Full text in pdf format

 

Sex determination in honey bees(Apinae and Meliponinae) and itsconsequences

 

 

Warwick Estevam Kerr

Departamento de Genética e Bioquímica, Universidade Federal de Uberlândia, 38400-902 Uberlândia, MG, Brasil.

 

 


ABSTRACT

The first experiments on sex determination in bees began with Dzierzon, Meves, Nachtsheim, Paulcke, Petrunkewitsch, Manning. Whiting, (1943) found multiple alleles in Bracon xo that are the Rosetta stone of sex determination in Hymenoptera. Whiting also discovered that some species of microhymenoptera do not possess xo sex alleles. Therefore, Hymenoptera apparently presents two types of sex determination superimposed on haplodiploidy. In the panmictic groups hemizygous (xo1, xo2,... xon) and homozygous (xo1xo1, xo2xo2... xonxon) are males while heterozygous (xo1xo2, ... xon-1xon) are females. There is no such series of xon in endogamous Hymenoptera, since the constant elimination of diploid males would be damaging to the population and the mutation of xo to xon would be quickly eliminated. Besides the Whiting hypothesis, four others are discussed. The new hypothesis of genomic imprinting, of Beukeboom, is eliminated since: a) spermatozoa that develop within the egg produce male tissue; b) telitokous parthenogenesis due to the fusion of two haploid cells develop into females; c) last instar larvae treated with juvenile hormone become queens. The Cunha and Kerr hypothesis (female determining genes are totally or partially additive and male determination is totally or partially nonadditive) explains all known cases. The xo is a female determining gene. Sex determination in social bees led to the gradual evolution of two systems of caste determination: one in which queens and workers are similar and males are very different (Apinae), and another in which workers and males are very similar and both very different from the queens (Meliponinae). This second system in stingless bees implies that many of the mutations that improve worker capacities also affect the males that will carry out some activities that in Apis are clearly female ones. Ten of these activities are described.

Keywords: Sex determination; Apinae; Meliponinae.


 

 

REFERENCES

Adams, J., Rothman, E.D., Kerr, W.E. and Paulino, Z.L. (1977). Estimation of the number of sex alleles and queen matings from diploid male frequencies in a population of Apis mellifera. Genetics 86: 583-593.

Beig, D. (1968). Produção de machos e desenvolvimento embrionário em Trigona (Scaptotrigona) postica. PhD thesis, UNESP, Rio Claro, SP.

Beukeboom, L.W. (1995). Sex determination in Hymenoptera: a need for genetic and molecular studies. BioEssays 17: 813-816.

Bonetti, A.M. and Kerr, W.E. (1985). Sex determination in bees. XX. Estudo da ação gênica em Melipona marginata e Melipona compressipes a partir de análise morfométrica. Braz. J. Genet. 8: 629-638.

Bonetti, A.M, Kerr, W.E. and Matusita, S.H. (1995). Effects of juvenile hormones I, II and III, in single and fractionated dosage in Melipona bees. Braz. J. Genet. 55 (Suppl. I): 113-120.

Borstel, R.C. Von and Smith, P.A. (1960). Haploid intersexes in the wasp Habrobracon. Heredity 15: 29-34.

Brenha, S.L.A. (1986). Abelhas sociais (Apidae, Apoidea) e seus hospedeiros alimentares em São Luís, MA, Brasil. Monography for obtaining the degree of BSc of Biology. Fed. Univ. Maranhão, São Luís, MA, Brasil.

Bridges, C.B. (1925). Sex in relation to chromosomes and genes. Am. Nat. 59: 127-137.

Camargo, C.A. (1977a). Properties of the xo gene, sex determination in Melipona quadrifasciata Lep. (Hymenoptera, Apidae). VIII Congress Int. Union for the Study of Soc. Insects, pp. 191-192.

Camargo, C.A. (1977b). Effect of juvenile hormone on diploid drones of Melipona quadrifasciata Lep. (Hymenoptera, Apidae). Vlllth Int. Congress IUSSI, pp. 193-194.

Camargo, C.A. (1979). Sex determination in bees. XI. Production of diploid males and sex determination in Melipona quadrifasciata. J. Apic. Res. 18: 77-84.

Camargo, C.A. (1984). Spermatozoa numbers and migration to the seminal vesicles in haploid and diploid males of Melipona quadrifasciata Lep. J. Apic. Res. 23: 15-17.

Cameron, S.A. (1985). Brood care by male bumble bees. Proc. Nat. Acad. Sci. USA 82: 6371-6373.

Campos, L.A.O. (1975). Determinação de castas do gênero Melipona (Hymenoptera, Apidae). Papel do hormônio juvenil. Master's thesis, Dept. Genética, Fac. Medicina de Ribeirão Preto, USP, Ribeirão Preto, SP, Brasil.

Campos, L.A.O. (1978). Sex determination in bees. VI. Effect of a juvenile hormone analogue in males and females of Melipona quadrifasciata (Apidae). J. Kans. Entomol. Soc. 51: 228-234.

Campos, L.A., Velthuis, K.F. and Velthuis, H.H. (1975). Sex determination in bees. VII. Effect of juvenile hormone analogues in caste determination of Melipona. Naturwissenschaften 62: 98-99.

Campos, L.A.O., Drummond, M.S. and Lacerda, L.M. (1983). Determinação do sexo em abelhas. XVIII. Papel do hormônio juvenil I, II, III, na diferenciação das castas de Scaptotrigona xanthotricha (Hymenoptera, Apidae). Ciênc. Cult. 35: 209-211.

Carvalho, G.A., Kerr, W.E. and Nascimento, V.A. (1995). Sex determination in bees. XXXIII. Decrease of xo heteroalleles in a finite population of Melipona scutellaris (Apidae, Meliponinae). Braz. J. Genet. 18: 13-16.

Chaud-Neto, J. (1972). Operárias triplóides em Apis mellifera. In: Em homenagem a Warwick Estevam Kerr, Rio Claro, Brasil, pp. 63-70.

Chaud-Neto, J. (1975). Sex determination in bees. II. Additivity of maleness genes in Apis mellifera. Genetics 79: 213-217.

Chaud-Neto, J. and Duarte, F.M. (1975). Sex determination in bees. V. The action of sexual genes in Apis mellifera. Ciênc. Cult. 27: 125-129.

Chaud-Neto, J., Kerr, W.E. and Bezerra, M.A.F. (1983). Mutation in honeybees. 2. Average rate of mutation based on seven genes for eye colour. J. Apic. Res. 22: 17- 21.

Cook, J.M. (1993). Experimental tests of sex determination inGoniozus nephantidis (Hymenoptera: Bethylidae). Heredity 71: 130-137.

Cortopasi-Laurino, M. (1979). Observações sobre a atividade de machos de Plebeia droryana Friese (Apidae, Meliponinae). Rev. Bras. Ent. 2: 177-191.

Crozier, R.H. (1977). Evolutionary genetics of the Hymenoptera. Ann. Rev. Entomol. 22: 263-288.

Cruz-Landim, C. (1967). Estudo comparativo de algumas glândulas de abelhas e respectivas implicações evolutivas. Arq. Zool. São Paulo, 15: 177-290.

Cunha, A.B. and Kerr, W.E. (1957). A genetical theory to explain sex determination by arrhenotokous parthenogenesis. Forma Functio (4): 33-36.

Devlin, R.H., Grigliatti, T.A. and Holm, D.G. (1985). Gene dosage compensation in trisomics of Drosophila melanogaster. Dev. Genet. 64: 39-58.

Dobzhansky, T. (1930). Genetical and enviromental factors influencing the type of intersexes in Drosophila melanogaster. Am. Nat. 64: 261-271.

Drory, E. (1874). Arbeit über Meliponen. Bienenzeitung 30: 281-286.

Drory, E. (1877). Les mélipones et les trigones. Rucher J. d'Apic. Rationnelle 5: 144-149.

Drory, E. (1883). Nouvelles observations sur les mélipone. Le Rucher du Sud-Duest 1: 59-61.

Drummond, M.S. (1997). A system of social interaction in Zethus miniatus based on the analysis of descendant viability: consideration on the evolution of eusociality in Hymenopera. Braz. J. Genetics (in press).

Dzierzon, J. (1845). Gutachten über die von Herrn Direktor Stohr im ersten and zweiten Kapitel des GeneralGutachtens aufgestellten Fragen. Bienenzeitung 1: 109113,119-121.

Dzierzon, J. (1854). Fernere Beobachtungen über Vermehrung and Reinerhaltung der italienischen Bienen. Bienenzeitung 10: 251-254.

Dzierzon, J. (1898). Widerlegung der jüngst gegen meine Theorie der Fortpflanzung der Bienen erhobene Einwande. 43 Wanderversammlung. Salzburg. Bienenzeitung 54: 299-302.

Dzierzon, J. (1899). Grundlosigkeit and Haltlosigkeit der neuen Lehre. Erste gemeinsame Wanderversammlung.... in Köln a. Rh. Bienenzeitung 55: 318-320.

Engels, E. and Engels, W. (1988). Age-dependent queen attractiveness for drones and mating in the stingless bees, Scaptotgrigona postica. J. Apic. Res. 27: 3-8.

Garofalo, C.A. (1973). Occurrence of diploid drones in a neotropical bumble bee. Experientia 29: 726-727.

Garofalo, C. and Kerr, W.E. (1975). Sex determination in bees. I. Balance between femaleness and maleness genes in Bombus atratus. Genetica 45: 203-209.

Gergen, J.P. (1987). Dosage compensation in Drosophila: evidence that daughterless and sex-lethal control X-chromosome activity at the blastoderm stage of embryogenesis. Genetics 117: 477-485.

Goldschmidt, R.B. (1958). Theoretical Genetics. X. University of California Press, Berkeley, USA, pp. 56.

Gondim, C.G.E. (1984). Alguns aspectos da biologia reprodutiva do guaraná (Paullinia cupana var. sorbilis (Mart., Ducke). Master's thesis, Univ. Amazonas, Manaus, AM, Brasil.

Hartfelder, K. and Engels, W. (1992). Allometric and multivariate analysis of sex and caste polymorphism in the neotropical stingless bee Scaptotrigona postica. Insectes Soc. 39: 1-16.

Hoshiba, H., Ichiji, O. and Kusanagi, A. (1981). The diploid drone of Apis cerana japonica and its chromosomes. J. Apic. Res. 20: 143-147.

Imai, H.T., Crozier, R.H. and Taylor, R.W. (1977). Karyotype evolution in ants. Chromossoma 59: 341-393.

Imperatriz-Fonseca, V.L. (1970). Aspectos da biologia deParatrigona subnuda. Master's thesis, Dept. Zool., Univ. de São Paulo, Brasil.

Imperatriz-Fonseca, V.L. (1973). Miscelaneous observations on the behavior of Schwarziana quadripunctata. Biol. Zool. Biol. Mar. 30: 633-640.

Kelley, R.L. and Kuroda, M.I. (1995). Equality of X chromosomes. Science 270: 1607-1610.

Kerr, W.E. (1950). Estudos sobre a genética de populações de himenópteros em geral e dos apídeos sociais em particular. "Livre Docência" thesis, ESALQ, USP.

Kerr, W.E. (1951). Bases para estudo da genética de populações dos Hymenoptera em geral e dos Apinae sociais em particular. Anais da ESALQ, USP, Piracicaba, SP, Brasil, 8: 219-354.

Kerr, W.E. (1962). Genetics of sex determination. An. Rev. Entomol. 7: 157-176.

Kerr, W.E. (1973). Genética e Biologia de abelhas. Ciênc. Cult. 25: 927-934.

Kerr, W.E. (1986a). Determinação do sexo nas abelhas. XVI. Informações adicionais sobre alelos xo, xa e xb. Rev. Bras. Biol. 47: 111-112.

Kerr, W.E. (1986b). Mutation in bees. 3. Application in bee populations of a mutation rate of g = 1.6 x 10-6. Braz. J. Genet. 9: 1-10.

Kerr, W.E. (1987a). Biologia, manejo e genética de Melipona compressipes fasciculata Smith (Hymenoptera, Apidae). Thesis for Full Professor of Genetics, Univ. Federal do Maranhão, S. Luis, Brasil.

Kerr, W.E. (1987b). Sex determination in bees. XVII. Systems of caste determination in the Apinae, Meliponinae and Bombinae and their phylogenetical implications. Braz. J. Genet. 10: 685-694.

Kerr, W.E. (1987c). Sex determination in bees. XXIV. Critical appraisal of sex determination in bees (in Japanese). Honeybee Sci. 8: 176-182.

Kerr, W.E. (1987d). Sex determination in bees. XXI. Number of xo-heteroalleles in a natural population of Melipona compressipes fasciculata (Apidae). Insectes Soc. 34: 274279.

Kerr, W.E. (1990). Why are workers in social Hymenoptera not males? Braz. J. Genet. 13: 133-136.

Kerr, W.E. (1994). Communication among Melipona workers (Hymenoptera, Apidae). J. Insect Behav. 7: 123-128.

Kerr, W.E. and Cunha, R. (1990). Sex determination in bees. XXVI. Masculinism of workers in the Apidae. Braz. J. Genet. 13: 479-489.

Kerr, W.E. and Esch, H. (1965). Comunicação entre as abelhas sociais brasileiras e sua contribuição para o entendimento de sua evolução. Ciênc. Cult. 17: 527-538.

Kerr, W.E. and Rocha, R. (1988). Comunicação em Melipona rufiventris e M. compressipes. Ciênc. Cult. 40: 1200-1202.

Kerr, W.E., Zucchi, R., Nakadaira, I.T. and Butolo, J.E. (1962). Reproduction in the social bees. J. N. Y. Entomol. Soc. 70: 265-276.

Kerr, W.E., Stort, C.G. and Montenegro, M.J. (1966). Importância de alguns fatores ambientais na determinação de castas do gênero Melipona. An. Acad. Bras. Ciênc. 32: 149-168.

Kerr, W.E., Akahira, Y. and Camargo M.A. (1975). Sex determination in bees. IV. Genetic control of juvenile hormone production in Melipona quadrifasciata. Genetics 81:749-759.

Kerr, W.E., Cunha, R. and Pisani, I.F. (1978). Genética da determinação do sexo. XII. Aplicação de métodos numéricos para agrupar sexos e castas de Melipona quadrifasciata anthidioides Lep. (Apidae). Rev. Bras. Biol. 38: 319-324.

Kerr, W.E., Chaud-Neto, J. and Silva, A.T. (1980). Mutação em abelhas. I. Taxa de mutação reversa para genes que afetam a cor dos olhos nas abelhas. Braz. J. Genet. 3: 275-284.

Kerr, W.E., Monteiro, S.G. and Kerr, H.A.S. (1988). Sex determination in bees. XXV. Adaptive value of the xo' gene in its origin. Braz. J. Genet. 11: 469-473.

Laidlaw, H.H., Gomes, F.P. and Kerr, W.E. (1956). Estimation of the number of lethal alleles in a panmitic population of Apis mellifera. Genetics 41: 179-188.

Legner, E.F. (1979). Prolonged culture and inbreeding effects on reproductive rates of two Pteromalid parasites of muscoid flies. Ann. Soc. Am. 72: 114-118.

Maciel-Silva, V. and Kerr, W.E. (1991). Sex determination in bees. XXVII. Castes obtained from larvae fed homogenized food in Melipona compressipes (Hymenoptera, Apidae). Apidologie 22: 15-19.

Mackensen, O. (1951). Viability and sex determination in the honey bee (Apis mellifera). Genetics 36: 500-509.

Mackensen, O. (1955). Further studies on a lethal series in the honey bee. J. Hered. 46: 72-74.

Makino, S. (1951). An Atlas of the Chromosome Numbers in Animals. 2nd edn. (First American Edition). XXVIII. 290. The Iowa State College Press, Ames, Iowa, USA.

Manning, F.J. (1950). Sex determination in the honey bee. V. The sperm. Microscope 7: 303-305.

Meves, F. (1907). Die Spermatocytenteilung bei der Honigbiene (Apis mellifera L.), nebst Bemerkungen über Chromatinreduktion. Arch. Mikr. Anat. Entwg. 70: 414-491 + 5 tables.

Mitchell, T.B. (1929). Sex anomalies in the genus Megachile, with descriptions of new species (Hymenoptera, Megachlidae). Trans. Am. Entomol. Soc. 54: 321-383.

Mitchell, T.B. (1941). Some additional intersexes in Megachile (Hymenoptera, Megachilidae). Pan-Pac. Entomol. 17: 165-168.

Mota, M.H.V.B. (1988). Estudo comparativo das glândulas epidérmicas do abdômen dos meliponíneos (Hymenoptera, Apidae, Meliponinae). Doctoral thesis. IBRC/ UNESP, Rio Claro, SP, Brasil.

Nachtsheim, H. (1913). Cytologische Studien über die Geschlechtsbestimmung bei der Honigbiene (Apis mellifera L.). Arch. Zellforsch. 11: 169-241.

Nogueira-Neto, P. (1963). Novas pesquisas sobre Meliponíneos. Chácaras Quintaes 108: 2690-2691.

Nogueira,-Neto, P. (1964). Abelhas indígenas sem ferrão algumas observações. Chácaras Quintaes 110: 691-692.

Oliveira, D.A.G. (1992). Compensação de dose em Scaptotrigona postica (Hymenoptera, Apidae) e em Melittobia hawaiensis. Master's thesis, UNESP, Rio Claro, SP.

Oliveira, D.A.G., Kerr, W.E. and Palma, M.S. (1992). Compensação de dose em Scaptotrigona postica (Hymenoptera, Apidae). Proceedings of the X Congresso Latino Americano e XXXVIII Congresso Nacional de Genética. Braz. J. Genet. 15 (Suppl. 1): 256-260.

Parkhurst, S.M., Bopp, D. and Horowicz, I.S.H. (1990). X:A, The primary sex-determining signal in Drosophila is transduced by Helix-loop proteins. Cell 63: 1179-1191.

Paulcke, W. (1899). Zur Frage der parthenogenetischen Entstehung der Drohnen (Apis mellifica). Anat. Anz. 16: 185-187.

Petrunkewitsch, A. (1901). Die Richtungskörper and ihr Schicksal im befruchteten and unbefruchteten Bienenei. Zool. Jahrb. Anat. ii. Ont. 14: 573-608.

Quintero, D.A and Cambra, R.A.T. (1994). Systematics of Pseudomethoca areia (Cameron): sex association, description of the male and a gynandromorph and a new synonymy (Hymenoptera, Mutillidae). J. Hym. Res. 3: 303-308.

Riek, E.F. (1970). Hymenoptera (wasps, bees, ants). In: The Insects of Australia (Michener, C.D., ed.). Division of Entomology, C.S.I.R. Org., Camberra, Austrália, pp. 867-983 (pages 943-951, on bees).

Rothenbuler, W. (1957). Diploid male tissue as new evidence on sex determination in honey bees. J. Hered. 48: 160- 168.

Rothenbuler, W.C., Gowen, J.W. and Park, W. (1952). Androgenesis and zygogenesis in gynandromorphic honeybees (Apis mellifera L.). Science 115: 637-638.

Salt, G.H. (1929). A contribution to the ethology of the Meliponinae. Trans. Ent. Soc. 77: 431-470.

Schmidt, G.H. (1974). Sozialpolymorphismus bei Insekten. Wissenchaftliche Verlag. MBH Stuttgard, Germany.

Severson, D.W., Williamson, J.L. and Aiken, J.M. (1989). Caste-specific transcription in the female honey bee. Insect Biochem. 19: 215-220.

Siebold, C.TH. (1856a). Wahre Parthenogenesis bei Schmetterlingen and Bienen. Engelmann, Leipzig.

Siebold, C.TH. (1856b). Die Drohneneier sind nicht befruchtet. Bienenzeitung 12: 181-184.

Silva, D.L.N. (1977). Estudos bionômicos em colônias mistas de Meliponinae (Hymenoptera, Apoidea). Bol. Zool. Univ. S. Paulo 2: 7-106.

Tucker, K.W. (1958). Automitic parthenogenesis in the honey bee. Genetics 43: 299-316.

Velthuis, H.H.W. and Sommeijer, M.J. (1991). Roles of morphogenetic hormones in caste polymorphism in stingless bees. In: Morphogenetic Hormones in Arthropods: Roles in Histogenesis, Organogenesis and Morphogenesis (Gupta, A.P., ed.). Rutgers University Press, New Brunswick, New Jersey, USA, pp. 346-383.

Von Frisch, K. (1967). The Dance Language and Orientation of Bees. Belknap Press of Harvard Univ. Press, Cambridge, MA, USA.

Whiting, P.W. (1943). Multiple alleles in complementary sex determination of Habrobracon. Genetics 28: 365-382.

Whiting, P.W. (1945). The evolution of male haploidy. Quart. Rev. Biol. 20: 231-260.

Wilson, F. and Woolcock, L.T. (1960). Temperature determination of sex in a parthenogenetic parasite, Ooencyrtus submetallicus (Howard) (Hymenoptera: Ooencyrtidae). Aust. J. Zool. 8: 153-169.

Woyke, J. (1963). Drone larvae from fertilized eggs of the honeybee. J. Apic. Res. 2: 73-76.

Woyke, J. (1979). Sex determination in Apis cerana indica. J. Apic. Res. 118: 122-127.

Woyke, J. (1986). Sex determination. In: Bee Genetics and Breeding (Rinderer, T.E., ed.). Academic Press Inc., New York, pp. 91-119.