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A chromosome map of Belgica antarctica Jacobs (Diptera: Chironomidae) from Antarctica, including chromosome variability

Published online by Cambridge University Press:  02 October 2023

Paraskeva Michailova Open the ORCID record for Paraskeva Michailova [Opens in a new window] ,
Pavlo A. Kovalenko Open the ORCID record for Pavlo A. Kovalenko [Opens in a new window] ,
Svitlana Serga Open the ORCID record for Svitlana Serga [Opens in a new window] ,
Ivan Parnikoza Open the ORCID record for Ivan Parnikoza [Opens in a new window] ,
Iryna Kozeretska Open the ORCID record for Iryna Kozeretska [Opens in a new window]  and
Peter Convey Open the ORCID record for Peter Convey [Opens in a new window]
Paraskeva Michailova
Affiliation:
Institute of Biodiversity and Ecosystem Research at the Bulgarian Academy of Sciences, Sofia, 1000, Bulgaria
Pavlo A. Kovalenko*
Affiliation:
Institute for Evolutionary Ecology of the National Academy of Sciences of Ukraine, Kyiv, 03143, Ukraine National Antarctic Scientific Center of Ukraine, Kyiv, 01601, Ukraine
Svitlana Serga
Affiliation:
National Antarctic Scientific Center of Ukraine, Kyiv, 01601, Ukraine Taras Shevchenko National University of Kyiv, Kyiv, 01601, Ukraine CBGP, INRAE, CIRAD, IRD, SupAgro, University Montpellier, Montpellier, 34980, France
Ivan Parnikoza
Affiliation:
National Antarctic Scientific Center of Ukraine, Kyiv, 01601, Ukraine Institute of Molecular Biology and Genetics of National Academy of Science of Ukraine, Kyiv, 03143, Ukraine
Iryna Kozeretska
Affiliation:
National Antarctic Scientific Center of Ukraine, Kyiv, 01601, Ukraine
Peter Convey
Affiliation:
British Antarctic Survey, NERC, Cambridge, CB3 0ET, UK Department of Zoology, University of Johannesburg, Auckland Park, Johannesburg, 2006, South Africa Millennium Institute Biodiversity of Antarctic and Sub-Antarctic Ecosystems, Santiago, Chile
*
pavlo.kovalenko97@yahoo.com
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Abstract

Belgica antarctica Jacobs (Diptera: Chironomidae) is the only endemic insect found in the Antarctic Peninsula region and has stimulated considerable research interest. Due to recent rapid changes in regional climate in Antarctica, there is growing interest in studying the responses of this species to environmental changes, in particular at the chromosomal level. Chromosomal inversions are known to play an important role in speciation and adaptation in many insect species, but their frequencies in natural populations are poorly understood. In the current study, we provide the first standard polytene chromosome map for B. antarctica, which will enable the precise location of chromosomal abnormalities in future studies. We further analysed chromosomal polymorphisms in fourth-instar larvae collected from two different locations on Galindez Island, Argentine Islands, western coast of the Antarctic Peninsula. We found four previously reported and two new inherited inversions, and we discuss their possible adaptive role in response to environmental stressors in the Antarctic Peninsula region. Our data provide a foundation for future studies exploring the potential role of B. antarctica chromosomal polymorphisms in adaptation to the changing environment.

Keywords

Antarctic midgechromosome aberrationspolytene chromosomes
Type
Biological Sciences
Information
Antarctic Science , Volume 35 , Issue 5 , October 2023 , pp. 328 - 344
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Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press on behalf of Antarctic Science Ltd

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References

Allegrucci, G., Carchini, G., Convey, P. & Sbordoni, V. 2012. Evolutionary geographic relationships among orthocladine chironomid midges from maritime Antarctic and sub-Antarctic islands. Biological Journal of the Linnean Society, 106, 258–274.10.1111/j.1095-8312.2012.01864.xCrossRefGoogle Scholar
Atchley, W.R. & Davis, B.L. 1979. Chromosomal variability in the Antarctic insect, Belgica antarctica (Diptera: Chironomidae). Annals of the Entomological Society of America, 72, 246–252.CrossRefGoogle Scholar
Bargagli, R. 2020. Terrestrial ecosystems of the Antarctic Peninsula and their responses to climate change and anthropogenic impacts. Ukrainian Antarctic Journal, 2, 84–97.CrossRefGoogle Scholar
Bickham, J.W. & Smolen, M.J. 1994. Somatic and heritable effects of environmental genotoxins and the emergence of evolutionary toxicology. Environmental Health Perspectives, 102, 25–28.10.1289/ehp.94102s1225CrossRefGoogle ScholarPubMed
Chown, S.L. & Convey, P. 2016. Antarctic entomology. Annual Review of Entomology, 61, 119–137.10.1146/annurev-ento-010715-023537CrossRefGoogle ScholarPubMed
Chu, W.-L., Dang, N.-L., Kok, Y.-Y., Ivan Yap, K.-S., Phang, S.-M. & Convey, P. 2019. Heavy metal pollution in Antarctica and its potential impacts on algae. Polar Science, 20, 75–83.10.1016/j.polar.2018.10.004CrossRefGoogle Scholar
Clopper, C.J. & Pearson, E.S. 1934. The use of confidence or fiducial limits illustrated in the case of the binomial. Biometrika, 26, 404–413.10.1093/biomet/26.4.404CrossRefGoogle Scholar
Convey, P. & Block, W. 1996. Antarctic Diptera: ecology, physiology and distribution. European Journal of Entomology, 93, 1–13.Google Scholar
Convey, P. & Peck, L.S. 2019. Antarctic environmental change and biological responses. Science Advances, 5, eaaz0888.10.1126/sciadv.aaz0888CrossRefGoogle ScholarPubMed
Cornette, R., Gusev, O., Nakahara, Y., Shimura, S., Kikawada, T. & Okuda, T. 2015. Chironomid midges (Diptera, Chironomidae) show extremely small genome sizes. Zoological Science, 32, 248–254.CrossRefGoogle ScholarPubMed
Da Cunha, A.B. 1960. Chromosomal variation and adaptation in insects. Annual Review of Entomology, 5, 85–110.10.1146/annurev.en.05.010160.000505CrossRefGoogle Scholar
Devlin, J.J., Unfried, L., Lecheta, M.C., McCabe, E.A., Gantz, J.D., Kawarasaki, Y., et al. 2022. Simulated winter warming negatively impacts survival of Antarctica's only endemic insect. Functional Ecology, 36, 1949–1960.10.1111/1365-2435.14089CrossRefGoogle Scholar
Fischer, J. 1978. Zum problem der chromosomen - Evolution durch translokationen bei Chironomus (Diptera). Archiv für Genetik, 51, 73–98. [In German]Google Scholar
Fisher, R.A. 1922. On the interpretation of χ2 from contingency tables, and the calculation of P. Journal of the Royal Statistical Society, 85, 87–94.CrossRefGoogle Scholar
Fuller, Z.L., Leonard, C.J., Young, R.E., Schaeffer, S.W. & Phadnis, N. 2018. Ancestral polymorphisms explain the role of chromosomal inversions in speciation. PLoS Genetics, 14, e1007526.CrossRefGoogle ScholarPubMed
Gunderina, L., Golygina, V. & Broshkov, A. 2015. Chromosomal organization of the ribosomal RNA genes in the genus Chironomus (Diptera, Chironomidae). Comparative Cytogenetics, 9, 201–220.Google ScholarPubMed
Hoffmann, A.A. & Rieseberg, L.H. 2008. Revisiting the impact of inversions in evolution: from population genetic markers to drivers of adaptive shifts and speciation? Annual Review of Ecology, Evolution, and Systematics, 39, 21–42.CrossRefGoogle ScholarPubMed
Hoffmann, A.A., Sgrò, C.M. & Weeks, A.R. 2004. Chromosomal inversion polymorphisms and adaptation. Trends in Ecology and Evolution, 19, 482–488.CrossRefGoogle ScholarPubMed
Ilkova, J., Michailova, P., Szarek-Gwiazda, E., Kownacki, A. & Ciszewski, D. 2017. The response of genome of the Chironomidae (Diptera) to heavy metal pollution in two rivers of southern Poland. Acta Zoologica Bulgarica (Supplement), 8, 9–15.Google Scholar
John, B. & Lewis, K.R. 1966. Chromosome variability and geographic distribution in insects. Science, 152, 711–721.CrossRefGoogle ScholarPubMed
Kaiser, T.S., Poehn, B., Szkiba, D., Preussner, M., Sedlazeck, F.J., Zrim, A., et al. 2016. The genomic basis of circadian and circalunar timing adaptations in a midge. Nature, 540, 69–73.10.1038/nature20151CrossRefGoogle Scholar
Kapun, M., van Schalkwyk, H., McAllister, B., Flatt, T. & Schlötterer, C. 2014. Inference of chromosomal inversion dynamics from Pool-seq data in natural and laboratory populations of Drosophila melanogaster. Molecular Ecology, 23, 1813–1827.CrossRefGoogle ScholarPubMed
Kelley, J.L., Peyton, J.T., Fiston-Lavier, A.S., Teets, N.M., Yee, M.C., Johnston, J.S., et al. 2014. Compact genome of the Antarctic midge is likely an adaptation to an extreme environment. Nature Communications, 5, 4611.CrossRefGoogle Scholar
Keyl, H.G. 1962. Chromosomenevolution bei Chironomus. Chromosoma, 13, 464–514. [In German]10.1007/BF00327342CrossRefGoogle Scholar
Kiknadze, I., Istomina, A., Golygina, V. & Gunderina, L. 2016. Karyotypes of Palearctic and Holarctic species of the genus Chironomus. Novosibirsk: Academic Publishing House ‘Geo', 489 pp.Google Scholar
Kirkpatrick, M. 2010. How and why chromosome inversions evolve. PLoS Biology, 8, e1000501.CrossRefGoogle ScholarPubMed
Kirov, N., Wurtz, T. & Daneholt, B. 1991. The complexity of 75S premessenger RNA in Balbiani ring granules studied by a new RNA band retardation assay. Nucleic Acids Research, 19, 3377–3382.CrossRefGoogle ScholarPubMed
Kozeretska, I., Serga, S., Kovalenko, P., Gorobchyshyn, V. & Convey, P. 2022. Belgica antarctica (Diptera: Chironomidae): a natural model organism for extreme environments. Insect Science, 29, 2–20.CrossRefGoogle ScholarPubMed
Kruskal, W.H. & Wallis, W.A. 1952. Use of ranks in one-criterion variance analysis. Journal of the American Statistical Association, 47, 583–621.CrossRefGoogle Scholar
Magesh, N.S., Tiwari, A., Botsa, S.M. & da Lima Leitao, T. 2021. Hazardous heavy metals in the pristine lacustrine systems of Antarctica: insights from PMF model and ERA techniques. Journal of Hazardous Materials, 412, 125263.10.1016/j.jhazmat.2021.125263CrossRefGoogle ScholarPubMed
Martin, J. 1962. Inversion polymorphism in an Antarctic species living in a simple environment. The American Naturalist, 96, 317–318.10.1086/282239CrossRefGoogle Scholar
Martinez, J.L., Sanchez-Elsner, T., Morcillo, G. & Diez, J.L. 2001. Heat shock regulatory elements are present in telomeric repeats of Chironomus thummi. Nucleic Acid Research, 29, 4760–4766.CrossRefGoogle ScholarPubMed
Matheson, P. & McGaughran, A. 2023. How might climate change affect adaptive responses of polar arthropods? Diversity, 15, 47.CrossRefGoogle Scholar
Michailova, P.V. 1989. The polytene chromosomes and their significance to the systematics of the family Chironomidae, Diptera. Acta Zoologica Fennica, 186, 1–107.Google Scholar
Michailova, P.V. 1994. The role of heterochromatin in the speciation of family Chironomidae, Diptera. Folia Biologica, 42, 79–87.Google Scholar
Michailova, P.V., Sella, G. & Petrova, N. 2012. Chironomids (Diptera) and their salivary gland chromosomes as indicators of trace-metal genotoxicity. Italian Journal of Zoology, 79, 218–230.CrossRefGoogle Scholar
Michailova, P.V., Ilkova, J., Kovalenko, P., Dzhulai, A & Kozeretska, I. 2021. Long-term retainment of some chromosomal inversions in a local population of Belgica antarctica Jacobs (Diptera, Chironomidae). Czech Polar Reports, 11, 16–24.CrossRefGoogle Scholar
Noor, M.A.F., Grams, K.L., Bertucci, L.A. & Reiland, J. 2001. Chromosomal inversions and the reproductive isolation of species. Proceedings of the National Academy of Sciences of the United States of America, 98, 12084–12088.CrossRefGoogle ScholarPubMed
Ochyra, R., Smith, R.I.L. & Bednarek-Ochyra, H. 2008. The illustrated moss flora of Antarctica. Cambridge: Cambridge University Press, 704 pp.Google Scholar
Otto, S.P. & Barton, N.H. 1997. The evolution of recombination: removing the limits to natural selection. Genetics, 147, 879–906.CrossRefGoogle ScholarPubMed
Parnikoza, I., Abakumov, E., Korsun, S., Klymenko, I., Netsyk, M., Kudinov, A., et al. 2016. Soils of the Argentine Islands, Antarctica: diversity and characteristics. Polarforschung, 86, 83–96.Google Scholar
Peck, L.S., Convey, P. & Barnes, D.K.A. 2006. Environmental constraints on life histories in Antarctic ecosystems: tempos, timings and predictability. Biological Reviews, 81, 75–109.CrossRefGoogle ScholarPubMed
Richard, K.J., Convey, P. & Block, W. 1994. The terrestrial arthropod fauna of the Byers Peninsula, Livingston Island, South Shetland Islands. Polar Biology, 14, 371–379.CrossRefGoogle Scholar
Rinehart, J.P., Hayward, S.A.L., Elnitsky, M.A., Sandro, L.H., Lee, R.E. Jr & Denlinger, D.L. 2006. Continuous up-regulation of heat shock proteins in larvae, but not adults, of a polar insect. Proceedings of the National Academy of Sciences of the United States of America, 103, 14223–14227.10.1073/pnas.0606840103CrossRefGoogle Scholar
Sella, G., Bovero, S., Ginepro, M., Michailova, P., Petrova, N., Robotti, C.A., et al. 2004. Inherited and somatic cytogenetic variability in Palearctic populations of Chironomus riparius Meigen 1804 (Diptera, Chironomidae). Genome, 47, 332–344.CrossRefGoogle ScholarPubMed
Theodorakis, C.W. 2008. Mutagenesis. In Jørgensen, S.E. & Fath, B.D., eds, Encyclopedia of ecology. Oxford: Academic Press, 2475–2484.Google Scholar
Turner, J., Barrand, N., Bracegirdle, T., Convey, P., Hodgson, D., Jarvis, M., et al. 2014. Antarctic climate change and the environment: an update. Polar Record, 50, 237–259.CrossRefGoogle Scholar
Usher, M.B. & Edwards, M. 1984. A dipteran from south of the Antarctic Circle: Belgica antarctica (Chironomidae), with a description of its larvae. Biological Journal of the Linnean Society, 23, 19–31.CrossRefGoogle Scholar
Wellenreuther, M. & Bernatchez, L. 2018. Eco-evolutionary genomics of chromosomal inversions. Trends in Ecology and Evolution, 33, 427–440.CrossRefGoogle ScholarPubMed
White, B.J., Hahn, M.W., Pombi, M., Cassone, B.J., Lobo, N.F., Simard, F. & Besansky, N.J. 2007. Localization of candidate regions maintaining a common polymorphic inversion (2La) in Anopheles gambiae. PLoS Genetics, 3, e217.CrossRefGoogle ScholarPubMed
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