapidly removed from the 

population's gene pool.



Many beekeepers have seen an extraordinary occurrence that is an exception to this general 

rule in the Afficanization of the European honey bees (EHB). As Africanized honey bees 

(AHB) have migrated throughout the warmer regions in the Americas, many traits 

commonly associated with the EHB have been replaced by those of the Affricanized honey 

bee. How can this happen?



How EHB become Africanized was the subject of a research project conducted at the Carl 

Hayden Bee Research Center in Tucson, Arizona. The question was addressed by 

constructing a mathematical model to describe the Africanization process. The model 

suggested that development times of queens might be a pivotal factor in the Affricanization 

of the EHB, according to the following scenario.





When AHB swarms migrate into an area with resident EHB colonies, European queens 

will mate with both European and African drones. If the daughter queens with African 

fathers (called African patriline queens) take a shorter time to develop than their half-sisters 

with European patrilines, then the African patriline queens will emerge first. Since the 

emergence of the queen prompts the destruction of all the remaining queens still inside their 

cells, a queen with an African patriline now will head the colony. This new African 

patriline queen will produce drones carrying African genes, which can mate with other 

European queens and thus spread the Africanization process to other colonies. If African 

patriline queens have shorter development times than European, hive by hive European 

patriline queens will be replaced by those with African patrilines. Over time, the resident 

EHB population will change into AHB.



To test the hypothesis that queens with African patrilines have shorter development times 

than those with European patrilines, we captured swarms of



Africanized honey bees and reared queens from them. At the same time, we also reared 

queens from European queens mated to European drones. To simulate the natural event, we 

then mated the European and African queens to both European and African drones. These 

daughter queens were reared in colonies until their cells were sealed. Each queen cell then 

was placed in an individual via] inside an incubator maintained at temperatures of 34.4 

(94'F), 32.8 (91*F), or 31.1*C (88'F). From previous research (DeGrandi-Hoffman et al. 

1993), we knew that those temperatures are typically experienced by developing queens in 

the hive. Every four hours, we checked the incubators and recorded the time that each 

queen emerged. Our results are summarized in the six histograms shown in Figure 1.



In all trials, African patriline queens emerged before those with European patrilines, thus 

supporting our hypothesis. Our data show that even under the controlled temperature 

conditions in the incubators and careful aging of the larvae grafted into queen cells, queens 

have a range of development.







Fig. I . Development times of queens produced from mating European or African queen 

mothers with African and European drones (patrilines). The temperatures that the queen 

cells were maintained at during the postcapping interval are indicated above each pair of 

graphs. Individual graphs represent data from the emergence of 24-27 queens.



Development times. The time to emergence was shorter in all circumstances for queens in 

the incubator with the highest temperature. This was expected since the development rate of 

most insects increases with temperature. 



The queen mothers we used in these experiments were artificially inseminated using equal 

numbers of European and African drones. What would be the chance of an African patriline 

daughter queen emerging first if her mother mated with only 20% African drones? To 

answer this question, we constructed a second mathematical model using the data of queen 

development times. This model predicts the chances that an African patriline queen will 

emerge first given various ratios of European and African drones mating with a queen. The 

results are shown in the graphs in Figure 2. 'Me solid line shows the predictions from our 

model, and the broken line indicates the chances of an African patriline queen emerging first if this 

was based only on the proportion of 

African drones mating with the queen. The differences between the two lines are an 

indication of the influence of queen development time on the chances that an African 

patriline will emerge first. To determine the probability that an African patriline queen will 

emerge first if a queen mated with 20% African and 80% European drones, first find 0.2 or 

20% along the horizontal axis for the proportion of AHB patriline. Next, trace vertically 

above 0.2 until you reach the curve, then move horizontally to the vertical axis to about 

0.35 or 35%. Thus, the graphs show that the probability is about 35% (i.e., the chances 

are 35 out of 100) that an AH13 patriline queen emerges first. If colonies are not managed 

by removing African patriline queens, the model predicts a continuous increase in the 

proportion of matings with African drones and the fraction of colonies that will become Africanized. 

The two graphs also show that the probabilities 

of an African patriline queen emerging first differ, depending upon how the crosses are 

made. Queens from cross. es between an African queen and African drones develop faster 

than those from crosses between European queens and African drones (i.e., the reciprocal 

cross). This could be because metabolic rates are higher for honey bees that are products of 

crosses with African queens compared with the same crosses using European queens 

(Harrison and Hall 1993). The higher metabolic rates could result in shorter development 

times.



Are we certain about our conclusions? Not completely. The shape of the curves could 

change considerably if we take into account the behavior of the different castes of honey 

bee. If, during queen replacement. worker bees prefer to rear daughter queens from their 

own patriline (Page and Erickson, 1984, Page et al., 1989), then this would influence the 

Africanization process. The location of queen cells on a frame and in a colony might be 

different patrilines. Since queen cells reared in the center of the frame or colony are kept 

warmer than those around the edges are, this difference would influence queen 

development times. For example, if developing African patriline queens are maintained at a 

slightly higher temperature than European patriline queens, then the difference in queen 

development times would be even larger and the chance that an African patriline queen 

emerges first would be even higher. If this is the case, then the Africanization process may 

be more rapid than the curves suggest. We are directing our efforts to understanding the 

effect of behaviors during queen replacement that might further influence the odds that a 

queen with an African patriline emerges first.



The Africanization of EHB begins with matings between EHB queens and African drones. 

Consequently, a large population of European drones is essential for insuring that EHB 

queens mate with predominantly European drones. This will increase the chances that EHB 

queens in areas with AHB mate with a high proportion of European drones, thus 

decreasing the chances of a queen with an African patriline emerging first. Queen breeders 

also can select for EHB queens with shorter development times. Currently, development 

time is not a factor in queen breeding programs and queens with shorter development times 

are produced along with those taking longer to mature. This might explain why EHB 

queens on average, have longer development times than AHB. In nature. queens with 

longer development times probably rarely emerge. Over time, natural selection would 

reduce the average queen development for a population toward its minimum. Indeed, this 

might be why queens from feral AHB population have shorter development times than EHB.

Fig. 2 . Probabilities of a queen with an African father (patriline) emerging first in a colony  where the queen mother mated with various ratios of European and African drones. The top  graph (European Queen Mother) represents a European queen that mated with various  proportions of African drones and the bottom graph (African Queen Mother) represents an; African queen that mated with various proportions of African drones.

Literature Cited

                DeGrandi-Hoffman, G., M. Spivak, and

        Acknowledgments J.H. Martin. 1993. Role of ther-



The authors thank Maryann Frazier and   moregulation by nestmates on the

Diana Sammataro for helpful comments    development time of honey bee

on an earlier version of this manuscript.       (Hymenoptera: Apidac) queens.



Ann. Entomol. Soc. Am. 86:165-172.



Harrison, J.F. and H.G. Hall 1993. African-European honeybee hybrids have low 

nonintermediate metabolic capacities. Nature (London) 363:258-260.



Page, R.E., Jr., and E.H. Erickson, Jr. 1984. Selective rearing of queens by worker 

honey bees: kin or nestmate recognition. Anti. Entomol. Soc. Am. 77:578-580.



Page, R.E., Jr., G.E. Robinson, M.K. Fondrk. 1989. Genetic specialists, kin recognition, 

and nepotism in honey-bee colonies. Nature (Lond) 338:576-579.



'Southwest Regional Institute for the Mathematical Sciences, Dept. of Mathematics, 

University of Arizona, Tucson, AZ 85721