Cytological Characterisation of Autosomes and Sex Chromosomes in Tephritid Fruit Flies Bactrocera zonata and Zeugodacus tau (Diptera, Tephritidae)

F. Yesmin; D. Haymer; M.  Nazim Uddin; M.  Hasanuzzaman

doi:10.15407/zoo2025.01.021

F. Yesmin Cytology and Biocontrol Research (CBR), Radiation Entomology and Acarology Division (READ), Institute of Food and Radiation Biology (IFRB), Atomic Energy Research Establishment (AERE), Bangladesh Atomic Energy Commission (BAEC) https://orcid.org/0000-0002-6661-0691
D. Haymer Department of Cell and Molecular Biology, University of Hawaii, Honolulu, USA https://orcid.org/0000-0002-0226-7062
M. Nazim Uddin Darshana Government College, Chuadanga, Bangladesh
M. Hasanuzzaman Cytology and Biocontrol Research (CBR), Radiation Entomology and Acarology Division (READ), Institute of Food and Radiation Biology (IFRB), Atomic Energy Research Establishment (AERE), Bangladesh Atomic Energy Commission (BAEC) https://orcid.org/0000-0002-7390-5412

DOI: https://doi.org/10.15407/zoo2025.01.021

Keywords: peach fruit fly, pumpkin fruit fly, metaphase spreads, chromosome morphology

Abstract

Two fruit fly species, Bactrocera zonata (Saunders, 1842) and Zeugodacus tau (Walker, 1849) (Diptera: Tephritidae) were studied with regard to their autosomes and sex chromosomes from mitotic metaphase spreads. Both species are native to South and South- East Asia and have major economic impacts in agriculture sectors of these areas. They are polyphagous, can easily adapt and spread. Both of them have the same diploid chromosome number of 2n = 12 (10 autosomes + heteromorphic sex chromosome pair XX/ XY). The male is heterogametic (XY) and the female is homogametic (XX). Chromosomes were classiﬁed into groups on the basis of centromere position and arranged in order of decreasing size. For B. zonata, chromosome formula is (3sm + 2m + Xm + Ydot-shape) and for Z. tau, the formula is (1sm + 4m + Xm + Ydot-shape). The results are analyzed and compared to chromosome studies done for other species of Tephritid fruit flies using chromosome morphometrics. Detailed images of mitotic chromosomes and measurements of various parameters relating to these chromosomes are provided. These cytological data are useful for systematics and contribute to a better understanding of the chromosomal evolution of these fruit fly species.

References

Augustinos, A., Drosopoulou, E., Gariou-Papalexiou, A., Bourtzis, K., Mavragani-Tsipidou, P. & Zacharopoulou, A. 2014. The Bactrocera dorsalis species complex: comparative cytogenetic analysis in support of Sterile Insect Technique applications. BMC Genetics, 15 suppl. 2, 1-16.

https://doi.org/10.1186/1471-2156-15-S2-S16

Baimai, V., Harrison, B. A. & Somchit, L. 1981. Karyotype differentiation of three anopheline taxa in the Balabacensis complex of Southeast Asia (Diptera: Culicidae). Genetica, 57, 81-86.

https://doi.org/10.1007/BF00131231

Baimai, V., Green, C. A., Andre, R. G., Harrison, B. A. & Peyton, E. L. 1984. Cytogenetics studies of some species complexes of Anopheles in Thailand and Southeast Asia. Southeast Asian Journal of Tropical Medicine and Public Health, 15 (4), 536-546. PMID: 6543543

Baimai, V., Trinachartvanit, W., Tigvattananont, S., Grote, P. J., Poramacom, R. & Kijchalao, U. 1995. Metaphase karyotypes of fruit flies of Thailand. I. Five sibling species of the Bactrocera dorsalis complex. Genome, 38 (5), 1015-1022.

https://doi.org/10.1139/g95-134

Baimai, V., Trinachartvanit, W., Tigvattananont, S. & Grote P. J. 1996. Metaphase karyotypes of fruit flies of Thailand. II. Five species of four subgenera of Bactrocera. Journal of the Science Society of Thailand, 22, 97-104.

Baimai, V., Phinchongsakddit, J. &Trinachartvanit, W. 1999 a. Metaphase karyotypes of fruit flies of Thailand (III). Six members of the Bactrocera dorsalis complex. Zoological Studies, 38, 110-118.

Baimai, V., Phinchongsakuldit, J. & Trnachartvanit, W. 1999 b. Metaphase karyotypes of fruit flies of Thailand (IV): Evidence for six new species of the Bactrocera dorsalis complex. Cytologia, 64, 371-377.

https://doi.org/10.1508/cytologia.64.371

Baimai, V., Phinchongsakuldit, J. & Sumrandee, C. 2000. Cytological evidence for a complex of species within the taxon Bactrocera tau (Diptera: Tephritidae) in Thailand. Biological Journal of the Linnean Society, 69 (3), 399-409.

https://doi.org/10.1111/j.1095-8312.2000.tb01213.x

Bedo, D. G. 1987. Polytene chromosome mapping in Ceratitis capitata (Diptera: Tephritidae). Genome, 29 (4), 598-611. .

https://doi.org/10.1139/g87-101

Bhatnagar, S., Kaul, D. & Chaturvedi, R. 1980. Chromosomal studies in three species of the genus Dacus (Trypetidae: Diptera). Genetica, 54, 11-15.

https://doi.org/10.1007/BF00122402

Bonizzoni, M., Zheng, L., Guglielmino, C., Haymer, D., Gasperi, G., Gomulski, G. & Malacrida, A. 2001. Microsatellite analysis of medfly bioinfestations in California. Molecular Ecology,

https://doi.org/10.1046/j.0962-1083.2001.01376.x

Boontop, Y., Schutze, M. K., Clarke, A. R., Cameron, S. L. & Krosch, M. N. 2017. Signatures of invasion: using an integrative approach to infer the spread of melon ﬂy, Zeugodacus cucurbitae (Diptera: Tephritidae), across Southeast Asia and the West Paciﬁc. Biological Invasions, 19, 1597-1619.

https://doi.org/10.1007/s10530-017-1382-8

Canovai, R., Macelloni, G. & Galleni, L. 1996. Karyology of some Italian populations of the olive fly Bactroceraoleae (Gmelin) (Diptera: Tephritidae). Caryologia, 49 (3-4), 247-255.

https://doi.org/10.1080/00087114.1996.10797369

Dillon, M. K., Sing, M., Naresh, J. S. & Sharma, H. C. 2005. The melon fruit fly, Bactroceracucurbitae: A review of its biology and management. Journal of Insect Science, 5 (40), 1-16.

https://doi.org/10.1093/jis/5.1.40

Drew, R. A. I. 1989. The Tropical fruit flies (Diptera: Tephritidae: Dacinae) of the Australasian and Oceanian regions. Memoirs of the Queensland Museum, 26, 1-521.

Drew, R. A. I. & Romig, M. 2013. Tropical fruit flies of South-East Asia (Tephritidae: Dacinae). CAB International, Wallingford, UK, i-vii + 1-653.

Drosopoulou, E., Koeppler, K., Kounatidis, I., Nakou, I. & Papadopoulos, N. T. 2010. Genetic and cytogenetic analysis of the walnut-husk fly (Diptera: Tephritidae). Annals of the Entomological Society of America, 103 (6), 1003-1011.

https://doi.org/10.1603/AN10059

Drosopoulou, E., Augustinos, A. A., Nakou, I., Koeppler, K., Kounatidis, I., Vogt, H., Papadopoulos, N. T., Bourtzis, K. & Mavragani-Tsipidou, P. 2011 a. Genetic and cytogenetic analysis of the American cherry fruit fly, Rhagoletis cingulata (Diptera: Tephritidae). Genetica, 139 (11-12), 1449-1464.

https://doi.org/10.1007/s10709-012-9644-y

Drosopoulou, E., Nestel, K., Nakou, I., Kounatidis, I., Papadopoulos, N. T., Bourtzis, K. & Mavragani-Tsipidou, P. 2011 b. Cytogenetic analysis of the Ethiopian fruit fly Dacus ciliatus (Diptera: Tephritidae). Genetica, 139, 723-732.

https://doi.org/10.1007/s10709-011-9575-z

Duyck, P.F., Sterlin, J.F. &Quilici, S. 2004. Survival and development of different life stages of Bactrocera zonata (Diptera: Tephritidae) reared at five constant temperatures compared to other fruit fly species. Bulletin of Entomological Research, 94, 89-93.

https://doi.org/10.1079/BER2003285

Duyck, P. F., David, P. & Quilici, S. 2007. Can more K-selected species be better invaders? A case study of fruit flies in La Reunion. Diversity and Distributions, 13, 535-543.

https://doi.org/10.1111/j.1472-4642.2007.00360.x

EPPO 2020. EPPO Global database. In: EPPO Global database, Paris, France: EPPO.

Green, C. A. & Baimai, V. 1985. Cytogenetic evidence for a complex of species within the taxon Anopheles maculatus (Diptera: Culicidae). Biological Journal of the Linnean Society, 24 (4), 321-328.

https://doi.org/10.1111/j.1095-8312.1985.tb00378.x

Hasyim, A., Muryati, I. M. & de Kogel, W. J. 2007. Male fruit fly, Bactrocera tau (Diptera; Tephritidae) Attractants from ElsholtziapubescensBth. Asian Journal of Plant Sciences, 6 (1), 181-183.

https://doi.org/10.3923/ajps.2007.181.183

Hunwattanakul, N. & Baimai, V. 1994. Mitotic karyotypes of four species of fruit flies (Bactrocera) in Thailand. Kasetsart Journal Natural Sciences, 28 (1), 142-148.

Leblanc, L., Hossain, M. A., Khan, S. A., San Jose, M. & Rubinoff, D. 2014. Additions to the fruit fly fauna (Diptera: Tephritidae: Dacinae) of Bangladesh, with a key to the species. Proceedings of the Hawaiian Entomological Society, 46, 31-40.

Leblanc, L., Hossain, M. A., Doorenweerd, G., Khan, S. A., Momen, M., San Jose, M. & Rubinoff, D. 2019. Six years of fruit fly surveys in Bangladesh: a new species, 33 new country records and discovery of the highly invasive Bactrocera carambolae (Diptera: Tephritidae). Zookeys, 876, 87-109.

https://doi.org/10.3897/zookeys.876.38096

Lemeunier, F. & Ashburner, M. 1976. Relationships within the Melanogaster species subgroup of the genus Drosophila (Sophophora) II. Phylogenetic relationships between six species based upon polytene chromosome banding sequences. Proceedings of the Royal Society ofLondon.,193, 275-294.

https://doi.org/10.1098/rspb.1976.0046

Levan, A., Fredga, K. & Sandberg, A. A. 1964. Nomenclature for centromeric position on chromosomes. Heriditas, 52 (2), 201-220.

https://doi.org/10.1111/j.1601-5223.1964.tb01953.x

Li, X., Yang, H., Hu, K. & Wang, J. 2020. Temporal dynamics of Bactrocera (Zeugodacus) tau (Diptera: Tephritidae) adults in north Jiangxi, a subtropical area of China revealed by eight years of trapping with cuelure. Journal of Asia Pacific Entomology, 23, 1-6.

https://doi.org/10.1016/j.aspen.2019.10.007

Mavragani-Tsipidou, P., Karamanlidou, G., Zacharopoulou, A., Koliais, S. & Kastritsis, C. 1992. Mitotic and polytene chromosome analysis in Dacus oleae (Diptera: Tephritidae). Genome,35 (3), 373-378.

https://doi.org/10.1139/g92-056

Morgante, J. S., Sevilon, D., Solferini, V. N. & Matioli, S. R. 1993. Evolutionary patterns in specialist and generalist species of Anastrepha. In: Aluja M, Liedo P., eds. Fruit Flies: Biology and Management. New York, Springer Verlag, 14-20.

https://doi.org/10.1007/978-1-4757-2278-9_3

Mosleh, Y. Y., Moussa, S. F. M. & Mohamed, L. H. Y. 2011. Comparative toxicity of certain pesticides to Peach fruit fly, Bactrocerazonata Saunders (Diptera: Tephritidae) under laboratory conditions. Plant Protection Science, 47 (3), 115-120.

https://doi.org/10.17221/52/2009-PPS

Radu, M., Rossle, Y. & Koltin, Y. 1975. The chromosomes of the Mediterranean fruit fly Ceratitis capitata (Wied.): karyotype and chromosomal organization. Cytologia, 40 (3-4), 823-828.

https://doi.org/10.1508/cytologia.40.823

Robertson, J. G. 1957. Somatic metaphase chromosomes in geographic isolates of the Carrot rust fly, Chamaepsilarosae (F.) (Diptera: Psilidae). Canadian Journal of Zoology, 35 (3), 453-458.

https://doi.org/10.1139/z57-037

Rothfels, K. 1979. Cytotaxonomy of black flies (Simulidae). Annual Review of Genetics, 24, 507-539.

https://doi.org/10.1146/annurev.en.24.010179.002451

Schutze, M. K et al. 2015. Synonymization of key pest species within the Bactrocera dorsalis species complex (Diptera: Tephritidae): taxonomic changes based on a review of 20 years of integrative morphological, molecular, cytogenetic, behavioral and chemoecological data. Systematic Entomology, 40 (2), 456-471.

https://doi.org/10.1111/syen.12113

Shahjahan, R. M. & Yesmin, F. 2002. Polytene chromosome maps of the melon fly, Bactrocera cucurbitae (Coq.) (Diptera: Tephritidae). Genome, 45 (6), 1167-1174.

https://doi.org/10.1139/g02-081

Vargas, R. I., Mau, R. F. L., Jang, E. B., Faust, R. M, & Wong, L. 2008. The Hawaii fruit fly area wide pest management programme. In: Koul, O., Cuperus, G., eds. Area wide Pest Management: Theory and Implementation. CABI Books, London, UK, 300-325.

https://doi.org/10.1079/9781845933722.0300

Virgilio, M., Jordaens, K., Verwimp, C., White, I. M. & De Meyer, M. 2015. Higher phylogeny of frugivorous flies (Diptera, Tephritidae, Dacini): Localised partition conflicts and a novel generic classification. Molecular Phylogenetics and Evolution, 85, 171-179.

https://doi.org/10.1016/j.ympev.2015.01.007

White, I. M. & Evenhuis, N. L. 1999. New species and records of Indo-Australasian Dacini (Diptera: Tephritidae). Raffles Bulletin of Zoology, 47, 487-540. ISSN, 0217-2445.

Yesmin, F. & Clyde, M. M. 2011. Fruit flies of economic importance: Karyotype studies on some Bactrocera spp. 59th Annual Meeting of the Entomological Society of America, Entomology 2011, 13-16 Nov. Reno, Nevada, USA, 45. http://esa.confex.com/esa/2011/webprogram/Paper60502.html

Yesmin, F. & Clyde, M. M. 2012. The chromosomes of the Carambola fruit fly Bactrocera carambolae (Diptera: Tephritidae): Metaphase karyotype and polytene genome. GSTF Journal of BioSciences, 1 (2), 1-15.

Yesmin, F. 2013. Chromosomes of Bactrocera papayae Drew and Hancock and Bactrocera carambolae Drew and Hancock (Diptera: Tephritidae): Mitotic metaphase karyotype and polytene genome. PhD Thesis, Universiti Kebangsaan Malaysia (UKM), Malaysia.

Yesmin, F. & Clyde, M. M. 2014. Cytological study of the Asian papaya fruit fly, Bactrocera papayae. Acta Horticulturae (ISHS), 1024, 301-305.

https://doi.org/10.17660/ActaHortic.2014.1024.41

Zacharopoulou, A., Sayed, W. A. A., Augustinos, A. A., Yesmin, F., Robinson, A. S. & Franz, G. 2011. Analysis of Mitotic and polytene chromosomes and photographic polytene chromosome maps in Bactrocera cucurbitae (Diptera: Tephritidae). Annals of the Entomological Society of America, 104 (2), 306-318.

https://doi.org/10.1603/AN10113

Zacharopoulou, A., Augustinos, A. A., Drosopoulou, E., Tsoumani, K. T, Gariou-Papalexiou, A., Franz. G., Mathiopoulos, K. D., Bourtzis, K. & Mavragani-Tsipidou, P. 2017. A review of more than 30 years of cytogenetic studies of Tephritidae in support of sterile insect technique and global trade. Entomologia Experimentaliset Applicata, 164, 204-225.

https://doi.org/10.1111/eea.12616

Zhao, J. T., Frommer, M., Sved, J. A. & Zacharopoulou, A. 1998. Mitotic and polytene chromosome analyses in the Queensland fruit fly, Bactrocera tryoni (Diptera: Tephritidae). Genome, 41, 510-526.

https://doi.org/10.1139/g98-053