Estudos sobre o gênero Melipona

Estudos sobre o gênero Melipona

Warwick Estevam Kerr

Assistente da Cadeira e Secção de Citología e Genética Geral da Escola Superior de Agricultura "Luiz de Queiroz'' Universidade de Sao Paulo

RESUMO

1°' - Cita-sé a evolução das abelhas segundo MICÍÍENÉR" (1944).

2.° - A evolução dos Melíponíneos é estudada sob o ponto de vista da sua biologia, estabelecendo-se o tipo do meliponíneo primitivo.

3.° - São feitas considerações sobre a distribuição geográfica dos meliponíneos, entrando-se em detalhes sobre os seus fosseis, sobre a influência dos deslocamentos geológicos do cenozoico sobre sua distribuição, com particular referência ao seu estabelecimento na América do Sul. Considera-se também o e$eito das glaciações e a descontinuidade por ela provocada na distribuição dos meliponíneos.

4.° - São feitas hipóteses sobre a época em que se formaram as Meliponas, sobre o processo de determinação das castas e sua influência na evolução das mesmas. O tipo M. marginata é considerado o mais primitivo dos existentes atualmente.

É dada uma hipótese, baseada na biologia e genética das Meliponas, para explicar sua evolução a partir de uma Trígona primitiva.

5.° - Sugere-se que a M. fascisrfta (excluidas a M. punc-ticollis e M. concinnula, que necessitam de estudos) seja do tipo da Meliponatrifatorial primitiva, tomando-se por base a sua proximidade a M. marginata, sua distribuição e sua variação.

6.° - Sugere-se como centro de origem das Meliponas a Bacia Amazônica, por ser esse lugar a zona onde há maior variação e por ser o centro geográfico da área habitada pelas Meliponas.

SUMMARY

Studies on the genus Melipona

1 - Introduction and acknowledgements.

2 - Systematica.

Three modern trends in the systematics of the Meliponini are cited: Ducke (1916), Schwarz (1932) and Moure (1946); The 14 species known of the genus Meliponaare given.

3 - Contribution to the Biology.

There are three castes in Melipona: drones, workers and queens, which are easily distinguished on account of the differences in size, color, proportions and behavior.

While the queen of Apis emerges in a state of sufficient development to be fertilized and to begin the laying of eggs, the queen of Melipona, on the other side, in a glance seems undernourished, get having received the same food as the workers, both in quantity and in quality. They emerge with undeveloped ovaries and, only after the fertilized queen is dead or too old, virgin queens may be fertilized and begin to be fed by workers. After 15 to 30 days, according to the number of workers and the food gathered, the queen begins to lay eggs.

The queens, drones and workers emerge from cells of the same size and with more or less the same quantity of food. Variations of the quantity of food do not change the caste, but only the size of the bee.

The caste determination in Trigonai (another genus of Meliponini) depends evidently upon differences in nutrition. It is easily seen that the cells which furnish drones and workers are different in size, though equal in form, from those from which emerge the queens.

Somie data concerning the biology of the Meliponini are given below: 1st - The number of eggs laid by a queen:

Melipona quadrifasciata anthiodioides - in 44 days (July 9th to Aug. 22nd - 1946) 590 eggs, with an average of 13 eggs per day, and a maximum of 22 eggs per day.

Trígona (Plebéia) mosquito, (Mirim-guassú) - from July 9th to July 24th 1946, 249 eggs. Prom Aug. 9th to Aug. 24th, 1946 laid 1035 eggs; with an average of 69 eggs per day and a maximum of 120 eggs.

2nd) - A table is given showing the percentage of drones observed in the total of individuals in samples of brood combs. (See Quadro I and Quadro EE).

3rd) - The duration of the several phases in the lives of the Meliponaworkers and queens is:

Phases Worker Queen

Hatching of the egg 4,5 to 6,5 days 4,5 to 6,5 days

Larva 7 to 8 days 7 to 8 days

Prepupa 5 to 5,5 days 4,5 to 5 days

Pupa 15,5 to 18 days 11,5 to 15 days

Total, from egg to imago 34 to 37 days 30 to 34 days

It is mentioned that the Meliponini constructs large honey and pollen pots of characteristic size, and form both In natural hives and in experimental colonies in wooden boxes.

The workers in weak colonies of M. Marginata and M. schencki produce little wax, and excepcionally, use brood cells for storage Instead of pots, showing that their reactions are very variable.

Other details of the brood cell, such as brood cells disposition, construction, destruction, etc., are discussed.

4 - Anatomy of the reprodutive organs.

The sexual organs of the male consist of: a) Two testicles envolved by a thin membrane, each of the testicles formed by four testicular tubes, b) two vasa deferentia, c) two vesiculae seminales, which are spherical and very small, d) one ejaculatory duct and e) the pente. There are no accessory glands as in Apis and Bombus. (BORDAS, 1895) See Fig. 6 and 46).

The reprodutive organs of the female consist of: a) two ovaries, each formed by four ovardoles. The length of these pvarioles is: 1,7 to 2,0 mms. in the worker or sterile female, 11,1 to 11,5 mms. in the virgin queen and 76 mms. in the fecundated queen (measures taken on Meliponafasciata melano ven ter), b) two oviducts, c) vagina and d) spermatheca with a pair of glands. This same description is applied to Trígona and Bombus, varying the proportions.

5 - Citology

Studies on the cytology of the genera Melipona and Trigona were carried out Ovaries òf the pupas queens and workers, testicles of prepupas and young pupas of drones, brains and other somatic' ttisues of larvae were examined. The details of the technique and the results are given. ;The somatic tissue of the females, both queens and workers, presents 18 chromosomes. The spermatogeneáfó is normal, following the type described for Apis by Meves (1907) with expulsion of a cytoplasmatic Bud in the first division, and a nucleated bud in the second,

The sperfiuatogonia and spermatids show 9 chromosomes. 'Polyploid ^ccel|sl and tissues are fre'quent, even in the testicles but polyploid secondary spermatocytes do not go through a second meiotic division. No polyploid individuals have been found às yet. The number of chromosomes is the same in all Melipona, studied: M. fasciata, M. marginata, M scheneki. M. quadrifasciata, A. e. 18 in the female and 19 in the male.

6 - Determination cf castes of queen and worker.

There are many papers discussing the problem of caste determination in the social insects (Bibliography in the papers of Light, 1943 and Wheeler, 1928)* Two,, theoriescome always under discussion: a) the. Blasjtógezüc or_; genptypJc determination and b) the Trophogenfè or somatogenic one. In the first case, special genes are supposed to be responsible while in the second case the determination is by means of food or other environmental factors.

No one doubts today that the caste of .males In Hyme-hoptera is genetically determined by arrhenotoky, wjth very few exceptional casss. The Meliponabees do not escape this rule, as shown by chromosome counts. The opinions aré however divided with regard to the female castes.

There is at present a trend attempting to prove the tro-phogenic theory, by means of comparisons, analogies and generalizations. The studies of Perez (1895), Ihering (1903), Salí (1929), Schwarz (1932),and Kerr (1946) are cited in this Connection.

Mhetods: Combs with a variable number of "cells were taken into the laboratory and the caste of each bee was re gistered. in the pupal stage or a short time after emerging.

The proportions of queens cannot be determined by sam Estado» sobra o gênero Melipona pling in the colony, because numerous queens are killed soon after emerging from their cells.

Material used: Hives of Meliponaquadrifasciata anthidioides (Lep. 1836), M. quadrifasciata vicjna (Lep. 1836), Melipona quadrifasciata quadrifasciata (Lep. 1J3JB), Melipona fasciata rufiveritris (Lep. IB36>, M. faseiata melanoventer (Schwarz, 1932), M. marginata margmata (L?p. 1836), Melipona schencki schencki (Gribodo, 1893).

Results: - The results of the counts ate registered in two tables, one refering to large Meliponas (Table m) and the other to Melipona margmata (Table IV).

In consequence of abnormalities in the' conditions we may alter the proportions and results obtained, given in Table V, will be discussed later.

As it may be seen, there are in each case (Table in and XV) two groups in the percentages of queens over the total number of females: one with á high percentage, corresponding to the period front September to April and the other of low percentage, during the dry season (May to August).

We shall analyse in the first place the high percentage group which occurs in the time where the hive has its maximum-pi vitality.

Both in the Tables m and IV, the data of this normal period are callea group 1 -f group 3. In a total of 1489 bees of the Table HI, we have 169 queens and 1320 workers, or 11,35% of queens. In the other Table IV there were in a total of 398 bees (group 1 -f group 3) 87 queens and 311 workers, or a percentage of 21,86%.

It was found in the preliminar statistical analyses (Kerr, 1946), that for the percentage of the queens, in the first case, a value of 12,5% may be accepted as mean and in the second a value of 25%.

As may be seen in the Thables m and IV, all the results agree with these means and vary around 12,5% respectively agree with these values and vary around 12,5% and 25% respectively as proved by the 2-test.

EXPLANATION

The proportion of 75% of workers to 25% of queens corresponds to a mendelian bifactorlal back-cross ratio of 3:1.

Since in the Hymenoptera the males are always haplold and thus produce only one genotype in their gametes, they behave In crosses in the same way as a diploid homozygote. Furthermore, since we obtain a bifactorlal segregation, it fol- lows that the queen must be a double heterozygote. Thus we may represent the reproduction in these bees by any one of the following formula :

Queen x Drone = 1 Queen + 3 Workers

AaBb x AB = AaBb + AABB + AABb + AaBB

AaBb x Ab = AaBb + AABb + AAbb + Aább

AaBb x ab = AaBb + Aabb + aaBb + aabb

In order to explain the second case, where the proportion of queens in around 12,5% Table VII it is sufficient to assume that in this species there are three pairs of factors, the queen being the triple heterozygote : Aa Bb Gc.

Our formulas may now be written as follows :

Queen x Drone = 1 Queen + 7 Workers

AaBbCc x ABC = AaBbCc + AABBCC + AABBCc +

AABbCC + AABbCc + AaBBCC + AaBBCc + AaBbCC

AaBbCc x aBC = AaBbCc + AaBBCC + AaBBCc +

AaBbCC + aaBBCC + aaBBCc + aaBbCC + aaBbCc

There is at the moment no possibility to confirm experimentally these formulas since we have not yet discovered any linked charater. Though we may expect any proportion under the conditions of a phenotypic determination of castes, the occurrence of two related mendelian ratios cannot be attributed to a mere accident. The failure to encounter the third related mendelian proportion, of a monofactorial segregation (1:1), will be explained later.

Thus we conclude that fertile females or queens are only the bees which are completely heterozygous, while both in the bifactorial as in the trifactorial case the workers are the individuals which are homozygous for one or more factors, e. g. AAbb, aabb, AaBB, aabbcc, AaBbCC, etc.

We heve not been able to find any identical case in the literature, but we may interprete the situation as an exemple of heterosis or hybrid vigour. Thus the experiments of Wright and Dobzhansky (1946) on Drosophila pseudoobscura and of Gustafsson (1947) on barley may be cited as parallel cases.

Additional Proofs:

In, addition we cite some observations which may be considered as an auditorial proof of our hypothesis:

1) The queérí of Apis is' different from the workers only in size and proportions, but queens of the several Meliponaspecies are different not only in size and proportions, but also in color. In Meliponaquadrifaseiata, for instance, the workers have black abdomen with broad yellow bands While the queen is brownish black all-over. This effect is difficult to attribute to alimention.

Fritz Mtlller (1875) examining nestes of Meliponacoyrepu, MtiUer, thought he had found a parasitic species, M. cueulina, Miiller, but when revised by Ihering (1903) it was found to be the virgin queen. This is sufficient to show how different the queens are from the workers.

2) The cells of Melipona queens have the same size and the same quantity of food. This fact was verified by all the biologists who studied this genus (Silvestri 1902, Ihering 1903, Márianno 19Ü, Wheeler 1923, 1928, Salt 1929) arid also extensively confirmed by the author.

3) The cells of Meliponaare filled with food indiscrimina-tedly by several workers and after this operation is completed, the queen lays the egg. Thus it seems impossible to assume that there may be any systematic difference in the food distribution because there are no specialized cells with different sizes to provoke the specific reaction on the part of the worker like in Apis.

4) In Apis as in Trígona observations were made on the disposition of royal cells in the comb and it was found that it is notat random. On the contrary, in Apis, the great major rity of royal cells are placed in the inferior terminal part of toé comb and are produced in a large scale only when the queen is dead. In Trígona bees the royal cells are preferentially on the edges of the comb but when the queen has died no increase of these cells is possible since all are already filled with food and sealed. If food should be the determining factor in Melipona, it should be expected that the queen cells would be localized in some kind of preferential grouping in the comb; but counting was made of two combs, one of M. quadrifaseiata and other of M. marginata» with respectively 189 and 85 cells, and the cells which gave workers and those which gave queens were noted. The statistical analysis showed that the distribution of cells from which queens were bom is at random with no pre ferential grouping-.

Proportions of the castes daring the winter.

As it was related, in the period from May to August the percentage of queens falls from 12,5% and 25% to nearly 3% and 6% respectively, as one can see in the Tables III and IV.

One case of reduction of percentages well known is of Lebistes, discussed by Winge (1934).

The mechanism that causes the reduction in the percentage of queens is unknown so far. but several hypothesis; are discussed:

a) Elimination of queens by the workers, during the larval estage, does not occur, since all cells are sealed after egg laying and are not opened again before emerging.

b) Preferential oosorption of the eggs which should give queens - This hipo thesis was rejected since there is not sufficient time after the fecundation for a preferential degeneration of eggs.

c) Loss of chromosomes - Cytological aberrations were observed in two males, but this cytological hypothesis can be rejected for the females because counting the chromosomes of nealy 50 larvae during the winter we found that ail of them had 18 chromosomes.

d) Abnormalities during the fertilizations:

1) Preferential fertilization.

2) Parthenogenetic development with preferential fusion of two haploid nuclei or fusion of cleavage nuclei.

8) Elimination of the spermatozoa in the cytopiasma of the egg which is denser, owing to the shortage of food given to the queen or to low temperature. To restore the diploid number there are two ways: There may be either a preferential fusion of meiotic nuclei or a fusion of first cleavage nuclei.

The hypothesis of a fusion of cleavage nuclei seems the most probable, since it gives automatically only homozygous individuals, and never heterofcigons queens. Such cases of female parthenogenese, have been observed in other Hymenoptera (Mackensen 1943, Smith 1941). The effect of low temperatures doubling the "chromosomes of haploid eggs has been observed in Trituras by Griffiths (1338), Moore (1941) and Fahkhauser (1942).

Discussion of analogous case in termites anil ants.

The existence of castes among the male termites suggests that they may have also a mechanism for caste determination as in Melipona. The hetercsigous should thus be the sexual forms and the individuals homozigous for one or more factors, the sterile forms.

The paper of Light (1943), based upon thousands of "incipient colonies**, mainly of Zootermopsis nevadensis, favors an extrinsic determination of castes. But studies should be made with normal Termites colonies, to obtain a proof that men-delian proportions occur when there is no elimination.

Wheeler (1937), adopted a theory of a genetic determination of castes, based on observation with several mosaics and mutations recorded, mainly, in Acromyrmex octospinosus.

To explain the mosaics we may suggest the following :

a) Gynergates (female-worker mosaics) are supposed to derive from an egg Aa Bb which should be a qusen. Owing to non-disjunction of the A chromosomes cleavage division resulted in nucleus ABb (worker, since only Bb is heterozygous) and a nucleus Aaa Bb (queen, since both Aaa and Bb are heterozygous).

A mutation from A to a and vice-versa will produce the same effect b) Diploergate (major and media worker mosaics): If we suppose that absence of alleles has the same effect as homo-zygosis (ABB being equal to AABB, and aa BB, both however different from Aa BB) non disjunction in a cleavage division will give the result expected in mosaics: A BB small and Aaa BB large.

c) Gynandromorphs will not be discussed here because too many hypothesis are possible.

Whitting (1939) in a complete review of the paper by Wheeler suggests "that we are here dealing not with sex and caste mosaics but with sex and caste intergrades of another sort, namely, intersexes and intercastes". "Intersexuality may be caused genetically by race-crossing as in Lymantria, or it may result from trophogenic or other environmental influences". At the end of his paper we read: "The single haploid male caste is without question differentiated genetically. As for the various female castes, the reviewer Inclines toward the trophogenic theory. Any blastogenic scheme involving hereditary differences would necessitate some system for maintaining in the reproductive members of pure race genie dif- ferences whic might segregate to form the sterile castes. Such is "Conceivable but doubtfull".

Believing to have shown that caste determination in Meliponais genetic, we must admit the possibility that the same is the case in ants under discussion and that mosaics are due to non-disjunctions or mutations.

Papers of Wesson (1940) on Leptothorax curvispinosus, Bhattacharya (1943) on Oecophylla smaragdina, and others are rapidly discussed.

7) Evolution of the genus Melipona.

Since.Bombus is in several respects, a primitive form of social bee, the ancestral type of Meliponini and Apiniis described as having caste such, as in Bombus; there is difference of food determining castes; storage is in pots and old cocoons; cells for drones and workers of the same size, in clusters; wax is secreted by dorsal and ventral glands; etc.. By further development of the process for determining castes, by specialization of ventral wax glands, by adoption of a vertical system of combs, etc., the modern Apini have arisen.

By specialization of dorsal wax glands, loss of sting, improvement of storage in pots, combs of brood cells organized in clusters (like Trígona silvestrii, T. schrettkyi, T. duckei, T. iridipennis, T. minima. T. muelleri, etc.) the primitive Meliponini were obtained.

From thds type of primitive Meliponini, nearer to Trígona than Meliponain its biology, the modern stingless bees were derived.

The geographic distribution of the Meliponini is given, emphazising the fact that the Meliponabees are restricted to the Americas. It is shown also that the Meliponini are dis-continuously distributed.

According to H. G. Wells J. Huxley and G. P. Wells (1935) a distribution of any group of terrestrial animals depends of: 1st -region in which the group arose; 2and conections among this regions and other continental lands; 3rd - chances for survival for the group in the several regions into which it will pass.

Studying these three points, considerations were made about the fossils of the Meliponini and other social bees, about the several geographical links between South and North America and about the effects of the ice age and their importance for the distribution and evolution of the genus Melipona.

Owing to the restricted distribution of this genus it is suggested that it arose at about the Ice age, a little before or a little v after, which may explain why -it did not expand to other continents like Trígona.

There -are two types of genetical segregations of castes among the known Meliponas : one bifactorial (Aa Bb) and other trifactorial (Aa Bb Cc) suggesting that a primitive mo-nof actorial«type (Aa) must have existed or may still-exist.

The genetc evolution* of such Meliponas may _vbj&,r summarized as follows :

In a hive of a primitive Trígona (or Meliponaor Mellponorytes) with genetic constitution AA BB CC DD.... a mutation happened in a worker for the gene a withe-following effect: well developed sexual organs, independent of feeding, and greater precocity occur in heterozygote Aa. Owing to that well developed sexual organs and the fertility, independent from food supply, such a queen was prefered by the drone (A) to be fertilized when the old queen died.

' Since the gens tic çonstituion is Aa, it segregates into : 50% Aa and 50% AA. Both, these types of eggs, AA and Aa, could give queens, but (Aa) will be fertile in all circunstaces while. (AA) and (aa) remains dependent of the special feeding; this fact may be considerad as responsable for favorable selection and thus an increase of the new allele.

This type_; of selection may have lead to an accumulation of other modifying factors, increasing the tendency of the heterozygous, queen (Aa) for laying only and not working and to sterilize and increase the working ability of the homozygous (AA and aa). However, on, the other side, such a type can hardly survive for long, because 50% of its population would become unable to works.

It is supposed that the same was repeated with regard to a second mutation in another locus (B), and thus the caste becomes dependent upon a bifactorial segregation, the fertile females now being AaBb.

Before this mutation from B to b, there were A A BB or aa BB, and the queens Aa BB. The new combination Aa Bb should have special advantages against Aa BB such as: greater fertility or precocity, more atracliivine&s to the males, etc., so that the selection was in theür favor this strong selection permitted rearrangement of the modifiers so that they begin to cause a loss of fertility of all more or less homozygous animals, until they became workers. The bifactorial type became more frequent than the monofactorial one, since it causes a definite advantage: the proportion of workers was changed from 1:1 to the more favorable proportion of 3:1.

One representative of this type still exists at present: Melipona marginata with all its subspecies.

The origin of the trifactorial type may be explained by repetition of the same process. It is now assumed that a mutation of a gene (C) to (c) occured.

Again the complete heterozygotes (Aa Bb Cc) should be of advantages in selection, and there should occur a fenoti-pic reversion to workers in all queens partially homozygous. The new proportion between workers and queens is of 87,5% to 12,5%, being more favorable than the previous one, and thus the trifactorial determination became predominant.

Parallel or analogous cases of a fenotipic reversion are cited from breeding experiments. The following references are made concerning the occurence of changes in the "modifier shift": crosses in Nicotiana (Brieger, 1929), in Crepis (Hol-lingshead, 1930), and selections in pod corn (Brieger, 1943).

Thus the bifactorial Melipona marginata is considered as the most primitive type of Melipona.

One may consider Melipona fasciata (with exclusion of M. pujncticollis and M. conelnnula, which are suspected as having bifactorial determination of castes) as the most primitive trifactorial species since: a) it is in its behavor, variation and coloration the nearest to Melipona marginata.

b) It had the widest range ot distribution.

c) It is the most polymorphous species with the greatest number of subspecies:

M. fasciata - 22 subsp; M. Interrupta - 8 subsp; M. favosa - 7 subspecies; M. quadrifasciata, ML beecheii, M. schencki - 2 subsp; M. flavipennis, M. mandaçâia, M. quinqoefasciata, M. Subnitda, M. rufipes - 1 subspecies (Schwarz, 1932, 1938).

There may of course be still other causes for variation found in M. fasciata besides the hypothesis that it is the oldest species and thus had more time at its disposal for accumulating mutations.

We may accept as the most probable region of origin of the Meliponas the Amazon Valley, for the following reasons : 1st) The Amazon valley is the geographic center of the regions Inhabited by the Meliponas and since we are dealing with a relatively new genus it seems improbable to suppose that there may exist already a secondary center.

2nd) The Amazon valley represents also the zone of the greatest variation of this genus, as shown by the number of species, subspecies and varieties existing there, following Schwarz (1932, 1938), Ducfce (1916) and Marianno Filho (1911.)

As it is always the case with deductions about the phytogeny of any systematic group, these considerations for the genus Meliponaand on its caste determination are largely hypothetical, but we hope that the indirect evidence presented may be considered as a sufficient Justification.

Explanation of the principal figures

Fig. 5 - Comb of brood cells oí M. quadrifaseiata anthidioides showing helicoidal organization. As in fig. 4 one can see that all cells are of the same size.

Fig. 6 - Sexual mate organ of M. quadrifaseiata anthidioides.

Fig. 8 - Ovary of pupa of virgin queen of M. quadrifaseiata anthidiodes.

Fig. 10 - Ovary of pupa of worker of M. quadrifaseiata anthidioides.

Fig 11 - Ovary of old fecundated queen of M. schencki-schencki.

Fig. 12, 18, 19 - Somatic cells of worker showing 18 chromosomes.

Fig. 13 - Somatic cells of queen showing 18 chromosomes. Fig. 14 and 15 - Somatic cells of drone showing 9 chromosomes.

Fig. 20 to 40 - Spermatogenesis.

Fig 41 and 42 - Comb of Meliponaquadrifaseiata anthidioides (Fig. 41) andM. marginata marginata (Fig. 42) with the cells marked from which queens have emerged. The cells giving drones are not included.

Fig. 43 - Graphical representation of the segregation in the trifactorial Meliponas.

Fig. 44 - Graphic of the segregation in the M. marginata marginata.

Fig. 45 - Meteorological data.

Fig. 47 - Phylogenetic tree suggesting relationships of the various sub-families and tribes of bees, according to C. D. Michener (1944).

Fig. 48 - Worker of Mellponorytes succini, Tosi (1896).

Fig. 49 - Phylogeny of the genus Meliponabased on biological datas and caste determination.

Fig. 50 - Map showing the geographic distribution of the Meliponini.

Fig. 51 - Hive of Bombus lapidarius showing clusters of cocoons (like Trígona silvestrii), honey and polen pots (identical to that of all Meliponini) and old cocoons full with honey and polen (some identical to combs used by honey bee). (After F. W. Sladen - cited by Wheeler, 1923)

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Datas de Publicação

• Publicação nesta coleção
  05 Fev 2013
• Data do Fascículo
  1948