The Adaptive Value of Chromosomal Inversions and Climatic Change-Studies on the Natural Populations of Drosophila subobscura from the Balkans

Abstract

The adaptive value of the Drosophila subobscura chromosomal inversion polymorphism with regard to environmental effects is well-known. However, the specific details of the inversion adaptations to the global warming scenario deserve to be analyzed. Toward this aim, polymorphism and karyotypes were studied in 574 individuals from Petnica (Serbia) in annual samples taken in June for the period 2019-2022. Comparing the results of Petnica (Cfa: humid subtropical climate) with those from Avala (Serbia: Cfb, temperate oceanic climate) and Font Groga (Barcelona, Spain; Csa: hot-summer Mediterranean climate), significant differences were observed for their chromosomal polymorphism. In Petnica, inversions from U and E chromosomes mainly reacted significantly with regard to temperature, humidity, and rainfall. Moreover, the inversion polymorphism from Petnica (2019-2022) was compared with that from 1995. In this period, a significant increase in mean and maximum temperature was observed. However, to properly explain the observed variations of inversions over time, it was necessary to carefully analyze annual seasonal changes and particular heat wave episodes. Interestingly, yearly fluctuations of U chromosome 'warm'-adapted inversions corresponded with opposite changes in 'non-thermal' inversions. Perhaps these types of inversions were not correctly defined with regard to thermal adaptation, or these fluctuations were also due to adaptations to other physical and/or biological variables. Finally, a joint study of chromosomal inversion polymorphism from many Balkan populations of D. subobscura indicated that different climatic regions presented distinct composition, including thermal-adapted inversions.

Keywords: adaptation; chromosomal thermal index; global warming; natural selection; temperature.

Figure 1

Map with the geographical location of the Serbian and Montenegrin D. subobscura populations used. Belgrade is also presented for geographical reference.

Figure 2

Multivariate analysis of the chromosomal inversion composition of the Petnica, Avala, and Font Groga populations of D. subobscura. (A) Principal coordinate analysis. Two groups are clearly differentiated on the left, corresponding to the Petnica and Avala collections. On the right is the group of samples from Font Groga. (B) GEVA-Ward cluster study. The first partition differentiates the Font Groga collections from those of the Serbian populations (Petnica and Avala). The second partition generates two groups, one with the Petnica samples and the other with those from Avala. The abbreviations used are: in blue, P19 (Petnica 2019), P20 (Petnica 2020), P21 (Petnica 2021), and P22 (Petnica 2022); in red, A14 (Avala 2014), A15 (Avala 2015), A16 (Avala 2016), and A17 (Avala 2017); in dark green, F11 (Font Groga 2011), F12 (Font Groga 2012), F13 (Font Groga 2013), F14 (Font Groga 2014), and F15 (Font Groga 2015).

Figure 2

Multivariate analysis of the chromosomal inversion composition of the Petnica, Avala, and Font Groga populations of D. subobscura. (A) Principal coordinate analysis. Two groups are clearly differentiated on the left, corresponding to the Petnica and Avala collections. On the right is the group of samples from Font Groga. (B) GEVA-Ward cluster study. The first partition differentiates the Font Groga collections from those of the Serbian populations (Petnica and Avala). The second partition generates two groups, one with the Petnica samples and the other with those from Avala. The abbreviations used are: in blue, P19 (Petnica 2019), P20 (Petnica 2020), P21 (Petnica 2021), and P22 (Petnica 2022); in red, A14 (Avala 2014), A15 (Avala 2015), A16 (Avala 2016), and A17 (Avala 2017); in dark green, F11 (Font Groga 2011), F12 (Font Groga 2012), F13 (Font Groga 2013), F14 (Font Groga 2014), and F15 (Font Groga 2015).

Figure 3

Cluster analysis of O chromosome inversion polymorphism from the Balkan populations. The Mt. Parnes (Grece) and Font Groga (Barcelona, Spain) populations were used as reference outgroups. The colors indicate the climate: dark green (Csa), blue (Cfb), red (Cfa), and orange (Csb). The numbers stand for the used populations: 1. Mt. Parnes May 2006; 2. Apatin June 1994; 3. Apatin June 2008; 4. Apatin June 2009; 5. Apatin June 2018; 6. Avala Sept. 2003; 7. Avala June 2004; 8. Avala Sept. 2004; 9. Avala Sept. 2005; 10. Avala June 2011; 11. Avala June 2014; 12. Avala June 2015; 13. Avala June 2016; 14. Avala June 2017; 15. Djerdap June 2001; 16. Djerdap Aug. 2001; 17. Djerdap June 2002; 18. Jastrebac June 1990; 19. Jastrebac June 1993; 20. Jastrebac June 1994; 21. Kamariste June 1996; 22. Petnica May 1995; 23. Petnica June 1995; 24. Petnica Aug. 1995; 25. Petnica May 2010; 26. Petnica June 2019; 27. Petnica June 2020; 28. Petnica June 2021; 29. Petnica June 2022; 30. Fruska Gora 1971? (year not specified in the paper); 31. Zanjic June 1997; 32. Font Groga Oct.–Nov. 2011; 33. Font Groga Oct.–Nov. 2012; 34. Font Groga Oct.–Nov. 2013; 35. Font Groga Oct.–Nov. 2014; 36. Font Groga Oct.–Nov. 2015. References for these populations are presented in the text.

Figure 4

Changes in frequency (percentage) over the years (1995, 2019, 2020, 2021, and 2022) for the Petnica chromosomal inversions classified according to thermal adaptation. (a) ‘Cold’-adapted. (b) ‘Warm’-adapted. (c) ‘Non-thermal’. The filled circles stand for: blue for the A chromosome, red for the J chromosome, black for the U chromosome, green for the E chromosome, and orange for the O chromosome.