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First constitutive heterochromatin characterization and Karyotype of white stork Ciconia ciconia (Aves: Ciconiidae)

Primeira caracterização constitutiva de heterocromatina e cariótipo de cegonha-branca Ciconia ciconia (Aves: Ciconiidae)

Abstract

The karyotype and constitutive heterochromatin pattern of the white stork Ciconia ciconia samples obtained from Manzala lake, Dimiaat, Egypt was described. Somatic cells of Ciconia ciconia samples have diploid number 2n= 68 chromosomes. Out of 68 chromosomes, 11 pairs including sex chromosomes were macrochromosomes and the remaining pairs were microchromosomes. Of the 11 macrochromosome pairs, no.1, 2, 4 and 5 were submetacentric and pairs no. 6, 7 and 8 were described as metacentric. In addition, the autosome pair no.3 was subtelocentric, while autosome pair no.9 was acrocentric. Also, the sex chromosome Z represents the fourth one in size and it was classified as submetacentric while, W chromosome appeared as medium size and was acrocentric. Furthermore, C-banding pattern (constitutive heterochromatin) revealed variation in their sizes and occurrence between macrochromosomes. Pairs no. 7 and 8 of autosomes exhibited unusual distribution of heterochromatin, where they appeared as entirely heterochromatic. This may be related to the origin of sex chromosomes Z and W. However, there is no sufficient evidence illustrate the appearance of entirely heterochromatic autosomes. Therefore, there is no available cytogenetic literature that describes the C-banding and karyotype of Ciconia Ciconia, so the results herein are important and may assist in cytogenetic study and evolutionary pattern of Ciconiiformes.

Keywords:
karyotype; Ciconia ciconia; constitutive heterochromatin; Egypt

Resumo

O cariótipo e o padrão constitutivo de heterocromatina das amostras de cegonha-branca Ciconia ciconia obtidas no lago Manzala, Dimiaat, Egito, foram descritos. As células somáticas de amostras de Ciconia ciconia possuem número diploide 2n = 68 cromossomos. Dos 68 cromossomos, 11 pares incluindo cromossomos sexuais eram macrocromossomos e os pares restantes eram microcromossomos. Dos 11 pares de macrocromossomos, os nos 1, 2, 4 e 5 eram submetacêntricos, e os pares nos 6, 7 e 8 foram descritos como metacêntricos. Além disso, o par de autossomos no 3 era subtelocêntrico, enquanto o par de autossomos no 9 era acrocêntrico. Além disso, o cromossomo sexual Z representa o quarto em tamanho e foi classificado como submetacêntrico, enquanto o cromossomo W apareceu como de tamanho médio e acrocêntrico. Além disso, o padrão de bandamento C (heterocromatina constitutiva) revelou variação em seus tamanhos e ocorrência entre macrocromossomos. Pares nos 7 e 8 dos autossomos exibiram distribuição incomum de heterocromatina, onde apareceram como totalmente heterocromáticos. Isso pode estar relacionado à origem dos cromossomos sexuais Z e W. No entanto, não há evidências suficientes para ilustrar o aparecimento de autossomos totalmente heterocromáticos. Portanto, não há literatura citogenética disponível que descreva o bandamento C e o cariótipo de Ciconia ciconia, portanto os resultados aqui apresentados são importantes e podem auxiliar no estudo citogenético e no padrão evolutivo de Ciconiiformes.

Palavras-chave:
cariótipo; Ciconia ciconia; heterocromatina constitutiva; Egito

1. Introduction

The white stork, Ciconia ciconia belongs to the Ciconiiformes, family Ciconiidae. It has white plumage with black feather on the wings, the adults have long red legs and pointed red beaks. The breeding season of these birds is in central and southern Europe, the Middle East and west-central Asia during the warm summer months. Ciconia ciconia migrates to southern Africa in winter. It prefers drier habitats including grasslands, cultivated fields, and savannahs. In summer, they prefer freshwater habitats such as wet pastures, flood-plains, marshes, lakes and rice-fields for breeding.

Ciconiiformes are represented by five living families out of the seven which compose this major taxon (Sick and Barruel, 1997SICK, H. and BARRUEL, P., 1997. Ornitologia Brasileira, uma Introdução. Sao Paulo: Nova Fronteira. 912 p.; Welty and Baptista, 1988WELTY, J.C. and BAPTISTA, L., 1988. The Life of Birds. 4th ed. Orlando: Saunders College Publishing.). They include: Herons, Ibises, Spoonbills, and Storks. They are distinguished by long legs with slightly webbed feet and elongated toes. For feather maintenance, the middle toe of Ciconiiformes may be well developed. Most of them have long necks with vertebrae of 15 to 20 (Terry and Douglas, 2015TERRY, M. and DOUGLAS, P., 2015. Whiteside. In: R.E. MILLER and M.E. FOWLER, eds. Fowler's Zoo and Wild Animal Medicine. St. Louis: Elsevier.). Wild populations of these birds are currently vulnerable in several important ecosystems, mainly due to some environmental modifications caused by human activities (Gariboldi et al., 1998GARIBOLDI, J.C., JAGOE, C.H. and BRYAN JUNIOR, A.L., 1998. Dietary exposure to mercury in nestling wood storks (Mycteria americana) in Georgia. Archives of Environmental Contamination and Toxicology, vol. 34, no. 4, pp. 398-405. http://dx.doi.org/10.1007/s002449900336. PMid:9543511.
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). Families of Ciconiiformes are found in the Pantanal flood plain which extends throughout most of the Paraguay River hydrographic basin (Sick and Barruel, 1997SICK, H. and BARRUEL, P., 1997. Ornitologia Brasileira, uma Introdução. Sao Paulo: Nova Fronteira. 912 p.) and Mycteria americana(Ciconiidae) andPlatalea ajaja (Threskiornithidae) are more abundant species. However, the distribution of both species in Brazil has been reduced and several local populations are threatened with extinction or have already become extinct.

There are observable changes in the European population of the White Stork Ciconia ciconia, followed by a rapid decrease of reproduction success and an increase of mortality in the last five years (Daniluk et al., 2006DANILUK, J., DANILUK-KORBAL, A. and MITRUS, C., 2006. Changes in population size, breeding success and nest location of a local White Stork Ciconia ciconia population in Eastern Poland. In: P. TRYJANOWSKI, T.H. SPARKS and L. JERZAK, eds. The White Stork in Poland: studies in biology, ecology and conservation. Poznań: BoguckiWyd. Nauk, pp 15-21.; Kamiński et al., 2015KAMIŃSKI, P., GROCHOWSKA, E., MROCZKOWSKI, S., JERZAK, L., KASPRZAK, M., KOIM-PUCHOWSKA, B., WOŹNIAK, A., CIEBIERA, O. and MARKULAK, D., 2015. Sex ratio of White Stork Ciconia ciconia in different environments of Poland. Environmental Science and Pollution Research International, vol. 22, no. 17, pp. 13194-13203. http://dx.doi.org/10.1007/s11356-015-4250-z. PMid:25940461.
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and Zhang et al., 2014ZHANG, G., LI, C., LI, Q., LI, B., LARKIN, D.M., LEE, C., STORZ, J.F., ANTUNES, A., GREENWOLD, M.J., MEREDITH, R.W., ÖDEEN, A., CUI, J., ZHOU, Q., XU, L., PAN, H., WANG, Z., JIN, L., ZHANG, P., HU, H., YANG, W., HU, J., XIAO, J., YANG, Z., LIU, Y., XIE, Q., YU, H., LIAN, J., WEN, P., ZHANG, F., LI, H., ZENG, Y., XIONG, Z., LIU, S., ZHOU, L., HUANG, Z., AN, N., WANG, J., ZHENG, Q., XIONG, Y., WANG, G., WANG, B., WANG, J., FAN, Y., DA FONSECA, R.R., ALFARO-NÚÑEZ, A., SCHUBERT, M., ORLANDO, L., MOURIER, T., HOWARD, J.T., GANAPATHY, G., PFENNING, A., WHITNEY, O., RIVAS, M.V., HARA, E., SMITH, J., FARRÉ, M., NARAYAN, J., SLAVOV, G., ROMANOV, M.N., BORGES, R., MACHADO, J.P., KHAN, I., SPRINGER, M.S., GATESY, J., HOFFMANN, F.G., OPAZO, J.C., HÅSTAD, O., SAWYER, R.H., KIM, H., KIM, K.W., KIM, H.J., CHO, S., LI, N., HUANG, Y., BRUFORD, M.W., ZHAN, X., DIXON, A., BERTELSEN, M.F., DERRYBERRY, E., WARREN, W., WILSON, R.K., LI, S., RAY, D.A., GREEN, R.E., O’BRIEN, S.J., GRIFFIN, D., JOHNSON, W.E., HAUSSLER, D., RYDER, O.A., WILLERSLEV, E., GRAVES, G.R., ALSTRÖM, P., FJELDSÅ, J., MINDELL, D.P., EDWARDS, S.V., BRAUN, E.L., RAHBEK, C., BURT, D.W., HOUDE, P., ZHANG, Y., YANG, H., WANG, J., JARVIS, E.D., GILBERT, M.T., WANG, J., YE, C., LIANG, S., YAN, Z., ZEPEDA, M.L., CAMPOS, P.F., VELAZQUEZ, A.M.V., SAMANIEGO, J.A., AVILA-ARCOS, M., MARTIN, M.D., BARNETT, R., RIBEIRO, A.M., MELLO, C.V., LOVELL, P.V., ALMEIDA, D., MALDONADO, E., PEREIRA, J., SUNAGAR, K., PHILIP, S., DOMINGUEZ-BELLO, M.G., BUNCE, M., LAMBERT, D., BRUMFIELD, R.T., SHELDON, F.H., HOLMES, E.C., GARDNER, P.P., STEEVES, T.E., STADLER, P.F., BURGE, S.W., LYONS, E., SMITH, J., MCCARTHY, F., PITEL, F., RHOADS, D. and FROMAN, D.P., 2014. Comparative genomics reveals insights into avian genome evolution and adaptation. Science, vol. 346, no. 6215, pp. 1311-1320. http://dx.doi.org/10.1126/science.1251385. PMid:25504712.
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). Despite of the development of some DNA markers that help in detection of chicken microchromosomes, avian cytogenetics has not reached its full potential, and most bird cytogenetic data concerned only with macrochromosome (Damas et al., 2017DAMAS, J., O’CONNOR, R., FARRÉ, M., LENIS, V.P.E., MARTELL, H.J., MANDAWALA, A., FOWLER, K.E., JOSEPH, S., SWAIN, M., GRIFFIN, D.K. and LARKIN, D.M., 2017. Upgrading short-read animal genome assemblies to chromosome level using comparative genomics and a universal probe set. Genome Research, vol. 27, no. 5, pp. 875-884. http://dx.doi.org/10.1101/gr.213660.116. PMid:27903645.
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2. Materials and Methods

2.1. Sampling and study area

White stork Ciconia ciconia samples were obtained by local fisherman from lake Manzala, Damietta, during April to July month, 2015 year. Manzala is the largest natural lake of the Egyptian northern lakes along the Mediterranean coast in Egypt and is located between longitudes 31° 45ʹ and 32° 22ʹ E and latitudes 31° 00ʹ and 31° 35ʹ N. It is one of the most vulnerable lakes. It is an example of the wetland in Egypt and it was famous with water birds and a migration route for some birds from Europe to Africa along the Mediterranean Sea (Ayache et al., 2009AYACHE, F., THOMPSON, J., FLOWER, J., BOUJARRA, A., ROUATBI, F. and MAKINA, H., 2009. Environmental characteristics, landscape history and pressures on three coastal lagoons in the Southern Mediterranean Region: Merja Zerga (Morocco), Ghar El Melh (Tunisia) and Lake Manzala (Egypt). Hydrobiologia, vol. 622, pp. 15-43. http://dx.doi.org/10.1007/s10750-008-9676-6.
http://dx.doi.org/10.1007/s10750-008-967...
).

2.2. Conventional preparation

The mitotic chromosome preparations were carried out according to air drying method (Yosida, 1973YOSIDA, T.H., 1973. Evolution of karyotype and differentiation in 13 Rattus species. Chromosoma, vol. 40, pp. 285-297.) with some modifications by Ata et al. (2005ATA, A.M., SALHA, A.E.A., ALLAM, H.Z. and FANDY, W.A., 2005. Cytogenetic studies on three species of domestic birds (Galliformes, Aves): I-chromosomal morphology and C-banding analysis. Minia Journal of Agricultural Research and Development, vol. 25, pp. 977-1000., 2019ATA, A. M., ALLAM, H. Z., ABUUSALHA, A. E., FANDY, W. M. and SHNAF, A.S.M.A., 2019. Constitutive heterochromatin pattern of five domestic duck breeds, (Aves: Anatidae) in Egypt. Egyptian Academic Journal of Biological Sciences, vol. 11, no. 2, pp. 57-69.). About 50 metaphase plates from each sample were examined at X100 magnification and good spreads were photographed using an Olympus BX51 microscope with a C-4040 zoom digital camera. The karyotype was determined on the basis of 10 well-spread metaphase cells from each sample. Macrochromosomes were measured under the microscope using the Soft Imaging System (SIS) analysis program (Version3.0) edited in 1999 by Soft Imaging System GmbH, Germany, and classified according to the system of nomenclature proposed by Levan et al. (1964)LEVAN, A., FREDGA, K. and SANDBERG, A., 1964. Nomenclature for centromeric position on chromosomes. Hereditas, vol. 52, no. 2, pp. 201-220. http://dx.doi.org/10.1111/j.1601-5223.1964.tb01953.x.
http://dx.doi.org/10.1111/j.1601-5223.19...
.

2.3. C-banding technique

C-bands were obtained according to the standard protocol of Sumner (1972)SUMNER, A.T., 1972. A simple technique for demonstrating centromeric heterochromatin. Experimental Cell Research, vol. 75, no. 1, pp. 304-306. http://dx.doi.org/10.1016/0014-4827(72)90558-7. PMid:4117921.
http://dx.doi.org/10.1016/0014-4827(72)9...
with major modifications as described by Ata et al. (2005ATA, A.M., SALHA, A.E.A., ALLAM, H.Z. and FANDY, W.A., 2005. Cytogenetic studies on three species of domestic birds (Galliformes, Aves): I-chromosomal morphology and C-banding analysis. Minia Journal of Agricultural Research and Development, vol. 25, pp. 977-1000., 2019ATA, A. M., ALLAM, H. Z., ABUUSALHA, A. E., FANDY, W. M. and SHNAF, A.S.M.A., 2019. Constitutive heterochromatin pattern of five domestic duck breeds, (Aves: Anatidae) in Egypt. Egyptian Academic Journal of Biological Sciences, vol. 11, no. 2, pp. 57-69.) and Shahin et al. (2014)SHAHIN, A.A., ATA, A.T. and SHNAF, A.S., 2014. Karyotype and C-banding pattern of the domestic geese Anser anser populations (Aves: Anatidae) in Egypt. Folia Biologica, vol. 62, no. 1, pp. 49-58. PMid:24745149.. At least 10 metaphase spreads of each bird were photographed and analyzed using Olympus BX51 microscope with a C-4040 zoom digital camera. The C-band sizes and distribution on the macrochromosomes of Ciconia ciconia samples were described and the number of heterochromatin blocks per micro-chromosomes in the examined cells was recorded. The ideogram was constructed using Microsoft Excel 2010 program according to karyological measurements on white stork Ciconia ciconia samples.

3. Results

3.1. Karyotype

Results of the examined mitotic spreads of Ciconia ciconia samples obtained from Manzala lake, Damietta revealed that the diploid number of chromosomes was 2n= 68. The chromosome set consists of 11 pairs, including sex chromosomes are macrochromosomes, while the remaining pairs are microchromosomes. Of the 10 autosomes macrochromosome pairs, pairs no.1, 2, 4 and 5 were submetacentric with total length ranging from 2.31 ± 0.16 µm to 6.78 ± 0.46 µm; pairs no. 6, 7,8 and 10 were classified as metacentric with total length ranged from 1.11± 0.14 µm to 1.86 ± 0.18 µm as in Table 1 and Figure 1. In addition, the autosome pair no.3 was subtelocentric with total length 3.87 ± 0.48 µm, while autosome pair no.9 was acrocentric and its size was 1.21 ± 0.16 µm. Moreover, the sex chromosome Z represents the fourth one in size and it was classified as submetacentric while, W chromosome appeared as medium size and was acrocentric.

Table 1
Measurements and nomenclature of macrochromosomes of white stork Ciconia Ciconia.
Figure 1
Image of metaphase cell chromosomes (a) and karyotype (b) of male white stork Ciconia ciconia collected from Manzala lake, Dimette. Note the female ZW chromosomes are added in (b), numbers refer to macrochromosomes.

3.2. Constitutive heterochromatin description (C-banding)

The results of C-banding revealed variation in their sizes and occurrence between macrochromosomes as in Figure 2. In the present study, chromosome pair no.1 and 2 have small to medium sized telomeric C-band while chromosome pair no.3 has large centromeric C-band in addition to faint telomeric distal C-band. However, the acrocentric chromosome pair no.9 has large block of C-band. Moreover, the remained biarmed autosomes have varied size centromeric C-band except autosome pairs no. 7 and 8 appeared completely entirely heterochromatic. In the other hand, the sex chromosome Z has medium sized centromeric C-band in addition to telomeric (distal) part. In addition to the description of C-banding on macrochromosomes, constitutive heterochromatin dots were counted in each metaphase set in all the examined samples of Ciconia ciconia. The results revealed that the mean number of C-band blocks on microchromosomes per cell was (25.33 ± 2.1).

Figure 2
Image of C-band metaphase spread (a) of the male white stork Ciconia ciconia, and an Ideogram (b) of macro-chromosomes illustrates the position and size of C-heterochromatin in it. Note arrows indicate to pairs no.7 and 8 (entirely heterochromatic) and W chromosome is added to the Ideogram (b).

4. Discussion

There was no previous data on the karyotype and C-banding pattern of white stork Ciconia Ciconia, so the data presented herein are important. Therefore, it helps in animal reproduction program and takes part in the pool of knowledge on chromosome evolution of Ciconiiformes. In the present study, chromosomal results of white stork Ciconia Ciconia collected from Manzala lake, Damietta revealed that the diploid number of chromosomes was 2n= 68. According to the parallel studies on Ciconiidae, Francisco and Galetti Junior (2000)FRANCISCO, M.R. and GALETTI JUNIOR, P.M., 2000. First karyotypical description of two American Ciconiiform birds, Mycteria Americana (Ciconiidae) and Platalea ajaja (Threskiornithidae) and its significance for the chromosome evolutionary and biological conservation approaches. Genetics and Molecular Biology, vol. 23, no. 4, pp. 799-801. http://dx.doi.org/10.1590/S1415-47572000000400015.
http://dx.doi.org/10.1590/S1415-47572000...
reported that Mycteria americana had a diploid number 2n=72, which was karyotypically similar to the previously described Mycteria cinerea (Belterman and Boer, 1990BELTERMAN, R.H.B. and BOER, L.E.M., 1990. A miscellaneous collection of bird karyotypes. Genetica, vol. 83, no. 1, pp. 17-29. http://dx.doi.org/10.1007/+BF00774685.). In addition, (Belterman and Boer, 1990BELTERMAN, R.H.B. and BOER, L.E.M., 1990. A miscellaneous collection of bird karyotypes. Genetica, vol. 83, no. 1, pp. 17-29. http://dx.doi.org/10.1007/+BF00774685.) Mycteria cinerea (2n=72) may represent the ancestral karyotype of Ciconiids. The results in the present study were in consistent with the previously reported by Belterman and Boer (1984)BELTERMAN, R.H.B. and BOER, L.E.M., 1984. A karyological study of 55 species of birds, including karyotypes of 39 species new to cytology. Genetica, vol. 65, no. 1, pp. 39-82. http://dx.doi.org/10.1007/BF00056765.
http://dx.doi.org/10.1007/BF00056765...
; Belterman and Boer (1990)BELTERMAN, R.H.B. and BOER, L.E.M., 1990. A miscellaneous collection of bird karyotypes. Genetica, vol. 83, no. 1, pp. 17-29. http://dx.doi.org/10.1007/+BF00774685.; Boer and Van Brink (1982)BOER, L.E.M. and VAN BRINK, J.M., 1982. Cytotaxonomy of Ciconiiformes (Aves), with karyotypes of eight species new to cytology. Cytogenetics and Cell Genetics, vol. 34, no. 1-2, pp. 19-34. http://dx.doi.org/10.1159/000131791. PMid:7151490.
http://dx.doi.org/10.1159/000131791...
and Takagi and Sasaki (1974)TAKAGI, N. and SASAKI, M., 1974. A phylogenetic study of bird karyotypes. Chromosoma, vol. 46, no. 1, pp. 91-120. http://dx.doi.org/10.1007/BF00332341. PMid:4134896.
http://dx.doi.org/10.1007/BF00332341...
in which there was decreasing in the number of microchromosomes among these species. The reduction in some genome of birds may be an adaptive characteristic due to natural selection. Moreover, some authors observed that the excellent flayer birds have small genome than the largest one which is present in unflying birds (Hughes and Hughes, 1995HUGHES, A.L. and HUGHES, M.K., 1995. Small genomes for better flyers. Nature, vol. 377, no. 6548, pp. 391. http://dx.doi.org/10.1038/377391a0. PMid:7566113.
http://dx.doi.org/10.1038/377391a0...
; Hughes, 1999HUGHES, A.L., 1999. Adaptive evolution of genes and genomes. Oxford: Oxford University Press.). However, this opinion was doubted, because there was no sufficient evidence showing which came first, the ability to fly, or the decrease in genome size (Gregory, 2002GREGORY, T. R. 2002. Genome size and developmental complexity.Genetica, vol. 115, pp. 131-146.; Waltari and Edwards, 2002WALTARI, E. and EDWARDS, S.V., 2002. Evolutionary dynamics of intron size, genome size, and physiological correlates in archosaurs.The American Naturalist, vol. 160, no. 5, pp. 539–552. https://doi.org/10.1086/342079.
https://doi.org/10.1086/342079...
). The decreasing in number of microchromosomes may be a common chromosome evolutionary strategy in some bird groups (Francisco and Galetti Junior, 2000FRANCISCO, M.R. and GALETTI JUNIOR, P.M., 2000. First karyotypical description of two American Ciconiiform birds, Mycteria Americana (Ciconiidae) and Platalea ajaja (Threskiornithidae) and its significance for the chromosome evolutionary and biological conservation approaches. Genetics and Molecular Biology, vol. 23, no. 4, pp. 799-801. http://dx.doi.org/10.1590/S1415-47572000000400015.
http://dx.doi.org/10.1590/S1415-47572000...
). Besides, the reduction in number of micochromosomes may be due to chromosomal fusion (Nanda et. al., 2007NANDA, I., KARL, E., GRIFFIN, D.K., SCHARTL, M. and SCHMID, M., 2007. Chromosome re-patterning in three representative parrots (Psittaciformes) inferred from comparative chromosome painting. Cytogenetic and Genome Research, vol. 117, no. 1-4, pp. 43-53. http://dx.doi.org/10.1159/000103164. PMid:17675844.
http://dx.doi.org/10.1159/000103164...
). Moreover, the appearance of biarmed chromosomes may be due to occurrence of reciprocal translocation.

In the present study, results of karyotype revealed that of 68 chromosomes, 11 pairs, including sex chromosomes are macrochromosomes, while the remaining pairs are microchromosomes. Of the 10 autosomes macrochromosome, pairs no.1, 2, 4 and 5 were submetacentric that was in disagreement with Francisco and Galetti Junior (2000)FRANCISCO, M.R. and GALETTI JUNIOR, P.M., 2000. First karyotypical description of two American Ciconiiform birds, Mycteria Americana (Ciconiidae) and Platalea ajaja (Threskiornithidae) and its significance for the chromosome evolutionary and biological conservation approaches. Genetics and Molecular Biology, vol. 23, no. 4, pp. 799-801. http://dx.doi.org/10.1590/S1415-47572000000400015.
http://dx.doi.org/10.1590/S1415-47572000...
in Mycteria americana (Ciconidae). On contrary, results here in was in agreement with Francisco and Galetti Junior (2000)FRANCISCO, M.R. and GALETTI JUNIOR, P.M., 2000. First karyotypical description of two American Ciconiiform birds, Mycteria Americana (Ciconiidae) and Platalea ajaja (Threskiornithidae) and its significance for the chromosome evolutionary and biological conservation approaches. Genetics and Molecular Biology, vol. 23, no. 4, pp. 799-801. http://dx.doi.org/10.1590/S1415-47572000000400015.
http://dx.doi.org/10.1590/S1415-47572000...
in Mycteria americana (Ciconidae) in which chromosome pair no.3 was subteloceentric; pair no.9; W chromosome was telocentric and Z chromosome was submetacentric. The maintenance of a similar karyotype in Mycteria americana suggests a conservative chromosome evolutionary pattern within this genus. On the other side, the autosomes pairs no. 6, 7, 8 and 10 were metacentric.

Regarding the description of constitutive heterochromatin (C-banding) of the white stork Ciconia ciconia, there is no previously available literatures which describe the C-banding of Ciconia ciconia. In the present study, Pattern of constitutive heterochromatin of the white stork Ciconia ciconia represented by occurrence of variable sized centromeric C- bands in all macrochromosomes except autosome pairs nos.1 and 2 that have faint heterochromatin on the telomeric region. Chromosome pair no.3 has large centromeric C-band in addition to faint telomeric distal C-band. However, the acrocentric chromosome pair no.9 has large block of C-band while the remained biarmed pairs no. 4, 5, 6 and 10 autosomes have varied sizes of centromeric C-band. Moreover, the submetacentric Z chromosome has a small sized centromeric C-band in addition to faint distal portion. From the above-mentioned results, the obvious variation of C-banding distribution in white stork chromosomes may be attributed to the variation of euchromatin with chromosome size and arrangement of constitutive heterochromatin as reported by previous studies on avian taxa (Ata et al., 2005ATA, A.M., SALHA, A.E.A., ALLAM, H.Z. and FANDY, W.A., 2005. Cytogenetic studies on three species of domestic birds (Galliformes, Aves): I-chromosomal morphology and C-banding analysis. Minia Journal of Agricultural Research and Development, vol. 25, pp. 977-1000., 2017, 2019ATA, A. M., ALLAM, H. Z., ABUUSALHA, A. E., FANDY, W. M. and SHNAF, A.S.M.A., 2019. Constitutive heterochromatin pattern of five domestic duck breeds, (Aves: Anatidae) in Egypt. Egyptian Academic Journal of Biological Sciences, vol. 11, no. 2, pp. 57-69.; Shahin et al., 2014SHAHIN, A.A., ATA, A.T. and SHNAF, A.S., 2014. Karyotype and C-banding pattern of the domestic geese Anser anser populations (Aves: Anatidae) in Egypt. Folia Biologica, vol. 62, no. 1, pp. 49-58. PMid:24745149.; Yosida, 1973YOSIDA, T.H., 1973. Evolution of karyotype and differentiation in 13 Rattus species. Chromosoma, vol. 40, pp. 285-297.). On the other hand, chromosome pairs no. 7 and 8 appeared entirely heterochromatic as well as W sex chromosome. This unusual distribution of constitutive hetrochromatin on somatic chromosomes was previously reported by some studies on aves as in ducks (Ata et al., 2019ATA, A. M., ALLAM, H. Z., ABUUSALHA, A. E., FANDY, W. M. and SHNAF, A.S.M.A., 2019. Constitutive heterochromatin pattern of five domestic duck breeds, (Aves: Anatidae) in Egypt. Egyptian Academic Journal of Biological Sciences, vol. 11, no. 2, pp. 57-69.), passerine bird Erithacus savecicus (Bhunya and Sultana, 1982BHUNYA, S.P. and SULTANA, T., 1982. Unusual distribution of constitutive heterochromatin C-bands in the somatic chromosomes of a passerine bird Erithacus Svecicus. Experientia, vol. 38, no. 7, pp. 806-807. http://dx.doi.org/10.1007/BF01972283.
http://dx.doi.org/10.1007/BF01972283...
). However, there is no sufficient evidence illustrate this phenomenon. On the other hand, Bergero and Charlesworth, 2009BERGERO, R. and CHARLESWORTH, D., 2009. The evolution of restricted recombination in sex chromosomes. Trends in Ecology & Evolution, vol. 24, no. 2, pp. 94-102. http://dx.doi.org/10.1016/j.tree.2008.09.010. PMid:19100654.
http://dx.doi.org/10.1016/j.tree.2008.09...
; Mank, 2013MANK, J.E., 2013. Sex chromosome dosage compensation: definitely not for everyone. Trends in Genetics, vol. 29, no. 12, pp. 677-683. http://dx.doi.org/10.1016/j.tig.2013.07.005. PMid:23953923.
http://dx.doi.org/10.1016/j.tig.2013.07....
reported that appearance of entirely heterochromatic autosome may be related to the origin of Z and W sex chromosomes which, they thought that sex chromosomes might arise from the somatic chromosomes throughout recombination and/or chromosomal exchanges during evolutionary processes. Additionally, the C-banding heterochromatin dots of microchromosomes in the present study were small. This could be attributed to either transformation of heterochromatin into euchromatin and vice versa (Ata et al., 2019ATA, A. M., ALLAM, H. Z., ABUUSALHA, A. E., FANDY, W. M. and SHNAF, A.S.M.A., 2019. Constitutive heterochromatin pattern of five domestic duck breeds, (Aves: Anatidae) in Egypt. Egyptian Academic Journal of Biological Sciences, vol. 11, no. 2, pp. 57-69.; King, 1991KING, M., 1991. The evolution of heterochromatin in amphibian genome. In: D. M. GREEN and S. K. SESSIONS, eds. Amphipian Cytogenetics and Evolution. New York: Academic Press, pp. 359-381.; Shahin et al., 2014SHAHIN, A.A., ATA, A.T. and SHNAF, A.S., 2014. Karyotype and C-banding pattern of the domestic geese Anser anser populations (Aves: Anatidae) in Egypt. Folia Biologica, vol. 62, no. 1, pp. 49-58. PMid:24745149.) or to involvement of structural chromosomal aberrations during karyotype evolution (White, 1973WHITE, M. J. D., 1973. Animal Cytology and Evolution. 3rd ed. Cambridge: Cambridge University Press.).

5. Conclusion

The diploid chromosome number of white storks Ciconia Ciconia collected from Manzala lake, Damietta was 2n= 68 chromosomes. 11 pairs, including sex chromosomes are macrochromosomes, while the remaining pairs are microchromosomes. C-banding description of the white stork Ciconia ciconia showed variable sized centromeric C- bands in all macrochromosomes except autosome pairs nos.1 and 2 that have faint heterochromatin on the telomeric region. In addition, autosomes pairs no. 7 and 8 appeared entirely heterochromatic.

Acknowledgements

This work was supported by Researchers Supporting Project number (RSP-2021–104) King Saud University, Riyadh, Saudi Arabia. Grateful acknowledgment is to Prof. Dr. Abdeltawab M. Ata, department of Genetics, faculty of Agriculture, Minia University, for his truthful help in reviewing the paper.

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Publication Dates

  • Publication in this collection
    15 Sept 2021
  • Date of issue
    2023

History

  • Received
    16 Feb 2021
  • Accepted
    27 Apr 2021
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