Ukrainian Antarctic Journal

Vol 22 No 2(29) (2024): Ukrainian Antarctic Journal
Articles

Chromosomal polymorphism of Belgica antarctica populations: possible links on ecology and geography

Pavlo Kovalenko
State Institution Institute for Evolutionary Ecology, National Academy of Sciences of Ukraine, Kyiv, 03143, Ukraine; State Institution National Antarctic Scientific Center, Ministry of Education and Science of Ukraine, Kyiv, 01601, Ukraine
Published December 31, 2024
Keywords
  • chromosomal aberration frequency,
  • chromosome variability,
  • endemic species,
  • polar insect,
  • salivary gland
How to Cite
Kovalenko, P. (2024). Chromosomal polymorphism of Belgica antarctica populations: possible links on ecology and geography. Ukrainian Antarctic Journal, 22(2(29), 198-218. https://doi.org/10.33275/1727-7485.2.2024.737

Abstract

Chromosomal inversion polymorphism is an important evolutionary mechanism for many species, particularly insects. Belgica antarctica (Chironomidae) is the only endemic insect of the Antarctic Peninsula and is currently considered a model organism for studying adaptations of living organisms to climate change in the extreme terrestrial ecosystems of Antarctica. This polar midge has salivary gland polytene chromosomes, making it convenient for investigating various chromosomal aberrations and analysing their potential relationship with geographical and ecological factors. In this study, chromosomal polymorphism was analysed in the salivary glands of 99 fourth-instar larvae of Belgica antarctica, collected in four different localities in the West Antarctic Peninsula region in 2022. Six of the seven previously described heritable heterozygous inversions for this species were found in the newly tested populations. Notably, the precise location of a large inversion in chromosome I, containing the nucleolar organizer region, was identified for the first time since its discovery in 1962. Additionally, the data on chromosomal inversion frequencies
were combined with all currently available data – together from 1436 Belgica antarctica individuals across 26 populations, from 1962 to 2022, to determine potential links to specific ecological (ecological complexity, ornithogenic influence, and whether samples were collected from nesting or non-nesting material) and geographical (longitude and latitude) factors. It was found that, overall, the ecological factors do not affect the frequency of the studied inversions. However, slight trends were observed in the frequency of four heterozygous rearrangements with latitude, as well as the frequency of specimens with at least one non-sex-linked heterozygous inversion with longitude.

References

  1. Ajayi, O. M., Gantz, J. D., Finch, G., Lee, R. E., Denlinger, D. L., & Benoit, J. B. (2021). Rapid stress hardening in the Antarctic midge improves male fertility by increasing courtship success and preventing decline of accessory gland proteins following cold exposure. The Journal of Experimental Biology, 224(14), jeb242506. https://doi.org/10.1242/jeb.242506
  2. 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(2), 258–274. https://doi.org/10.1111/j.1095-8312.2012.01864.x
  3. 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(2), 246–252. https://doi.org/10.1093/aesa/72.2.246
  4. Ayala, D., Guerrero, R. F., & Kirkpatrick, M. (2013). Reproductive isolation and local adaptation quantified for a chromosome inversion in a malaria mosquito. Evolution, 67(4), 946–958. https://doi.org/10.1111/j.1558-5646.2012.01836.x
  5. Balanyá, J., Oller, J. M., Huey, R. B., Gilchrist, G. W., & Serra, L. (2006). Global genetic change tracks global climate warming in Drosophila subobscura. Science, 313(5794), 1773–1775. https://doi.org/10.1126/science.1131002
  6. Bargagli, R. (2020). Terrestrial ecosystems of the Antarctic Peninsula and their responses to climate change and anthropogenic impacts. Ukrainian Antarctic Journal, (2), 84–97. https://doi.org/10.33275/1727-7485.2.2020.656
  7. Bartlett, J. C., Convey, P., Newsham, K. K., & Hayward, S. A. L. (2023). Ecological consequences of a single introduced species to the Antarctic: Terrestrial impacts of the invasive midge Eretmoptera murphyi on Signy Island. Soil Biology and Biochemistry, 180, 108965. https://doi.org/10.1016/j.soilbio.2023.108965
  8. Bartlett, J. C., Convey, P., Pertierra, L. R., & Hayward, S. A. L. (2020). An insect invasion of Antarctica: The past, present and future distribution of Eretmoptera murphyi (Diptera, Chironomidae) on Signy Island. Insect Conservation and Diversity, 13(1), 77–90. https://doi.org/10.1111/icad.12389
  9. Baust, J. G., & Edwards, J. S. (1979). Mechanisms of freezing tolerance in an Antarctic midge, Belgica antarctica. Physiological Entomology, 4(1), 1–5. https://doi.org/10.1111/j.1365-3032.1979.tb00171.x
  10. Benoit, J. B., Lopez-Martinez, G., Elnitsky, M. A., Lee, R. E., & Denlinger, D. L. (2009). Dehydration-induced cross tolerance of Belgica antarctica larvae to cold and heat is facilitated by trehalose accumulation. Comparative Biochemistry and Physiology: Part A, Molecular & Integrative Physiology, 152(4), 518–523. https://doi.org/10.1016/j.cbpa.2008.12.009
  11. Berdan, E. L., Barton, N. H., Butlin, R., Charlesworth, B., Faria, R., Fragata, I., Gilbert, K. J., Jay, P., Kapun, M., Lotterhos, K. E., Mérot, C., Durmaz Mitchell, E., Pascual, M., Peichel, C. L., Rafajlović, M., Westram, A. M., Schaeffer, S. W., Johannesson, K., & Flatt, T. (2023). How chromosomal inversions reorient the evolutionary process. Journal of Evolutionary Biology, 36(12), 1761–1782. https://doi.org/10.1111/jeb.14242
  12. Berdan, E. L., Mérot, C., Pavia, H., Johannesson, K., Wellenreuther, M., & Butlin, R. K. (2021). A large chromosomal inversion shapes gene expression in seaweed flies (Coelopa frigida). Evolution Letters, 5(6), 607–624. https://doi.org/10.1002/evl3.260
  13. Castro, M. F., Neves, J. C. L., Francelino, M. R., Schaefer, C. E. G. R., & Oliveira, T. S. (2021). Seabirds enrich Antarctic soil with trace metals in organic fractions. Science of the Total Environment, 785, 147271. https://doi.org/10.1016/j.scitotenv.2021.147271
  14. Chown, S. L., & Convey, P. (2016). Antarctic Entomology. Annual Review of Entomology, 61, 119–137. https://doi.org/10.1146/annurev-ento-010715-023537
  15. Chown, S. L., Clarke, A., Fraser, C. I., Cary, S. C., Moon, K. L., & McGeoch, M. A. (2015). The changing form of Antarctic biodiversity. Nature, 522(7557), 431–438. https://doi.org/10.1038/nature14505
  16. Christmas, M. J., Wallberg, A., Bunikis, I., Olsson, A., Wallerman, O., & Webster, M. T. (2019). Chromosomal inversions associated with environmental adaptation in honeybees. Molecular Ecology, 28(6), 1358–1374. https://doi.org/10.1111/mec.14944
  17. 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. https://doi.org/10.1016/j.polar.2018.10.004
  18. Chwedorzewska, K. J., Korczak-Abshire, M., & Znój, A. (2020). Is Antarctica under threat of alien species invasion? Global Change Biology, 26(4), 1942–1943. https://doi.org/10.1111/gcb.15013
  19. Clopper, C. J., & Pearson, E. S. (1934). The use of confidence or fiducial limits illustrated in the case of the binomial. Biometrika, 26(4), 404–413. https://doi.org/10.1093/biomet/26.4.404
  20. Convey, P., & Block, W. (1996). Antarctic diptera: Ecology, physiology and distribution. European Journal of Entomology, 93(1), 1–13.
  21. Convey, P., & Peck, L. S. (2019). Antarctic environmental change and biological responses. Science Advances, 5(11), eaaz0888. https://doi.org/10.1126/sciadv.aaz0888
  22. Darham, S., Zakaria, N. N., Zulkharnain, A., Sabri, S., Khalil, K. A., Merican, F., Gomez-Fuentes, C., Lim, S., & Ahmad, S. A. (2023). Antarctic heavy metal pollution and remediation efforts: State of the art of research and scientific publications. Brazilian Journal of Microbiology, 54(3), 2011–2026. https://doi.org/10.1007/s42770-023-00949-9
  23. Devlin, J. J., Unfried, L., Lecheta, M. C., McCabe, E. A., Gantz, J. D., Kawarasaki, Y., Elnitsky, M. A., Hotaling, S., Michel, A. P., Convey, P., Hayward, S. A. L., & Teets, N. M. (2022). Simulated winter warming negatively impacts survival of Antarctica’s only endemic insect. Functional Ecology, 36(8), 1949–1960. https://doi.org/10.1111/1365-2435.14089
  24. Díez, J. L., Cortés, E., Merino, Y., & Santa-Cruz, M. C. (1990). Galactose-induced puffing changes in Chironomus thummi Balbiani rings and their dependence on protein synthesis. Chromosoma, 99(1), 61–70. https://doi.org/10.1007/BF01737290
  25. Durmaz, E., Benson, C., Kapun, M., Schmidt, P., & Flatt, T. (2018). An inversion supergene in Drosophila underpins latitudinal clines in survival traits. Journal of Evolutionary Biology, 31(9), 1354–1364. https://doi.org/10.1111/jeb.13310
  26. Edgington, H., Pavinato, V. A. C., Spacht, D., Gantz, J. D., Convey, P., Lee, R. E., Denlinger, D. L., & Michel, A. (2023). Genetic history, structure and gene flow among populations of Belgica antarctica, the only free-living insect in the western Antarctic Peninsula. Polar Science, 36, 100945. https://doi.org/10.1016/j.polar.2023.100945
  27. Esteve, C., Lagares, C., & Mestres, F. (2020). First detection of chromosomal inversions in a natural population of the invasive pest species Drosophila suzukii. Journal of Genetics, 99(1), 82. https://doi.org/10.1007/s12041-020-01238-2
  28. Faria, R., Johannesson, K., Butlin, R. K., & Westram, A. M. (2019). Evolving inversions. Trends in Ecology and Evolution, 34(3), 239–248. https://doi.org/10.1016/j.tree.2018.12.005
  29. Fraser, C. I., Morrison, A. K., Hogg, A. M., Macaya, E. C., van Sebille, E., Ryan, P. G., Padovan, A., Jack, C., Valdivia, N., & Waters, J. M. (2018). Antarctica’s ecological isolation will be broken by storm-driven dispersal and warming. Nature Climate Change, 8(8), 704–708. https://doi.org/10.1038/s41558-018-0209-7
  30. Gressitt, J. L. (1967). Notes on arthropod populations in the Antarctic Peninsula-South Shetland Islands-South Orkney Islands area. In J. L. Gressitt (Ed.), Entomology of Antarctica, 10. https://doi.org/10.1029/AR010p0373
  31. Harada, E., Lee Jr., R. E., Denlinger, D. L., & Goto, S. G. (2014). Life history traits of adults and embryos of the Antarctic midge Belgica antarctica. Polar Biology, 37(8), 1213–1217. https://doi.org/10.1007/s00300-014-1511-0
  32. Hoffmann, A. A., Sgrò, C. M., & Weeks, A. R. (2004). Chromosomal inversion polymorphisms and adaptation. Trends in Ecology and Evolution, 19(9), 482–488. https://doi.org/10.1016/j.tree.2004.06.013
  33. Hughes, K. A., Pescott, O. L., Peyton, J., Adriaens, T., Cottier-Cook, E. J., Key, G., Rabitsch, W., Tricarico, E., Barnes, D. K. A., Baxter, N., Belchier, M., Blake, D., Convey, P., Dawson, W., Frohlich, D., Gardiner, L. M., González-Moreno, P., James, R., Malumphy, C., ... & Roy, H. E. (2020). Invasive non-native species likely to threaten biodiversity and ecosystems in the Antarctic Peninsula region. Global Change Biology, 26(4), 2702–2716. https://doi.org/10.1111/gcb.14938
  34. Hullé, M., & Vernon, P. (2021). Terrestrial macroarthropods of the sub-Antarctic islands of Possession (Crozet Archipelago) and Kerguelen: Inventory of native and non-native species. Zoosystema, 43(22), 549–561. https://doi.org/10.5252/zoosystema2021v43a22
  35. Hullé, M., Buchard, C., Georges, R., & Vernon, P. (2018). Guide d’identification des Invertébrés de Kerguelen et Crozet (Issue 2ème ed., 181 p.). HAL (Le Centre Pour La Communication Scientifique Directe). https://doi.org/10.15454/1.5375302767618145E12 (In French).
  36. Ivanets, V., Yevchun, H., Miryuta, N., Veselsky, M., Salganskiy, O., Konishchuk, V., Kozeretska, I., Dykyi, E., & Parnikoza, I. (2022). Skua and plant dispersal: Lessons from the Argentine Islands – Kyiv Peninsula region in the maritime Antarctic. Nordic Journal of Botany, 6, e03326. https://doi.org/10.1111/njb.03326
  37. Kapun, M., Fabian, D. K., Goudet, J., & Flatt, T. (2016). Genomic evidence for adaptive inversion clines in Drosophila melanogaster. Molecular Biology and Evolution, 33(5), 1317–1336. https://doi.org/10.1093/molbev/msw016
  38. 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(7), 1813–1827. https://doi.org/10.1111/mec.12594
  39. Kawarasaki, Y., Teets, N. M., Philip, B. N., Potts, L. J., Gantz, J. D., Denlinger, D. L., & Lee, R. E. (2019). Characterization of drought-induced rapid cold-hardening in the Antarctic midge, Belgica antarctica. Polar Biology, 42(6), 1147–1156. https://doi.org/10.1007/s00300-019-02503-6
  40. Kelley, J. L., Peyton, J. T., Fiston-Lavier, A.-S., Teets, N. M., Yee, M.-C., Johnston, J. S., Bustamante, C. D., Lee, R. E., & Denlinger, D. L. (2014). Compact genome of the Antarctic midge is likely an adaptation to an extreme environment. Nature Communications, 5(1), 4611. https://doi.org/10.1038/ncomms5611
  41. Knibb, W. R. (1982). Chromosome inversion polymorphisms in Drosophila melanogaster II. Geographic clines and climatic associations in Australasia, North America and Asia. Genetica, 58(3), 213–221. https://doi.org/10.1007/BF00128015
  42. Kovalenko, P., Trokhymets, V., Parnikoza, I., Protsenko, Yu., Salganskiy, O., Dzhulai, A., Dykyy, I., Nabokin, M., Kozeretska, I., & Gorobchyshyn, V. (2021). Current status of Belgica antarctica Jacobs, 1900 (Diptera: Chironomidae) distribution by the data of Ukrainian Antarctic Expeditions. Ukrainian Antarctic Journal, (2), 76–93. https://doi.org/10.33275/1727-7485.2.2021.679
  43. 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(1), 2–20. https://doi.org/10.1111/1744-7917.12925
  44. Kruskal, W. H., & Wallis, W. A. (1952). Use of ranks in one-criterion variance analysis. Journal of the American Statistical Association, 47(260), 583–621. https://doi.org/10.2307/2280779
  45. Leihy, R. I., Peake, L., Clarke, D. A., Chown, S. L., & McGeoch, M. A. (2023). Introduced and invasive alien species of Antarctica and the Southern Ocean Islands. Scientific Data, 10(1), 200. https://doi.org/10.1038/s41597-023-02113-2
  46. Mann, H. B., & Whitney, D. R. (1947). On a test of whether one of two random variables is stochastically larger than the other. The Annals of Mathematical Statistics, 18(1), 50–60. https://doi.org/10.1214/aoms/1177730491
  47. Martin, J. (1962). Inversion polymorphism in an Antarctic species living in a simple environment. The American Naturalist, 96(890), 317–318. https://doi.org/10.1086/282239
  48. McCarthy, A. H., Peck, L. S., & Aldridge, D. C. (2022). Ship traffic connects Antarctica’s fragile coasts to world-wide ecosystems. Proceedings of the National Academy of Sciences of the United States of America, 119(3), e2110303118. https://doi.org/10.1073/pnas.2110303118
  49. Michailova, P. (1980). Cytotaxonomic features of species of the subfamily Orthocladiinae (Diptera, Chironomidae) from Bulgaria. Genetica, 52(1), 263–266. https://doi.org/10.1007/BF00121835
  50. Michailova, P. V. (1989). The polytene chromosomes and their significance to the systematics and phylogeny of the family Chironomidae, Diptera. Acta Zoologica Fennica, 186, 1–107.
  51. Michailova, P. (2022). External morphology of larva and polytene chromosomes of Clunio marinus Haliday, 1855 (Diptera, Chironomidae, Orthocladiinae) from two localities of the Atlantic coast. Zootaxa, 5141(2), 163–173. https://doi.org/10.11646/zootaxa.5141.2.4
  52. Michailova, P., & Petrova, N. (2015). Bioindicator potential of cytogenetic variability in polytene chromosomes of chironomids (Diptera, Chironomidae) to assess environmental pollution. Cytology and Genetics, 49(4), 262–269. https://doi.org/10.3103/S0095452715040064
  53. Michailova, P., Ilkova, J., Duran, M., Karadurmus, E., Berber, R., & Sen, A. (2012). Structural and functional alterations in salivary gland chromosomes and enzyme activity of Chironomus riparius Mg. (Diptera, Chironomidae) from anthropogenically polluted sites in Bulgaria and Turkey. Caryologia, 65(2), 157–169. https://doi.org/10.1080/00087114.2012.711988
  54. Michailova, P., 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(1), 16–24. https://doi.org/10.5817/CPR2021-1-3
  55. Michailova, P., Ilkova, J., Szarek-Gwiazda, E., Kownacki, A., & Ciszewski, D. (2018). Genome instability in Chironomus annularius sensu Strenzke (Diptera, Chironomidae): A biomarker for assessment of the heavy metal contaminants in Poland. Journal of Limnology, 77(s1), 15–24. https://doi.org/10.4081/jlimnol.2018.1710
  56. Michailova, P., Kovalenko, P. A., Serga, S., Parnikoza, I., Kozeretska, I., & Convey, P. (2023). A chromosome map of Belgica antarctica Jacobs (Diptera: Chironomidae) from Antarctica, including chromosome variability. Antarctic Science, 35(5), 328–344. https://doi.org/10.1017/S0954102023000202
  57. Michailova, P., Petrova, N., Sella, G., Ramella, L., & Bovero, S. (1998). Structural–functional rearrangements in chromosome G in Chironomus riparius (Diptera, Chironomidae) collected from a heavy metal-polluted area near Turin, Italy. Environmental Pollution, 103(1), 127–134. https://doi.org/10.1016/S0269-7491(98)00085-2
  58. Michailova, P., Szarek-Gwiazda, E., & Kownacki, A. (2009). Effect of contaminants on the genome of some species of genus Chironomus (Chironomidae, Diptera) live in sediments of Dunajec River and Czorsztyn Reservoir. Water, Air, and Soil Pollution, 202(1), 245–258. https://doi.org/10.1007/s11270-008-9973-8
  59. Morcillo, G., Barettino, D., Carmona, M. J., Carretero, M. T., & Díez, J. L. (1988). Telomeric DNA sequences differentially activated by heat shock in two Chironomus subspecies. Chromosoma, 96(2), 139–144. https://doi.org/10.1007/BF00331046
  60. Naseeb, S., Carter, Z., Minnis, D., Donaldson, I., Zeef, L., & Delneri, D. (2016). Widespread impact of chromosomal inversions on gene expression uncovers robustness via phenotypic buffering. Molecular Biology and Evolution, 33(7), 1679–1696. https://doi.org/10.1093/molbev/msw045
  61. Parnikoza, I., Rozhok, A., Convey, P., Veselski, M., Esefeld, J., Ochyra, R., Mustafa, O., Braun, C., Peter, H.-U., Smykla, J., Kunakh, V., & Kozeretska, I. (2018). Spread of Antarctic vegetation by the kelp gull: Comparison of two maritime Antarctic regions. Polar Biology, 41(6), 1143–1155. https://doi.org/10.1007/s00300-018-2274-9
  62. Peckham, V. (1971). Notes on the chironomid midge Belgica antarctica Jacobs at Anvers Island in the Maritime Antarctic. Pacific Insects Monograph, 25, 145–166.
  63. Potts, L. J., Gantz, J. D., Kawarasaki, Y., Philip, B. N., Gonthier, D. J., Law, A. D., Moe, L., Unrine, J. M., McCulley, R. L., Lee, R. E., Denlinger, D. L., & Teets, N. M. (2020). Environmental factors influencing fine-scale distribution of Antarctica’s only endemic insect. Oecologia, 194(4), 529–539. https://doi.org/10.1007/s00442-020-04714-9
  64. Prion, S., & Haerling, K. A. (2014). Making sense of methods and measurement: Spearman-rho ranked-order correlation coefficient. Clinical Simulation in Nursing, 10(10), 535–536. https://doi.org/10.1016/j.ecns.2014.07.005
  65. R Core Team. (2024). R: A language and environment for statistical computing [Software]. R Foundation for Statistical Computing. https://www.R-project.org/
  66. Rezende, E. L., Balanyà, J., Rodríguez-Trelles, F., Rego, C., Fragata, I., Matos, M., Serra, L., & Santos, M. (2010). Climate change and chromosomal inversions in Drosophila subobscura. Climate Research, 43(1–2), 103–114. https://doi.org/10.3354/cr00869
  67. Richard, K. J., Convey, P., & Block, W. (1994). The terrestrial arthropod fauna of the Byers Peninsula, Livingston Island, South Shetland Islands. Polar Biology, 14(6), 371–379. https://doi.org/10.1007/BF00240257
  68. Rinehart, J. P., Hayward, S. A. L., Elnitsky, M. A., Sandro, L. H., Lee Jr, R. E., & Denlinger, D. L. (2006). Continuous upregulation 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(38), 14223–14227. https://doi.org/10.1073/pnas.0606840103
  69. Sella, G., Bovero, S., Ginepro, M., Michailova, P., Petrova, N., Robotti, C. A., & Zelano, V. (2004). Inherited and somatic cytogenetic variability in Palearctic populations of Chironomus riparius Meigen 1804 (Diptera, Chironomidae). Genome, 47(2), 332–344. https://doi.org/10.1139/g03-128
  70. Serra-Tosio, B. (1982). Description du male du Belgica albipes (Séguy, 1965), n. comb., rare Chironomide microptere des Iles Crozet (Diptera). Revue Française D’entomologie, 4, 97–100. (In French).
  71. Simões, P., & Pascual, M. (2018). Patterns of geographic variation of thermal adapted candidate genes in Drosophila subobscura sex chromosome arrangements. BMC Evolutionary Biology, 18(1), 60. https://doi.org/10.1186/s12862-018-1178-1
  72. Soares, T. A., Souza-Kasprzyk, J., Padilha, J. A. G., Convey, P., Costa, E. S., & Torres, J. P. M. (2024). Ornithogenic mercury input to soils of Admiralty Bay, King George Island, Antarctica. Polar Biology, 47(9), 891–901. https://doi.org/10.1007/s00300-023-03162-4
  73. Soulivongsa, L., Tengjaroenkul, B., & Neeratanaphan, L. (2020). Effects of contamination by heavy metals and metalloids on chromosomes, serum biochemistry and histopathology of the bonylip barb fish near sepon gold-copper mine, Lao PDR. International Journal of Environmental Research and Public Health, 17(24), 9492. https://doi.org/10.3390/ijerph17249492
  74. Stormo, B. M., & Fox, D. T. (2017). Polyteny: Still a giant player in chromosome research. Chromosome Research, 25(3–4), 201–214. https://doi.org/10.1007/s10577-017-9562-z
  75. Sugg, P., Edwards, J. S., & Baust, J. (1983). Phenology and life history of Belgica antarctica, an Antarctic midge (Diptera: Chironomidae). Ecological Entomology, 8(1), 105–113. https://doi.org/10.1111/j.13652311.1983.tb00487.x
  76. Szarek-Gwiazda, E., Michailova, P., Ilkova, J., Kownacki, A., Ciszewski, D., & Aleksander-Kwaterczak, U. (2013). The effect of long-term contamination by heavy metals on community and genome alterations of Chironomidae (Diptera) in a stream with mine drainage water (southern Poland). Oceanological and Hydrobiological Studies, 42(4), 460–469. https://doi.org/10.2478/s13545-013-0102-y
  77. Teets, N. M., Dalrymple, E. G., Hillis, M. H., Gantz, J. D., Spacht, D. E., Lee, R. E., & Denlinger, D. L. (2020). Changes in energy reserves and gene expression elicited by freezing and supercooling in the Antarctic midge, Belgica antarctica. Insects, 11(1), 18. https://doi.org/10.3390/insects11010018
  78. Turner, J., Barrand, N. E., Bracegirdle, T. J., Convey, P., Hodgson, D. A., Jarvis, M., Jenkins, A., Marshall, G., Meredith, M. P., Roscoe, H., Shanklin, J., French, J., Goosse, H., Guglielmin, M., Gutt, J., Jacobs, S., Kennicutt, M. C. K. II, Masson-Delmotte, V., Mayewski, P., ... & Klepikov, A. (2014). Antarctic climate change and the environment: An update. PolarRecord, 50(3), 237–259. https://doi.org/10.1017/S0032247413000296
  79. Usher, M. B., & Edwards, M. (1984). A dipteran from south of the Antarctic Circle: Belgica antarctica (Chironomidae) with a description of its larva. Biological Journal of the Linnean Society, 23(1), 19–31. https://doi.org/10.1111/j.1095-8312.1984.tb00803.x
  80. Valz, P. D., & Thompson, M. E. (1994). Exact inference for Kendall’s S and Spearman’s ρ with extension to Fisher’s Exact test in r x c contingency tables. Journal of Computational and Graphical Statistics, 3(4), 459–472. https://doi.org/10.2307/1390906
  81. Venables, W. N., & Ripley, B. D. (2002). Generalized linear models. In W. N. Venables, & B. D. Ripley (Eds.), Modern applied statistics with S (pp. 183–210). Springer. https://doi.org/10.1007/978-0-387-21706-2_7
  82. Wellenreuther, M., & Bernatchez, L. (2018). Eco-evolutionary genomics of chromosomal inversions. Trends in Ecology and Evolution, 33(6), 427–440. https://doi.org/10.1016/j.tree.2018.04.002
  83. Werle, S. F., Klekowski, E., & Smith, D. G. (2004). Inversion polymorphism in a Connecticut River Axarus species (Diptera: Chironomidae): biometric effects of a triple inversion heterozygote. Canadian Journal of Zoology, 82(1), 118–129. https://doi.org/10.1139/z03-227
  84. Wirth, W. W., & Gressitt, J. L. (1967). Diptera: Chironomidae (Midges) 1. In J. L. Gressitt (Ed.), Entomology of Antarctica, 10. https://doi.org/10.1029/AR010p0197
  85. Yoshida, M., & Goto, S. G. (2023). Thermal responses of the embryos and early instar larvae of the Antarctic midge Belgica antarctica (Insecta: Diptera). Polar Biology, 46(6), 539–544. https://doi.org/10.1007/s00300-023-03142-8