Inbreeding and building up small populations of stingless bees (Hymenoptera, Apidae)

Nogueira-Neto, Paulo

doi:10.1590/S0101-81752002000400025

Abstract

A study of the viability of small populations of Hymenoptera is a matter of importance to gain a better zoological, ethological, genetical and ecological knowledge of these insects, and for conservation purposes, mainly because of the consequences to the survival of colonies of many species of bees, wasps, and ants. Based on the Whiting (1943) principle, Kerr & Vencovski (1982) presented a hypothesis that states that viable populations of stingless bees (Meliponini) should have at least 40 colonies to survive. This number was later extended to 44 colonies by Kerr (1985). This would be necessary to avoid any substantial amount of homozygosis in the pair of chromosomic sexual loci, by keeping at least six different sexual gene alleles in a reproductive population. In most cases this would prevent the production of useless diploid males. However, several facts weigh against considering this as a general rule. From 1990 to 2001, 287 colony divisions were made, starting with 28 foundation colonies, in the inbreeding and population experiments with the Meliponini reported here. These experiments constitute the most extensive and longest scientific research ever made with Meliponini bees. In ten different experiments presented here, seven species (one with two subspecies) of Meliponini bees were inbred in five localities inside their wide-reaching native habitats, and in two localities far away from these habitats. This was done for several years. On the whole, the number of colonies increased and the loss of colonies over the years was small. In two of these experiments, although these populations were far (1,000 km and 1,200 km) from their native habitat, their foundation colonies were multiplied successfuly. It was possible to build up seven strong and three expanding medium populations, starting with one, two, three or even five colonies. However, in six other cases examined here, the Whiting (1943) principle and the hypothesis of Kerr & Vencovski (1982) and Kerr (1985), possibly hold up. In two other cases, the results are still unclear. Outside native habitats, most inbreeding experiments failed, possibly because of conditions that cause ecological stress. Although much more data are still needed, a new working hypothesis on the molecular level was presented to explain the results of the experiments described here. In the absence of any considerable stress, and in the eventuality of a good nutritive situation, even individual bees that are homozygous in the pair of chromosomic sexual locus would produce a sufficient amount of a sex determining substance. Therefore, the female genes of all the diploid individuals of a colony, both homozygous and heterozygous, would be activated. However, situations of considerable stress would cause a poor physiological and nutritive condition. This, together with homozygosis in the pair of chromosomic sexual locus, would lead to a smaller production of the sex determining substance. When this happens in the diploid homozygous individuals of a colony, in relation to sex, only male genes are activated. As a result, all such homozygous diploid bees of the colony become useless males. However, when there is a heterozygous situation in the chromosomic sexual locus of all bees of a colony, all diploid individuals would produce a high amount of the sex determining substance. Consequently, all diploid individuals of such a colony would become females (queens and workers). Stresses, including ecological stress, as well as the nutritive condition and the genetic situation in the chromosomic sexual loci, will have a key influence in the life and behavior of the Meliponini, including sex determination. In relation to genetic factors, hybrid vigour may often cause a greater production of biological substances. This may be due to the presence of a greater number of copies of allelic genes when there is heterozygosis. This is a hypothesis requiring further research. However, in the experiments presented here, this hypothesis seems to apply well to the production of a sex determining substance in bees (Apoidea) and other Hymenoptera.

Bee; genetics; imbreeding; population; meliponiculture; stresses; diploid males; sex determining bee substance

Inbreeding and building up small populations of stingless bees (Hymenoptera, Apidae)

Paulo Nogueira-Neto

Instituto de Biociências, Universidade de São Paulo. Caixa Postal 11461, 5422-970 São Paulo, São Paulo, Brasil

ABSTRACT

A study of the viability of small populations of Hymenoptera is a matter of importance to gain a better zoological, ethological, genetical and ecological knowledge of these insects, and for conservation purposes, mainly because of the consequences to the survival of colonies of many species of bees, wasps, and ants. Based on the Whiting (1943) principle, Kerr & Vencovski (1982) presented a hypothesis that states that viable populations of stingless bees (Meliponini) should have at least 40 colonies to survive. This number was later extended to 44 colonies by Kerr (1985). This would be necessary to avoid any substantial amount of homozygosis in the pair of chromosomic sexual loci, by keeping at least six different sexual gene alleles in a reproductive population. In most cases this would prevent the production of useless diploid males. However, several facts weigh against considering this as a general rule. From 1990 to 2001, 287 colony divisions were made, starting with 28 foundation colonies, in the inbreeding and population experiments with the Meliponini reported here. These experiments constitute the most extensive and longest scientific research ever made with Meliponini bees. In ten different experiments presented here, seven species (one with two subspecies) of Meliponini bees were inbred in five localities inside their wide-reaching native habitats, and in two localities far away from these habitats. This was done for several years. On the whole, the number of colonies increased and the loss of colonies over the years was small. In two of these experiments, although these populations were far (1,000 km and 1,200 km) from their native habitat, their foundation colonies were multiplied successfuly. It was possible to build up seven strong and three expanding medium populations, starting with one, two, three or even five colonies. However, in six other cases examined here, the Whiting (1943) principle and the hypothesis of Kerr & Vencovski (1982) and Kerr (1985), possibly hold up. In two other cases, the results are still unclear. Outside native habitats, most inbreeding experiments failed, possibly because of conditions that cause ecological stress. Although much more data are still needed, a new working hypothesis on the molecular level was presented to explain the results of the experiments described here. In the absence of any considerable stress, and in the eventuality of a good nutritive situation, even individual bees that are homozygous in the pair of chromosomic sexual locus would produce a sufficient amount of a sex determining substance. Therefore, the female genes of all the diploid individuals of a colony, both homozygous and heterozygous, would be activated. However, situations of considerable stress would cause a poor physiological and nutritive condition. This, together with homozygosis in the pair of chromosomic sexual locus, would lead to a smaller production of the sex determining substance. When this happens in the diploid homozygous individuals of a colony, in relation to sex, only male genes are activated. As a result, all such homozygous diploid bees of the colony become useless males. However, when there is a heterozygous situation in the chromosomic sexual locus of all bees of a colony, all diploid individuals would produce a high amount of the sex determining substance. Consequently, all diploid individuals of such a colony would become females (queens and workers). Stresses, including ecological stress, as well as the nutritive condition and the genetic situation in the chromosomic sexual loci, will have a key influence in the life and behavior of the Meliponini, including sex determination. In relation to genetic factors, hybrid vigour may often cause a greater production of biological substances. This may be due to the presence of a greater number of copies of allelic genes when there is heterozygosis. This is a hypothesis requiring further research. However, in the experiments presented here, this hypothesis seems to apply well to the production of a sex determining substance in bees (Apoidea) and other Hymenoptera.

Key words: Bee, genetics, imbreeding, population, meliponiculture, stresses, diploid males, sex determining bee substance

Full text available only in PDF format.

Texto completo disponível apenas em PDF.

ACKNOWLEDGEMENTS. I would like to thank Sandra Camerata and Clemilde Soares Pociano da Silva, secretaries; Wilson Carlos de Lima e Sousa, former driver, helper and carpenter (he also brought a colony of

M. subnitida

from Rio Grande do Norte); Juvenal Nascimento Flor, helper and driver; Mario Ribeiro, carpenter; José Vicente Caixeta, Aparecido Leite, Darcy Hickmann, Nelson Gomieiro, Paulo Rubilson, Genario Nascimento da Silva, and Servilio Homura, helpers; Lauro Schluter, who obtained colonies of

Melipona quadrifasciata

in Santa Catarina; Renato Barbosa, who obtained colonies of

M. scutellaris

in Pernambuco; Ana Maria Lopes Menezes, who sent me colonies of this species from Lençois, in Bahia; Luiz Costa, who brought

Scaptotrigona xanthotricha

from Serra da Bocaina (SP); Henrique Carazola, José Correia, Antonio Francisco, Luiz Costa, field finders of bee colonies. Thanks are also due to Professor Dr. Vera L. Imperatriz-Fonseca, to Dr. Marilda Cortopassi-Laurino, Prof. Dr. Dov Por, to the Bee Laboratory of the Departamento de Ecologia, Instituto de Biociências, USP, Prof. Dr. Vinalto Graf, Departamento de Zoologia, UFPR, to Mr. Richard Jones (IBRA); to N. Cristina Martorana for reviewing nearly all the text and my English, and to Usina Açucareira Ester (logistics). Last, but not the least, my thanks to Sociedade Brasileira de Zoologia (President Dr. Olaf H.H. Mielke and Editor Dr. Mirna M. Casagrande) that accepted this paper for publication, to the anonymous reviewers and to all the other people and institutions that helped me on this project. No funding grants were requested or received for this 10 year work.

Received in 11.III.2002; accepted in 07.X.2002.

Bego, L.R. 1982. On social regulation in Scaptotrigona postica Latreille, with special reference to male production cycles. Bol. Zool. Univ. São Paulo 7:181-196.
______. 1990. On social regulation in Nannotrigona (Scaptotrigona) postica Latreille, with special reference to productivity of colonies. Revta bras. Ent. 34:721-738.
Beye, M.; R.F. A. Moritz; R.H. Crozier & Y.C. Crozier. 1996. Mapping the sex locus of the honeybee (Apis mellifera). Naturwissenschaften 83:424-426
Buttermore, R.E.; N. Pomeroy; W. Hobson; T. Semmens & R. Hart. 1998. Assessment of the genetic base of Tasmanian bumble bees (Bombus terrestris) for development as pollination agents. Jour. Apic. Research 37(1):23-25.
Camargo, CA. 1974. Produção de machos diploides de Melipona quadrifasciata. Ci. Cult. 26(7):267.
_____. 1979. Sex determination in bees. XI. Production of diploid males and sex determination in Melipona quadrifasciata. Jour. Apic. Research 18 (2):77-78.
Cappas e Souza, J.P. 1992. Os meliponineos em Portugal e na Europa. Actas do V Congresso Ibérico de Entomologia. Bol. Soc. Portuguesa de Entomologia 1(Supl. 3):53-68.
Carvalho, G.A. 2001. The number of sex alleles (CSD) in a bee population and its practical importance (Hymenoptera, Apidae) Jour. Hymenop. Research 10(1):10-15.
Carvalho, G.A. & W.E. Kerr. 2000. Informações sobre a vida reprodutiva da uruçú (Melipona scutellaris Latreille) e da tiuba (Melipona compressipes fasciculata Smith). Eymba Acusy 1(4):2.
Cornuet, J.M. 1980. Rapid estimation of the number of sex alleles in panmitic honeybee populations. Jour. Apic. Research 19(1):3-5.
Crozier, R.H. 1971. Heterozygozity and sex determination in haplo-diploidy. Amer. Naturalist 105(945):399-412.
______. 1977. Evolutionary genetics of the Hymenoptera. Ann. Review Entomol. 22:263-288.
Cunha, A.B. da & W.E. Kerr. 1957. A genetical theory to explain sex determination by arrhenotokous parthenogenesis. Forma Function 1(4):33-36.
Duchateau, M.J.; H. Hoshiba & H.H. Velthuis. 1994. Diploid males males in the bumble Bombus terrestris. Entomol. Exp. Appl. 71:263-269.
Imperatriz-Fonseca, V.L.; H.H. Velthuis & E. Matos. 1997. Multiple mating in native stingless bees. Ann. XXXV International Apicultural Congress, Apimondia: 73-74.
Imperatriz-Fonseca, V.L.; E.T. Matos; F. Nogueira-Ferreira & H.H. Velthuis. 1998. A case of multiple mating in stingless bees (Meliponinae). Insects Soc. 45:231-233.
Kerr, W.E. 1974. Sex determination in bees. III. Caste determination and genetic control in Melipona. Insectes Sociaux 21(4):357-368.
______. 1985. Número máximo e mínimo de colonias de Meliponineos que devem ser colocados em um local. Bol. Capel., Belo Horizonte, 40:7-8
______. 1987. Sex determination in bees. XXI. Number of heteroalleles in a natural population of Melipona compressipes fasciculata. Insectes Sociaux 34(4):227-279.
Kerr, W.E. & W. Krause. 1950. Contribuição para o conhecimento da Bionomia dos Meliponini. Fecundação da rainha em Melipona quadrifasciata Lep. Dusenia, Curitiba, 1:275-282.
Kerr, W.E. & R.A. Nielsen. 1967. Sex determination in bees (Spinae). Jour. Apic. Research 6(1):1-9.
Kerr, W.E. & R. Vencovski. 1982. Melhoramento genético em abelhas. Efeito do número de colonias sobre o melhoramento. Rev. Bras. Genét. 5(2):279-285.
Kerr, W.E.; A.C. Stort & M.J. Montenegro. 1966. Importância de alguns fatores ambientais na determinação das castas do gênero Melipona. An. Acad. Brasil. Ciên. 38(1):149-168.
Kerr, W.E.; G.A. Carvalho & V.A. Nascimento. 1996. Abelha uruçu. Belo Horizonte, Editora Acangaú, 143p.
Laidlaw, H.H.; F.P. Gomes & W.E. Kerr. 1956. Estimation of the number of lethal alleles in a panmitic population of Apis mellifera. Genetics 41(2):179-188.
Lindauer, M. & W.E Kerr. 1960. Communication between the workers of stingless bees. Bee World 41:29-41, 65-71.
MacKensen, O. 1951. Viability and Sex determination in the honey bee. Genetics 36:500-509.
Michener, C.D. 2000. The bees of the world. Baltimore, Johns Hopkins Univ. Press, 913p.
Moure, J.S. 1951. Notas sobre Meliponinae. Dusenia, Curitiba, 2(1):25-70.
Nogueira-Neto, P. 1970. A criação de abelhas indígenas sem ferrão. São Paulo, Ed. Tecnapis, 2ª ed., 365p.
______. 1990a. The determination of sex and sexual characters in stingless bees. Publicações Tecnápis Ecologia Etologia, São Paulo, 1:1-6.
______. 1990b. Novas idéias sobre a determinação de sexo e castas nas abelhas indígenas sem ferrão. Rev. Brasil. Apicult. 7(39):32
______. 1996a (2000). Inbreeding experiments in colonies of the stingless bee Melipona quadrifasciata (Apidae, Meliponinae). Proceedings Sixth International Conference on Apiculture in Tropical Climates (1996) IBRA, Intl. Bee Research Association, p. 162-166.
______. 1996b. The survival of small populations of Scaptotrigona postica. An. 2º Encontro sobre abelhas, Ribeirão Preto, 2:50-53.
______. 1997. Vida e criação de abelhas indígenas sem ferrão. São Paulo, Edições Nogueirapis, ISBN-85-86525-01-4,446p.
______. 1999. Stressful situations and their consequences on sex determination and on the behaviour of stingless bees. Rev. Etologia 1(1):65-68.
Peters, J.M; D.C. Queller; V.L. Imperatriz-Fonseca; D.W. Roubick & J.E. Strassmann. 1998. Mate number, kin selection and social conflits in stingless bees and honeybess. Proc. Royal Soc. London 266:379-384
Rothenbuhler, W.C. 1957. Diploid male tissue as new evidence on sex determination in honey bees. Jour. Heredity 48:160-168
Roubik, D.W. 1982. Obligate necrophagy in a social bee. Science 217:1059-1060.
Sakagami, S.F. & R. Zucchi. 1963. Oviposition process in a stingless bee Trigona (Scaptotrigona) postica Latreille. Studia Entomol. 6(1-4):497-510.
Schmieder, R.G. 1933. The polymorphic forms of Melittobia chalybii Ashmed and the determining factors imolved in their production. Bio. Bull. 65:338-354.
______. 1938 The sex ratio in Melittobia chalybii Ashmed gametogenesis and cleavage in females and in haploid males. (Hymenoptera, Chalcidoidea, Eulophidae) Bio. Bull. 74:256-266.
Schmieder, R.G. & P.W. Whiting. 1947. Reproductive economy in the Chalcidoid wasp Melittobia. Genetics 32:29-37.
Silva, D.L.N. 1977. Estudos bionômicoa em colônias mistas de Meliponinae. Bol. Zool. 2(4):7-106.
Snell, G.D. 1935. The determination of sex in Habrobracon. Genetics 21:446-453.
Strassmann, J.E. 2001. The rarity of multiple mating by females in the social Hymenoptera. Insectes Sociaux 48:01-13.
Tamarin, R.H. 1996. Principios de Genética. Barcelona, Boston Univ., Editorial Reverte, 607p.
Wheeler, W.M. 1922-1923. Social life among insects. Constable & Co Ltd. 37, on stingless bees mostly p. 121-133.
Whiting, P.W. 1943. Multiple alleles in complementary sex determination in Habrobracon. Genetics 28:365-382.
Wilson, E.D.O. 1971. The insect societies. Belkanp, Harvard Univ. Press, 548p.
Woyke, J. 1963. Drone larvae from fertilized eggs of the honeybee. Jour. Apic. Research 2(1):19-24
______. 1980. Effect of Sex allele homo-heterozygosity on honey bee colony populations and their honey production. Jour. Apic. Research 19(1):51-63.
Yokoyama, S. & M. Nei. 1982. Population dynamics of sex-determinining alleles in honeybees and self-incompatibility alleles in plants. Genetics 91:609-626.

Publication Dates

Publication in this collection
11 May 2009
Date of issue
Dec 2002

History

Received
11 Mar 2002
Accepted
07 Oct 2002

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] Bego, L.R. 1982. On social regulation in Scaptotrigona postica Latreille, with special reference to male production cycles. Bol. Zool. Univ. São Paulo 7:181-196.

[2] ______. 1990. On social regulation in Nannotrigona (Scaptotrigona) postica Latreille, with special reference to productivity of colonies. Revta bras. Ent. 34:721-738.

[3] Beye, M.; R.F. A. Moritz; R.H. Crozier & Y.C. Crozier. 1996. Mapping the sex locus of the honeybee (Apis mellifera). Naturwissenschaften 83:424-426

[4] Buttermore, R.E.; N. Pomeroy; W. Hobson; T. Semmens & R. Hart. 1998. Assessment of the genetic base of Tasmanian bumble bees (Bombus terrestris) for development as pollination agents. Jour. Apic. Research 37(1):23-25.

[5] Camargo, CA. 1974. Produção de machos diploides de Melipona quadrifasciata. Ci. Cult. 26(7):267.

[6] _____. 1979. Sex determination in bees. XI. Production of diploid males and sex determination in Melipona quadrifasciata. Jour. Apic. Research 18 (2):77-78.

[7] Cappas e Souza, J.P. 1992. Os meliponineos em Portugal e na Europa. Actas do V Congresso Ibérico de Entomologia. Bol. Soc. Portuguesa de Entomologia 1(Supl. 3):53-68.

[8] Carvalho, G.A. 2001. The number of sex alleles (CSD) in a bee population and its practical importance (Hymenoptera, Apidae) Jour. Hymenop. Research 10(1):10-15.

[9] Carvalho, G.A. & W.E. Kerr. 2000. Informações sobre a vida reprodutiva da uruçú (Melipona scutellaris Latreille) e da tiuba (Melipona compressipes fasciculata Smith). Eymba Acusy 1(4):2.

[10] Cornuet, J.M. 1980. Rapid estimation of the number of sex alleles in panmitic honeybee populations. Jour. Apic. Research 19(1):3-5.

[11] Crozier, R.H. 1971. Heterozygozity and sex determination in haplo-diploidy. Amer. Naturalist 105(945):399-412.

[12] ______. 1977. Evolutionary genetics of the Hymenoptera. Ann. Review Entomol. 22:263-288.

[13] Cunha, A.B. da & W.E. Kerr. 1957. A genetical theory to explain sex determination by arrhenotokous parthenogenesis. Forma Function 1(4):33-36.

[14] Duchateau, M.J.; H. Hoshiba & H.H. Velthuis. 1994. Diploid males males in the bumble Bombus terrestris. Entomol. Exp. Appl. 71:263-269.

[15] Imperatriz-Fonseca, V.L.; H.H. Velthuis & E. Matos. 1997. Multiple mating in native stingless bees. Ann. XXXV International Apicultural Congress, Apimondia: 73-74.

[16] Imperatriz-Fonseca, V.L.; E.T. Matos; F. Nogueira-Ferreira & H.H. Velthuis. 1998. A case of multiple mating in stingless bees (Meliponinae). Insects Soc. 45:231-233.

[17] Kerr, W.E. 1974. Sex determination in bees. III. Caste determination and genetic control in Melipona. Insectes Sociaux 21(4):357-368.

[18] ______. 1985. Número máximo e mínimo de colonias de Meliponineos que devem ser colocados em um local. Bol. Capel., Belo Horizonte, 40:7-8

[19] ______. 1987. Sex determination in bees. XXI. Number of heteroalleles in a natural population of Melipona compressipes fasciculata. Insectes Sociaux 34(4):227-279.

[20] Kerr, W.E. & W. Krause. 1950. Contribuição para o conhecimento da Bionomia dos Meliponini. Fecundação da rainha em Melipona quadrifasciata Lep. Dusenia, Curitiba, 1:275-282.

[21] Kerr, W.E. & R.A. Nielsen. 1967. Sex determination in bees (Spinae). Jour. Apic. Research 6(1):1-9.

[22] Kerr, W.E. & R. Vencovski. 1982. Melhoramento genético em abelhas. Efeito do número de colonias sobre o melhoramento. Rev. Bras. Genét. 5(2):279-285.

[23] Kerr, W.E.; A.C. Stort & M.J. Montenegro. 1966. Importância de alguns fatores ambientais na determinação das castas do gênero Melipona. An. Acad. Brasil. Ciên. 38(1):149-168.

[24] Kerr, W.E.; G.A. Carvalho & V.A. Nascimento. 1996. Abelha uruçu. Belo Horizonte, Editora Acangaú, 143p.

[25] Laidlaw, H.H.; F.P. Gomes & W.E. Kerr. 1956. Estimation of the number of lethal alleles in a panmitic population of Apis mellifera. Genetics 41(2):179-188.

[26] Lindauer, M. & W.E Kerr. 1960. Communication between the workers of stingless bees. Bee World 41:29-41, 65-71.

[27] MacKensen, O. 1951. Viability and Sex determination in the honey bee. Genetics 36:500-509.

[28] Michener, C.D. 2000. The bees of the world. Baltimore, Johns Hopkins Univ. Press, 913p.

[29] Moure, J.S. 1951. Notas sobre Meliponinae. Dusenia, Curitiba, 2(1):25-70.

[30] Nogueira-Neto, P. 1970. A criação de abelhas indígenas sem ferrão. São Paulo, Ed. Tecnapis, 2ª ed., 365p.

[31] ______. 1990a. The determination of sex and sexual characters in stingless bees. Publicações Tecnápis Ecologia Etologia, São Paulo, 1:1-6.

[32] ______. 1990b. Novas idéias sobre a determinação de sexo e castas nas abelhas indígenas sem ferrão. Rev. Brasil. Apicult. 7(39):32

[33] ______. 1996a (2000). Inbreeding experiments in colonies of the stingless bee Melipona quadrifasciata (Apidae, Meliponinae). Proceedings Sixth International Conference on Apiculture in Tropical Climates (1996) IBRA, Intl. Bee Research Association, p. 162-166.

[34] ______. 1996b. The survival of small populations of Scaptotrigona postica. An. 2º Encontro sobre abelhas, Ribeirão Preto, 2:50-53.

[35] ______. 1997. Vida e criação de abelhas indígenas sem ferrão. São Paulo, Edições Nogueirapis, ISBN-85-86525-01-4,446p.

[36] ______. 1999. Stressful situations and their consequences on sex determination and on the behaviour of stingless bees. Rev. Etologia 1(1):65-68.

[37] Peters, J.M; D.C. Queller; V.L. Imperatriz-Fonseca; D.W. Roubick & J.E. Strassmann. 1998. Mate number, kin selection and social conflits in stingless bees and honeybess. Proc. Royal Soc. London 266:379-384

[38] Rothenbuhler, W.C. 1957. Diploid male tissue as new evidence on sex determination in honey bees. Jour. Heredity 48:160-168

[39] Roubik, D.W. 1982. Obligate necrophagy in a social bee. Science 217:1059-1060.

[40] Sakagami, S.F. & R. Zucchi. 1963. Oviposition process in a stingless bee Trigona (Scaptotrigona) postica Latreille. Studia Entomol. 6(1-4):497-510.

[41] Schmieder, R.G. 1933. The polymorphic forms of Melittobia chalybii Ashmed and the determining factors imolved in their production. Bio. Bull. 65:338-354.

[42] ______. 1938 The sex ratio in Melittobia chalybii Ashmed gametogenesis and cleavage in females and in haploid males. (Hymenoptera, Chalcidoidea, Eulophidae) Bio. Bull. 74:256-266.

[43] Schmieder, R.G. & P.W. Whiting. 1947. Reproductive economy in the Chalcidoid wasp Melittobia. Genetics 32:29-37.

[44] Silva, D.L.N. 1977. Estudos bionômicoa em colônias mistas de Meliponinae. Bol. Zool. 2(4):7-106.

[45] Snell, G.D. 1935. The determination of sex in Habrobracon. Genetics 21:446-453.

[46] Strassmann, J.E. 2001. The rarity of multiple mating by females in the social Hymenoptera. Insectes Sociaux 48:01-13.

[47] Tamarin, R.H. 1996. Principios de Genética. Barcelona, Boston Univ., Editorial Reverte, 607p.

[48] Wheeler, W.M. 1922-1923. Social life among insects. Constable & Co Ltd. 37, on stingless bees mostly p. 121-133.

[49] Whiting, P.W. 1943. Multiple alleles in complementary sex determination in Habrobracon. Genetics 28:365-382.

[50] Wilson, E.D.O. 1971. The insect societies. Belkanp, Harvard Univ. Press, 548p.

[51] Woyke, J. 1963. Drone larvae from fertilized eggs of the honeybee. Jour. Apic. Research 2(1):19-24

[52] ______. 1980. Effect of Sex allele homo-heterozygosity on honey bee colony populations and their honey production. Jour. Apic. Research 19(1):51-63.

[53] Yokoyama, S. & M. Nei. 1982. Population dynamics of sex-determinining alleles in honeybees and self-incompatibility alleles in plants. Genetics 91:609-626.