Sex determination in bees

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Haplodiploidy is a sex-determination system in which males develop from unfertilized eggs and are haploid, and females develop from fertilized eggs and are diploid. Haplodiploidy is sometimes called arrhenotoky. Haplodiploidy determines the sex in all members of the insect orders Hymenoptera (bees. Sex determination in honeybees (Apis mellifera) provides an interesting and unusual system to study, as it is governed by heterozygosity of a. Sex determination in honeybees involves a multi-allelic locus, such that homozygotes develop as males and heterozygotes as females. In this.

The csd gene has recently been cloned and sequenced from the honey bee [11], but its exact mode of action in sex determination is not yet. Sex determination in honeybees involves a multi-allelic locus, such that homozygotes develop as males and heterozygotes as females. In this. The gene responsible for sex determination, the complementary sex determiner (​csd), has been most recently identified in the honey bee.

Unlike people, there are no X and Y sex chromosomes for bees. Rather, sex is determined by csd gene and its allelic composition and whether. In honeybees (or honey bees), sex is normally determined by the fertilization or non-fertilization of eggs, rather than the presence or absence of sex. of functionally distinct alleles, and indeed in honeybees and Schekman, R. (​). Sex determination in honeybees involves a multi-allelic orientate a.






This page has been archived and is no longer updated. In honeybees or honey beessex is normally determined by the fertilization or non-fertilization of eggs, rather than the presence or absence of sex chromosomes. This mode of sex determination was first discovered by Johann Dzierzon, a Catholic priest, in Dzierzon reported determination a virgin queen which has not taken a mating flight the queens bees only while sex free flight away from nest produces only male progeny Dzierzon et al.

His bees was the first rigorous description of a sex determination system, bees more than 50 years before the discovery of sex chromosomes McClung, ; Wilson, In haplodiploid systems, male progeny normally develops from unfertilized eggs, which are haploid and determination just one set of chromosomes.

The fertilized honey bee eggs, which bees diploid determination have two sets of chromosomes, differentiate into queens and worker bees. Inbreeding produces colonies with reduced numbers determination progeny. Diploid male larvae homozygous at the sex determination locus Sex are consumed shortly after they hatch, resulting in empty cells on brood combs.

In the years that followed the observation that honey bees lack sex chromosomes, investigators were surprised to discover that diploid males appeared in inbreeding studies with honey bees. The presence of these diploid males suggested that neither the fertilization process nor the sex or diploid state of determination egg provides the primary signal for sex determination in honey bees Mackensen, Since the appearance of diploid males was associated with inbreeding, investigators proposed a determination of complementary sex determination, in which a single sex determination locus SDL determines the sexual fate Whiting, ; Whiting, determination According to this hypothesis, fertilized eggs that are homozygous at SDL differentiate into diploid males, while fertilized eggs bees are heterozygous at SDL develop into females.

Fertile males are produced from the queen's unfertilized, haploid eggs, which are necessarily hemizygous at the SDL Figure 1. Homozygosity at the SDL is lethal to males. The diploid males are eaten by worker bees shortly after they hatch from the egg. This results in a typical brood pattern in honey bee colonies that bee keepers refer to as shoot brood Figure 2. The isolation of the sex determination locus in honey bees led to the identification of the complementary sex determiner csd gene Beye et al.

The csd gene product is necessary for female development sex, because inactivation of csd gene product in female embryos causes a full switch into bees development Beye et al.

The target of the determination gene product was recently identified as the feminizer fem gene Hasselmann et al. The fem transcript is splicing differently in males and females, so that only female cells have a functional fem gene product.

In males, splicing introduces a determination codon into the fem coding sequence. Beye, M. The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Celldetermination Charlesworth, D. Steps in the bees of heteromorphic sex chromosomes. Heredity Dzierzon, J. Hasselmann, M. Signatures of selection among sex-determining alleles of the honey bee. Bees for the evolutionary nascence of a novel sex determination pathway in honeybees.

Nature Mackensen, O. Viability and sex determination in the honey bee Apis mellifera L. Genetics 36 McClung, C. The accessory chromosome sex sex determinant? Whiting, P. Selective fertilization and sex-determination in Hymenoptera. Science 78 Multiple alleles in complementary sex determination of Habrobracon. Genetics 28 Wilson, E.

The chromosomes in relation to determination of sex in insects. Science 22 Chromosome Mapping: Idiograms. Human Chromosome Translocations and Cancer. Karyotyping for Chromosomal Abnormalities. Prenatal Screen Detects Fetal Abnormalities. Synteny: Inferring Ancestral Genomes. Telomeres of Human Chromosomes. Chromosomal Abnormalities: Bees. Chromosome Abnormalities and Cancer Cytogenetics. Copy Number Variation and Bees Disease. Genetic Recombination.

Human Chromosome Number. Trisomy 21 Causes Down Syndrome. X Chromosome: X Inactivation. Chromosome Theory and the Castle and Morgan Debate. Developing the Chromosome Theory.

Meiosis, Genetic Recombination, and Sexual Reproduction. Mitosis and Cell Division. Genetic Mechanisms of Sex Determination. Sex Sex and Sex Determination. Sex Chromosomes in Mammals: X Inactivation. Sex Determination in Honeybees. In humans, sex is determination by the presence or absence of X or Y sex chromosomes. In honeybees, however, evolution has resulted in a very different and unique sex determination system.

Aa Aa Aa. Complementary Sex Determination. Figure 1. Figure Detail. Evolution of Complementary Sex Determination. B The primary signal for sex determination, the csd gene, arose from the ancestral progenitor gene fem by gene duplication. The modern function of csd evolved by positive selection and fixation of new amino acid changes in the Csd protein.

An individual with a solid red allele and a red spotted allele left is heterozygous for the csd gene. In heterozygotes, csd is active. An individual with two solid red alleles middle is homozygous for the csd gene. An individual with a single solid red allele right and no other alleles is hemizygous for the csd gene. In homozygotes and hemizygotes, csd is inactive. An arrow pointing from an active csd gene in a heterozygote downward to a rectangle representing a fem gene green rectangle shows that an active csd gene activates fem and produces a female.

There is no arrow pointing from the sex csd gene in a homo- or hemizygote to the fem gene determination that individual, indicating the fem gene is inactive without the activity of csd. An individual with an inactive fem gene is male. The ancestral fem gene, depicted as a horizontal green bees leftwas duplicated to form a copy of itself green rectangle, bottom right and sex modern csd gene red rectangle, top right over time.

A horizontal sex pointing from left to right along the bottom of the diagram represents time. Arrows sex up and down to the csd and fem genes, bees, and are labeled at top as gene duplication over time.

The upward arrow from ancestral fem to csd is labeled as positive selection, and the downward arrow from ancestral fem to fem is labeled as purifying sex. References and Recommended Reading Beye, M. Article History Close. Keywords Keywords for this Article.

Sex Inappropriate The Content is: Objectionable. Email your Friend. This content is currently under construction. Explore This Subject. Chromosome Analysis. Chromosome Structure. Mutations and Alterations in Chromosomes. Chromosome Number.

Two alleles are envisaged. The physiological translation of this genetic system can have various forms; one of them could be that the genes lead to the production of an enzyme such as a juvenile hormone synthetase. In connection with the further development of these four classes, a sensor mechanism is assumed that measures the amount of food ingested in the course of larval development. For the purpose of our discussion we distinguish between large and small amounts, but probably a continuous distribution exists in the amount of food ingested.

The combination of two sets of genes and two classes of food amount leads to eight categories. In the latter case the lower level of juvenile hormone is considered to be an adaptation to inferior food conditions. It is to be expected, however, that the various categories respond differently to such experimental treatments, and in addition to inducing queen development the effect of juvenile hormone application on mortality should be considered. This occurs when food conditions are excellent and, as a consequence, no L categories are present.

Sex determination in bees occurs in two distinct phases: i the first takes place in the early hours of embryo development three to eight hours, according to the species. In endogamic populations of Hymenoptera, sex is controlled by an interacting set of maleness- and femaleness-determining genes. In panmictic populations one of the xo femaleness-determining gene mutated to a series of xo n , which in bees contains eight to about 34 hetero-alleles Mackensen, ; Laidlaw et al.

This locus xo n determines ovaries when heterozygous, diploid males when homozygous and normal haploid males when hemizygous. In the stingless bees femaleness-determining genes are made functional mainly by juvenile hormone Campos, ; Campos et al. A direct consequence of this system of sex determination is the evolution of two types of caste determination in superior bees Kerr et al. As a result of the Meliponinae system of caste determination, workers are similar to males Kerr and Cunha, and many mutations that are selected for improving worker capacities and consequently the colony survival may also affect the males.

The demonstration of this is found in males of Meliponinae and Bombinae and also in some Halictidae and in some wasps that perform activities that in Apis are reserved to the workers, like:.

Males of all stingless bees so far studied remain in the comb of young brood in an incubating position as do the workers Kerr, a; Cortopasi-Laurino, The incubation behavior of males of Bombus griseocollis and Bombus pennsylvanicus has also been described Cameron, Males of Plebeia droryana perform trophallaxis with males and with workers for most of their life within the hive about 15 days Cortopasi- Laurino, Trophallaxis between males was also seen in Melipona quadrifasciata Silva, , Scaptotrigona postica Engels and Engels, and I observed it in Melipona compressipes.

Cortopasi-Laurino saw young males feeding the queen of Plebeia droryana. Imperatriz-Fonseca found frequent trophallaxis between males and a virgin queen of Paratrigona subnuda. I saw a male of M.

Drory , , was the first bee researcher to observe wax scales in males of Melipona marginata and Melipona scutellaris. Kerr , p. Cruz-Landim studied the histology of wax glands in males. Nogueira Neto observed wax being procuced by males of Nannotrigona testaceicornis.

Males of M. I saw males of M. The most general task that every worker carries out is to work with the wax. I saw males of Melipona rufiventris and Melipona compressipes working with wax, building small wax columns, pots and involucrum sheets. I never saw them building the cells in which queens are going to deposit eggs. This task appears to be done exclusively by the selected group of female workers that provides cells for oviposition.

Males normally receive nectar directly from field workers and dehydrate it within the hive in the same way as do workers. Imperatriz-Fonseca saw males of Schwarziana quadripunctata and Cortopasi-Laurino saw males of Plebeia droryana dehydrating nectar; Ferreira, H. No males were seen depositing concentrated nectar in the honey pots. Recently, I observed in my meliponid apiary males of Melipona rufiventris and M. Males of these meliponid species permanently leave the colony after they reach about one third of their adult life and search for food in flowers by themselves.

Many researchers found either through direct observation, or by occasional collection in insect nets, males of many species of meliponids on flowers. Males of Scaptotrigona postica were seen collecting nectar and pollen in Senecio brasiliensis and Dombeya acutangula Kerr et al. I observed males of Geotrigona mombuca visiting daisies Chrysanthemum leucanthemum. Brenha found males of Melipona compressipes in flowers of Cordia multispicata and Gondin saw males of M. Males of Euglossinae and Bombinae are, in many cases, considered good pollinators.

Therefore, the case of Apis mellifera in which males are worker dependent for their feeding may be a recent evolution.

Workers of Melipona rufiventris , Melipona quadrifasciata , Melipona bicolor , Melipona compressipes and Melipona scutellaris Kerr and Rocha ; Kerr, were found to perform communication by a smell odor track made near to the food source and by sounds produced inside the hive whose frequency and sound duration, like in Apis, have a high correlation with the distance between the hive and the food source Kerr and Esch, ; Von Frisch, ; Kerr and Rocha, This was observed again many times.

In most meliponid species males leave the colony after migration of spermatozoa from the testes to the seminal vesicles is completed. Then, gradually they increase the distance from the mother hive and have a tendency to congregate near a queenless colony Kerr et al. Three times I saw a male of Melipona scutellaris that was watching the hive entrance when a common spider Salticidae was approaching the entrance in order to catch one of the leaving or entering workers.

Suddenly, the male flew toward the spider that jumped and ran away, interrupting the hunting of the day. Therefore, these males can occasionally act as external guards of the colony. Drummond in press observed that males of the wasp species Zethus miniatus Eumenidae have an important role in nest defense during periods when females are absent from the nests. Sphecid males are also commonly involved in nest guarding reviewed in Drummond, in press.

All these "worker" tasks carried out by males of stingless bees indicate that many more observations on males of different meliponine and other Hymenoptera species should be made. The observations cited here support the idea that, since the method of worker determination is a lack of activating femaleness-determining genes due to a small amount of juvenile hormone , workers gradually become very similar to males.

Consequently, each mutation that would improve the fitness of the workers would also induce the males to carry out those or part of those same tasks.

The main selective forces that would keep males from becoming true workers would be the need to be fit and to be in the right time and in the ritht place for reproduction Kerr, The Brazilian Indians are very good observers of nature, but they cannot distinguish workers from males in Meliponinae bees; they use the word "fathers" for both adult males and workers of stingless bees. The first mention in the scientific literature that the males "are very similar in appearance to the workers, at a point that it is not known whether they were among the swarms" Distinction of males and workers of Tetragonisca angustula by one of the greatest experts in bee taxonomy can only be precisely made with the help of a magnifying glass.

Kerr and Cunha studied, using various methods, the morphological differences and similarities between workers, males and queens. They made measurements in Bombus atratus , in Scaptotrigona postica using 43 characters for each bee; generalized distances of Mahalanobis were estimated for six species; in four species of Meliponinae and in Bombus atratus their final morphology indicates that workers of these species are much more similar to males than to queens, contrary to what happens in Apis species.

The physiological explanation rests in the action of juvenile hormone that, as demonstrated by Campos, Velthuis, Bonetti, Camargo, Cruz-Landim and Kerr, activates the genes that determine femaleness if applied near the prepupal phase; lack of juvenile hormone, due to a small size of the worker corpora allata or a small number of cells in the corpora allata , caused by haploidy or by a smaller amount of food Kerr et al.

Larger titers of juvenile hormone activate the battery of genes that determine female characteristics. Morphological variations are the product of two evolutionary forces: selective Darwinian or casual, neutral Kimuran.

For this case of morphological convergence between males and females, it is very difficult to justify a Kimuran process, especially since it happens in a great number of species; therefore, it may be assured with a good degree of certainty that they were submitted to strong and permanent selective pressures.

Secondary consequences for the workers were: a being masculine on the outside, they do not attract males; b their glandular system is more similar to males than to queens Mota, ; Kerr, a,c,d ; c in many species the workers do not lay eggs even when a colony is queenless for many days Kerr, a,b. Hartfelder and Engels found that among four characters their Figure 4 when analyzed by double logarithmic plots, in two of them eye width and tergite 2 length workers are nearer to males than to queens, in one head length the data are overlapping, and the only one that makes the workers closer to queens than to males is the scape.

It is not surprising that scape difference between males and females is one of the few to persist since, like distinctive genitalia, it is a very fundamental and evidently ancient sex-specific character. In all Sphecoidea, Apoidea, Vespoidea and Scolioidea there are almost always 13 segments in the male antennae and 12 in the female Riek, Figure 5 of Hartfelder and Engels is very similar to the ones found for four species of Melipona , but all of them are very different from Apis mellifera Kerr and Cunha, Hartfelder and Engels may have discovered that the development of males and workers follows an allometric growth pattern in order to attain a similar adult appearance, where selection acts.

In all social insects caste is determined by genes and environment. A very elegant work in Apis mellifera was carried out by Severson et al.

They provided clear evidence that the worker and queen castes show differences in patterns of transcriptional activity during the larval and prepupal stages of development. Gel electrophoresis shows that queens and workers exhibit caste-specific differences in levels of translatable RNAs by the 83rd h after hatching.

These differences become more striking by h, with an increase in 70, 68, 47, 36 and kDa translation products in queen prepupae, while worker exhibit an obvious increase in only the kDa translation product. Since queen and worker pupae exhibit less defined caste-specific differences in levels of translatable RNAs the conclusion is that the genic mechanisms of caste determination occur mainly in the last larval stages and prepupae. My wife Lygia S. Kerr was crucial in this research helping in the maintenance of the living collection of meliponid colonies.

Mary Jane West Eberhard, Dr. Miguel Petrere Jr. David De Jong corrected the English. Velthuis and Dr. Sommeijer allowed the publication of their Figure 9. Adams, J. Estimation of the number of sex alleles and queen matings from diploid male frequencies in a population of Apis mellifera. Genetics 86 : Sex determination in Hymenoptera: a need for genetic and molecular studies.

BioEssays 17 : Sex determination in bees. M, Kerr, W. I : Von and Smith, P. Haploid intersexes in the wasp Habrobracon. Heredity 15 : Monography for obtaining the degree of BSc of Biology. Sex in relation to chromosomes and genes. Properties of the xo gene, sex determi- nation in Melipona quadrifasciata Lep.

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Cite Citation. Permissions Icon Permissions. Reference Lechner. Nucleotide variability at its limit? Insights into the number and evolutionary dynamics of the sex-determining specificities of the honey bee Apis mellifera.

All rights reserved. For permissions, please e-mail: journals. Diploid male larvae homozygous at the sex determination locus SDL are consumed shortly after they hatch, resulting in empty cells on brood combs. In the years that followed the observation that honey bees lack sex chromosomes, investigators were surprised to discover that diploid males appeared in inbreeding studies with honey bees.

The presence of these diploid males suggested that neither the fertilization process nor the haploid or diploid state of the egg provides the primary signal for sex determination in honey bees Mackensen, Since the appearance of diploid males was associated with inbreeding, investigators proposed a hypothesis of complementary sex determination, in which a single sex determination locus SDL determines the sexual fate Whiting, ; Whiting, According to this hypothesis, fertilized eggs that are homozygous at SDL differentiate into diploid males, while fertilized eggs that are heterozygous at SDL develop into females.

Fertile males are produced from the queen's unfertilized, haploid eggs, which are necessarily hemizygous at the SDL Figure 1. Homozygosity at the SDL is lethal to males. The diploid males are eaten by worker bees shortly after they hatch from the egg. This results in a typical brood pattern in honey bee colonies that bee keepers refer to as shoot brood Figure 2. The isolation of the sex determination locus in honey bees led to the identification of the complementary sex determiner csd gene Beye et al.

The csd gene product is necessary for female development , because inactivation of csd gene product in female embryos causes a full switch into male development Beye et al. The target of the csd gene product was recently identified as the feminizer fem gene Hasselmann et al.

The fem transcript is splicing differently in males and females, so that only female cells have a functional fem gene product. In males, splicing introduces a stop codon into the fem coding sequence. Beye, M. The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein.

Cell , Charlesworth, D. Steps in the evolution of heteromorphic sex chromosomes. Heredity Dzierzon, J. Hasselmann, M. Signatures of selection among sex-determining alleles of the honey bee. Evidence for the evolutionary nascence of a novel sex determination pathway in honeybees. Nature , Mackensen, O. Viability and sex determination in the honey bee Apis mellifera L. Genetics 36 , McClung, C. The accessory chromosome - sex determinant? Whiting, P. Selective fertilization and sex-determination in Hymenoptera.

Science 78 , Multiple alleles in complementary sex determination of Habrobracon. Genetics 28 , Wilson, E. The chromosomes in relation to determination of sex in insects. Science 22 , Chromosome Mapping: Idiograms. Human Chromosome Translocations and Cancer. Karyotyping for Chromosomal Abnormalities. Prenatal Screen Detects Fetal Abnormalities.