Dominant lethal mutations in the honeybee: a perspective 50 years later.

IN the 1950s no one thought of the honeybee as particularly adapted to answering genetic questions that were difficult in other organisms. But it has some distinct advantages. For one thing, unfertilized eggs develop into haploid males, whereas fertilized eggs become females, aproperty it shareswithotherhymenoptera.But in addition, a queen bee lays some 1000 eggs per day and the drone cells in the comb are distinguishable from those developing into workers. This makes it simple and unambiguous to distinguish between 100% dominant lethals and sperm inactivation and to have sufficient numbers for quantitative studies, much more difficult in Habrobracon (Heidenthal 1945). Finally, the queen beemates for lifeandcanretainsperm for several years. In the 1950s there was considerable discussion of whether therewas any repairofmutations in irradiatedsperm.The Drosophila data were not very extensive, since the sperm could be stored only for a week or two (Abrahamson and Telfer 1956). In contrast, in the honeybee sperm a possible repair process could be studied over years. Fifty years ago I presented research in Genetics entitled ‘‘The dosage response curve for radiation induced dominant lethal mutations in the honeybee’’ (Lee 1958). Having managed my own apiary of 60 colonies during high school and undergraduate years, I realized in graduate school that the honeybee offered unique characteristics for answering specific questions concerning dominant lethals, questions very difficult to answer in other organisms. This research based on my Ph.D. dissertation, at the University of Wisconsin, took advantage of the unique properties of the honeybee. Two significant results emerged. First, as the dosage of gamma radiation was increased, 100% dominant lethals occurred before sperm was inactivated. Second, irradiated mature sperm stored in the spermathecae of the queen did not show repair of mutational damage during a period of 1 year. In contrast to the advantages just mentioned, there are disadvantages in using the honeybee for studying dominant lethals: (1) the large number of chromosomes (n 1⁄4 16) and their small size makes this material unsuitable for cytogenetic analysis by standard techniques; (2) each queen must be artificially inseminated, a delicate technique, if matings are controlled; and (3) there is only one reproductive female per colony. My data on the dosage response curve included the effect of fractionating the dosage and the stability of dominant lethals in sperm stored in spermathecae of queens for 1 year. In these experiments, I exposed drones to gamma radiation from 500 to 23,000 R and artificially inseminated the pooled semen from simultaneously irradiated drones into virgin queens. The procedure included collecting and counting the eggs from inseminated queens, placing the eggs in colonies manipulated to ensure that a high percentage of the eggs hatched, and later determining the percentage that hatched. The small variance in these experiments among queens receiving similarly treated sperm suggested that no common lethal alleles affected the results. Such lethals are indeed common, because of their association with the large number of multiple alleles in the sex-determining system. In the results, the number of nonhatching eggs laid in worker cells increased with increasing gamma dosage until.99% of the eggs failed to hatch at a dose of 10,900 R, a dose that approximates 100% dominant lethals with ,1% of the eggs hatching. A plateau of,1% eggs hatching occurs from 10,900 to 23,000 R. At 34,000, 60,000, and 86,000 R, all progeny developed into drones showing parthenogenic development. Since the spermatheca of each queen on examination conAddress for correspondence: Department of Biological Sciences, 274 Life Sciences Bldg., Louisiana State University, Baton Rouge, LA 70803. E-mail: [email protected]