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Adaptation of Drosophila subobscura chromosomal inversions to climatic variables: the Balkan natural population of Avala

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Abstract

The adaptive value of chromosomal inversions continues raising relevant questions in evolutionary biology. In many species of the Drosophila genus, different inversions have been recognized to be related to thermal adaptation, but it is necessary to determine to which specific climatic variables the inversions are adaptive. With this aim, the behavior of thermal adapted inversions of Drosophila subobscura regarding climatic variables was studied in the natural population of Avala (Serbia) during the 2014–2017 period. The results obtained were compared with those previously reported in the Font Groga (Barcelona, Spain) population, which presents different climatic and environmental conditions. In both populations, it was observed that most thermal adapted inversions were significantly associated with the first, second or both principal components, which were related with maximum, minimum and mean temperatures. Moreover, a significant increase over years (2004–2017) for the minimum temperature was detected. In parallel, a significant variation over time in Avala was only observed for the frequencies of ‘warm’ and ‘non-thermal’ adapted inversions of the U chromosome. However, stability in the chromosomal inversion polymorphism was observed for the 2014–2017 period which might result from the temporal span of the study and/or selective process acting on the population.

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References

  • Ananina G, Peixoto AA, Bitner-Mathé BC, Souza WN, da Silva LB, Valente VLS, Klaczko LB (2004) Chromosomal inversion polymorphism in Drosophila mediopunctata: seasonal, altitudinal, and latitudinal variation. Genet Mol Biol 27:61–69

    Article  Google Scholar 

  • Araúz PA, Mestres F, Pegueroles C, Arenas C, Tzannidakis G, Krimbas CB, Serra L (2009) Tracking the origin of the American colonization by Drosophila subobscura: comparison between Eastern and Western Mediterranean populations. J Zool Syst Evol Res 47:25–34

    Article  Google Scholar 

  • Arenas C, Zivanovic G, Mestres F (2018) Chromosomal Thermal Index: a comprehensive way to integrate the thermal adaptation of Drosophila subobscura whole karyotype. Genome 61:73–78

    Article  PubMed  Google Scholar 

  • Argemí M, Monclús M, Mestres F, Serra L (1999) Comparative analysis of a community of Drosophilids (Drosophilidae; Diptera) sampled in two periods widely separated in time. J Zool Syst Evol Res 37:203–210

    Article  Google Scholar 

  • Argemí M, Mestres F, Prevosti A, Serra L (2003) Microevolutionary dynamics of a community of Drosophilids. J Zool Syst Evol Res 41:57–63

    Article  Google Scholar 

  • Ayala FJ, Coluzzi M (2005) Chromosome speciation: humans, Drosophila, and mosquitoes. Proc Natl Acad Sci USA 102:6535–6542

    Article  CAS  PubMed  Google Scholar 

  • Ayala FJ, Serra L, Prevosti A (1989) A grand experiment in evolution: the Drosophila subobscura colonization of the Americas. Genome 31:246–255

    Article  Google Scholar 

  • Ayala D, Ullastres A, González J (2014) Adaptation through chromosomal inversions in Anopheles. Front Genet 5:129

    Article  PubMed  Google Scholar 

  • Balanyà J, Serra L, Gilchrist GW, Huey RB, Pascual M, Mestres F, Solé A (2003) Evolutionary pace of chromosomal polymorphism in colonizing populations of Drosophila subobscura: an evolutionary time series. Evolution 57:1837–1845

    PubMed  Google Scholar 

  • Balanyà J, Solé E, Oller JM, Sperlich D, Serra L (2004) Long-term changes in the chromosomal inversion polymorphism of Drosophila subobscura. II. European populations. J Zool Syst Evol Res 42:191–201

    Article  Google Scholar 

  • Balanyà J, Oller JM, Huey RB, Gilchrist GW, Serra L (2006) Global genetic change tracks global climate warming in Drosophila subobscura. Science 313:1773–1775

    Article  PubMed  Google Scholar 

  • Balanyà J, Huey RB, Gilchrist GW, Serra L (2009) The chromosomal polymorphism of Drosophila subobscura: a microevolutionary weapon to monitor global change. Heredity 103:364–367

    Article  PubMed  Google Scholar 

  • Barriopedro D, Fischer EM, Luterbacher J, Trigo RM, García-Herrera R (2011) The hot summer of 2010: redrawing the temperature record map of Europe. Science 332:220–224

    Article  CAS  PubMed  Google Scholar 

  • Begon M (1976) Dispersal, density and microdistribution in Drosophila subobscura Collin. J Anim Ecol 45:441–456

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300

    Google Scholar 

  • Berg PR, Star B, Pampoulie C, Bradbury IR, Bentzen P, Hutchings JA, Jentoft S, Jakobsen KS (2017) Trans-oceanic genomic divergence of Atlantic cod ecotypes is associated with large inversions. Heredity 119:418–428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhattacharyya A (1946) On a measure of divergence between two multinomial populations. Sankhya 7:401–406

    Google Scholar 

  • Borda MA, Sambucetti PD, Gomez FH, Norry FM (2018) Genetic variation for egg-to-adult survival in Drosophila melanogaster in a set of recombinant inbred lines reared under heat stress in a natural thermal environment. Entomol Exp Appl 166:863–872

    Article  CAS  Google Scholar 

  • Carson HL (1955) The genetic characteristics of marginal populations of Drosophila. Cold Spring Harb Symp Quant Biol 20:276–287

    Article  CAS  PubMed  Google Scholar 

  • Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, Markov TA et al (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450:203–218

    Article  PubMed  Google Scholar 

  • Dolgova O, Rego C, Calabria G, Balanyà J, Pascual M, Rezende EL, Santos M (2010) Genetic constraints for thermal coadaptation in Drosophila subobscura. BMC Evol Biol 10:363

    Article  PubMed  PubMed Central  Google Scholar 

  • Durmaz E, Benson C, Kapun M, Schmidt P, Flatt T (2018) An inversion supergene in Drosophila underpins latitudinal clines in survival traits. J Evol Biol 31:1354–1364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Etges WJ, Levitan M (2008) Variable evolutionary response to regional climate change in a polymorphic species. Biol J Linn Soc 95:702–718

    Article  Google Scholar 

  • Fabian DK, Kapun M, Nolte V, Kofler R, Schmidt PS, Schlötterer C et al (2012) Genome-wide patterns of latitudinal differentiation among populations of Drosophila melanogaster from North America. Mol Ecol 21:4748–4769

    Article  PubMed  PubMed Central  Google Scholar 

  • Feuk L, MacDonald JR, Tang T, Carson AR, Li M, Rao G, Khaja R, Sherer SW (2005) Discovery of human inversion polymorphisms by comparative analysis of human and chimpanzee DNA sequence assemblies. PLoS Genet 1:e56

    Article  PubMed  Google Scholar 

  • Founda D, Giannakopoulos C (2009) The exceptionally hot summer of 2007 in Athens, Greece—a typical summer in the future climate? Glob Planet Change 67:227–236

    Article  Google Scholar 

  • Fuller ZL, Leonard CJ, Young RE, Schaeffer SW, Phadnis N (2018) Ancestral polymorphisms explain the role of chromosomal inversions in speciation. PLoS Genet 14:e1007526

    Article  PubMed  Google Scholar 

  • Galludo M, Canals J, Pineda-Cirera L, Esteve C, Rosselló M, Balanyà J, Arenas C, Mestres F (2018) Climatic adaptation of chromosomal inversions in Drosophila subobscura. Genetica 146:433–441

    Article  CAS  PubMed  Google Scholar 

  • Galludo M, Canals J, Pineda-Cirera L, Esteve C, Rosselló M, Madrenas R, Balanyà J, Arenas C, Mestres F (2020) Annual climatic effects on the autumnal drosophild fauna composition at the font Groga site (Tibidado, Barcelona). North-West J Zool 16:15–20

    Google Scholar 

  • Guillén Y, Ruiz A (2012) Gene alterations at Drosophila inversion breakpoints provide prima facie evidence for natural selection as an explanation for rapid chromosomal evolution. BMC Genomics 13:53

    Article  PubMed  Google Scholar 

  • Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann AA, Rieseberg LH (2008) Revisiting the impact of inversions in evolution: from population genetic markers to drivers of adaptive shifts and speciation? Annu Rev Ecol Evol Syst 39:21–42

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoffmann AA, Sgrò CM, Weeks AR (2004) Chromosomal inversion polymorphism and adaptation. Trends Ecol Evol 19:482–488

    Article  PubMed  Google Scholar 

  • Irigoien I, Arenas C, Fernández E, Mestres F (2010) GEVA: geometric variability-based approaches for identifying patterns in data. Comput Stat 25:241–255

    Article  Google Scholar 

  • Kapun M, Flatt T (2019) The adaptive significance of chromosomal inversion polymorphisms in Drosophila melanogaster. Mol Ecol 28:1263–1282

    Article  PubMed  Google Scholar 

  • Karageorgiou C, Gámez-Visairas V, Tarrío R, Rodríguez-Trelles F (2019) Long-read based assembly and synteny analysis of a reference Drosophila subobscura genome reveals signatures of structural evolution driven by inversions recombination-suppression effects. BMC Genomics 20:223

    Article  PubMed  Google Scholar 

  • Karageorgiou C, Tarrío R, Rodríguez-Trelles F (2020) The cyclically seasonal Drosophila subobscura inversion O7 originated from fragile genomic sites and relocated immunity and metabolic genes. Front Genet 11:565836

    Article  CAS  PubMed  Google Scholar 

  • Kirkpatrick M (2010) How and why chromosome inversions evolve. PLoS Biol 8:e1000501

    Article  PubMed  Google Scholar 

  • Krimbas CB (1992) The inversion polymorphism of Drosophila subobscura. In: Krimbas CB, Powell JR (eds) Drosophila inversion polymorphism. CRC Press Inc., Boca Raton, FL, pp 127–220

    Google Scholar 

  • Krimbas CB (1993) Drosophila subobscura: biology, genetics and inversion polymorphism. Verlag Dr. Kovac, Hamburg

    Google Scholar 

  • Krimbas CB, Loukas M (1980) The inversion polymorphism of Drosophila subobscura. Evol Biol 12:163–234

    Article  Google Scholar 

  • Kunze-Mühl E, Sperlich D (1955) Inversionen und chromosomale Strukturtypen bei Drosophila subobscura. Z Indukt Abstamm Vererb Lehre 87:65–84

    Google Scholar 

  • Kunze-Mühl E, Müller E (1958) Weitere Untersuchungen über die chromosomale Struktur und die natürlichen Strukturtypen von Drosophila subobscura. Chromosoma 9:559–570

    Article  PubMed  Google Scholar 

  • Laayouni H, Hasson E, Santos M, Fontdevila A (2003) The evolutionary history of Drosophila buzzatii. XXXV. Inversion polymorphism and nucleotide variability in different regions of the second chromosome. Mol Biol Evol 20:931–944

    Article  CAS  PubMed  Google Scholar 

  • Laayouni H, García-Franco F, Chávez-Sandoval BE, Trotta V, Beltran S, Corominas M et al (2007) Thermal evolution of gene expression profiles in Drosophila subobscura. BMC Evol Biol 7:42

    Article  PubMed  PubMed Central  Google Scholar 

  • Lewontin RC, Moore JA, Provine WB, Wallace B (1981) Dobzhanky’s genetics of natural populations I–XLIII. Columbia University Press, New York

    Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates Inc., Sunderland, MA

    Google Scholar 

  • Madrenas R, Balanyà J, Arenas C, Khadem M, Mestres F (2020) Global warming and chromosomal inversion adaptation in isolated islands: Drosophila subobscura populations from Madeira. Entomol Sci 23:74–85

    Article  Google Scholar 

  • McAllister BF, Sheeley SL, Mena PA, Evans AL, Schlötterer C (2008) Clinal distribution of a chromosomal rearrangement: a precursor to chromosomal speciation? Evolution 62:1852–1865

    Article  PubMed  Google Scholar 

  • Menozzi P, Krimbas CB (1992) The inversion polymorphism of D. subobscura revisited: synthetic maps of gene arrangement frequencies and their interpretation. J Evol Biol 5:625–641

    Article  Google Scholar 

  • Mestres F, Sanz J, Serra L (1998) Chromosomal structure and recombination between inversions in Drosophila subobscura. Hereditas 128:105–113

    Article  CAS  PubMed  Google Scholar 

  • Mestres F, Balanyà J, Arenas C, Solé E, Serra L (2001) Colonization of America by Drosophila subobscura: heterotic effect of chromosomal arrangements revealed by the persistence of lethal genes. Proc Natl Acad Sci USA 98:9167–9170

    Article  PubMed  Google Scholar 

  • Mestres F, Balanyà J, Pascual M, Arenas C, Gilchrist GW, Huey RB, Serra L (2009) Evolution of Chilean colonizing populations of Drosophila subobscura: lethal genes and chromosomal arrangements. Genetica 136:37–48

    Article  CAS  PubMed  Google Scholar 

  • Morgan TJ, Mackay TFC (2006) Quantitative trait loci for thermotolerance phenotypes in Drosophila melanogaster. Heredity 96:232–242

    Article  CAS  PubMed  Google Scholar 

  • Nie W, Wang J, Su W, Wang D, Tanomtong A, Perelman PL, Graphodatsky AS, Yang F (2012) Chromosomal rearrangements and karyotype evolution in carnivores revealed by chromosome painting. Heredity 108:17–27

    Article  CAS  PubMed  Google Scholar 

  • Norry FM, Scannapieco AC, Sambucetti P, Bertoli CI, Loeschcke V (2008) QTL for the thermotolerance effect of heat hardening, knockdown resistance to heat and chill-coma recovery in an intercontinental set of recombinant inbred lines of Drosophila melanogaster. Mol Ecol 17:4570–4581

    Article  CAS  PubMed  Google Scholar 

  • Orengo DJ, Prevosti A (1996) Temporal changes in chromosomal polymorphism of Drosophila subobscura related to climatic changes. Evolution 50:1346–1350

    Article  PubMed  Google Scholar 

  • Orengo DJ, Puerma E, Aguadé M (2016) Monitoring chromosomal polymorphism in Drosophila subobscura over 40 years. Entomol Sci 19:215–221

    Article  Google Scholar 

  • Orengo DJ, Puerma E, Papaceit M, Segarra C, Aguadé M (2017) Dense gene physical maps of the non-model species Drosophila subobscura. Chromosome Res 25:145–154

    Article  CAS  PubMed  Google Scholar 

  • Pegueroles C, Araúz PA, Pascual M, Mestres F (2010) A recombination survey using microsatellites: the O chromosome of Drosophila subobscura. Genetica 138:795–804

    Article  PubMed  Google Scholar 

  • Pegueroles C, Aquadro CF, Mestres F, Pascual M (2013) Gene flow and gene flux shape evolutionary patterns of variation in Drosophila subobscura. Heredity 110:520–529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pegueroles C, Ferrés-Coy A, Martí-Solano M, Aquadro CF, Pascual M, Mestres F (2016) Inversions and adaptation to the plant toxin ouabain shape DNA sequence variation within and between chromosomal inversions of Drosophila subobscura. Sci Rep 6:23754

    Article  CAS  PubMed  Google Scholar 

  • Pennisi E (2017) ‘Supergenes’ drive evolution. Science 357:1083

    Article  CAS  PubMed  Google Scholar 

  • Prevosti A, Ribo G, Serra L, Aguade M, Balaña J, Monclus M, Mestres F (1988) Colonization of America by Drosophila subobscura: experiment in natural populations that supports the adaptive role of chromosomal-inversion polymorphism. Proc Natl Acad Sci USA 85:5597–5600

    Article  CAS  PubMed  Google Scholar 

  • Prevosti A, Serra L, Aguadé M, Ribó G, Mestres F, Balanya J, Monclús M (1989) Colonization and establishment of the Palearctic species Drosophila subobscura in North and South America. In: Fontdevila A (ed) Evolutionary biology of transient unstable populations. Springer-Verlag, Berlin, pp 114–129

    Chapter  Google Scholar 

  • Provan J, Bennett KD (2008) Phylogeographic insights into cryptic glacial refugia. Trends Ecol Evol 23:564–571

    Article  PubMed  Google Scholar 

  • R Development Core Team (2014) R: a language and environment for statistical computing, R Foundation for Statistical Computing. Vienna, Austria

  • Rego C, Balanyà J, Fragata I, Matos M, Rezende EL, Santos M (2010) Clinal patterns of chromosomal inversion polymorphisms in Drosophila subobscura are partly associated with thermal preferences and heat stress resistance. Evolution 64:385–397

    Article  PubMed  Google Scholar 

  • Reis M, Vieira CP, Lata R, Posnien N, Vieira J (2018) Origin and consequences of chromosomal inversions in the virilis group of Drosophila. Genome Biol Evol 10:3152–3166

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Trelles F, Alvarez G, Zapata C (1996) Time-series analysis of seasonal changes of the O inversion polymorphism of Drosophila subobscura. Genetics 142:179–187

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodriguez-Trelles F, Rodriguez MA (1998) Rapid micro-evolution and loss of chromosomal diversity in Drosophila in response to climate warming. Evol Ecol 12:829–838

    Article  Google Scholar 

  • Rodríguez-Trelles F, Tarrío R, Santos M (2013) Genome-wide evolutionary response to a heat wave in Drosophila. Biol Lett 9:20130228

    Article  PubMed  Google Scholar 

  • Schaeffer SW, Anderson WW (2005) Mechanisms of genetic exchange within the chromosomal inversions of Drosophila pseudoobscura. Genetics 171:1729–1739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schaeffer SW, Goetting-Minesky MP, Kovacevic M, Peoples JR, Graybill JL, Miller JM et al (2003) Evolutionary genomics of inversions in Drosophila pseudoobscura: evidence for epistasis. Proc Natl Acad Sci USA 100:8319–8324

    Article  CAS  PubMed  Google Scholar 

  • Schar C, Jendritzky G (2004) Hot news from summer 2003. Nature 432:559–560

    Article  PubMed  Google Scholar 

  • Serra L, Pegueroles G, Mestres F (1987) Capacity of dispersal of a colonizing species: Drosophila subobscura. Genetica 73:223–235

    Article  Google Scholar 

  • Sgrò CM, Hoffmann AA (2004) Genetic correlations, tradeoffs and environmental variation. Heredity 93:241–248

    Article  PubMed  Google Scholar 

  • Smukowski Heil CS, Ellison C, Dubin M, Noor MAF (2015) Recombining without hotspots: a comprehensive evolutionary portrait of recombination in two closely related species of Drosophila. Genome Biol Evol 7:2829–2842

    Article  PubMed  Google Scholar 

  • Solé E, Balanyà J, Sperlich D, Serra L (2002) Long-term changes in the chromosomal inversion polymorphism of Drosophila subobscura. I. Mediterranean populations from Southwestern Europe. Evolution 56:830–835

    PubMed  Google Scholar 

  • Sperlich D, Feuerbach H (1969) Austausch-Ungleichgewicht zwischen unabhängigen Inversionen in naturlichen populationen von Drosophila subobscura. Theor Appl Genet 39:104–112

    Article  CAS  PubMed  Google Scholar 

  • Sperlich D, Feuerbach-Mravlag H (1974) Epistatic gene interaction, crossing over, and linked and unlinked inversions in Drosophila subobscura. Evolution 28:67–75

    Article  PubMed  Google Scholar 

  • Sperlich D, Pfriem P (1986) Chromosomal polymorphism in natural and experimental populations. In: Ashburner M, Carson HL, Thompson JN Jr (eds) The genetics and biology of Drosophila, vol 3e. Academic Press, London, pp 257–309

    Google Scholar 

  • Stefanon M, D’Andrea F, Drobinski P (2012) Heatwave classification over Europe and the Mediterranean region. Environ Res Lett 7:014023

    Article  Google Scholar 

  • Stevison LS, Hoehn KB, Noor MAF (2011) Effects of inversions on within-and between species recombination and divergence. Genome Biol Evol 3:830–841

    Article  CAS  PubMed  Google Scholar 

  • Sturtevant AH (1921) A case of rearrangement of genes in Drosophila. Proc Natl Acad Sci USA 7:235–237

    Article  CAS  PubMed  Google Scholar 

  • Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464

    Article  CAS  PubMed  Google Scholar 

  • Takahashi A, Takano-Shimizu T (2011) Divergent enhancer haplotype of ebony on inversion In(3R)Payne associated with pigmentation variation in a tropical population of Drosophila melanogaster. Mol Ecol 20:4277–4287

    Article  CAS  PubMed  Google Scholar 

  • Times The (1972) The Times atlas of the world, 4th edn. Times Newspapers, London, pp XXVI–XXVII

    Google Scholar 

  • Tzedakis PC (2004) The Balkans as prime glacial refugial territory of European temperate trees. In: Griffiths HI, Kryštufek B, Reed JM (eds) Balkan biodiversity. Springer, Dordrecht, pp 49–68

    Chapter  Google Scholar 

  • van Heerwaarden B, Lee RFH, Wegener B, Weeks AR, Sgró CM (2012) Complex patterns of local adaptation in heat tolerance in Drosophila simulans from eastern Australia. J Evol Biol 25:1765–1778

    Article  PubMed  Google Scholar 

  • Wielstra B, Arntzen JW (2020) Extensive cytonuclear discordance in a crested newt from the Balkan Peninsula glacial refugium. Biol J Linn Soc 130:578–585

    Article  Google Scholar 

  • Zivanovic G, Mestres F (2010) Viabilities of Drosophila subobscura homo- and heterokaryotypes at optimal and stress temperatures. I. Analysis over several years. Hereditas 147:70–81

    Article  PubMed  Google Scholar 

  • Zivanovic G, Mestres F (2011) Changes in chromosomal polymorphism and global warming: the case of Drosophila subobscura from Apatin (Serbia). Genet Mol Biol 34:489–495

    Article  PubMed  Google Scholar 

  • Zivanovic G, Arenas C, Mestres F (2012) Short- and long-term changes in chromosomal inversion polymorphism and global warming: Drosophila subobscura from the Balkans. Isr J Ecol Evol 58:289–311

    Google Scholar 

  • Zivanovic G, Arenas C, Mestres F (2014a) Inbreeding and thermal adaptation in Drosophila subobscura. Genome 57:481–488

    Article  PubMed  Google Scholar 

  • Zivanovic G, Arenas C, Mestres F (2014b) Inversion polymorphism in two Serbian natural populations of Drosophila subobscura: analysis of long-term changes. Russ J Genet 50:638–644

    Article  CAS  Google Scholar 

  • Zivanovic G, Arenas C, Mestres F (2015) Medium-term changes in Drosophila subobscura chromosomal inversion polymorphism: a possible relation with global warming? J Genet 94:343–346

    Article  PubMed  Google Scholar 

  • Zivanovic G, Arenas C, Mestres F (2016) Individual inversions or their combinations: which is the main selective target in a natural population of Drosophila subobscura? J Evol Biol 29:657–664

    Article  CAS  PubMed  Google Scholar 

  • Zivanovic G, Arenas C, Mestres F (2019) Rate of change for the thermal adapted inversions in Drosophila subobscura. Genetica 147:401–409

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We dedicate this research to the memory of Prof. George W. Gilchrist (1954–2020), an excellent evolutionary scientist and friend. This study was financially supported by grants from the Ministry of Education, Science and Technological Development of the Republic of Serbia (Grant Number 451-03-9/2021-14/200007), the Ministerio de Economía y Competitividad, Spain (CTM2017-88080 AEI/FEDER, UE) and the Generalitat de Catalunya, Spain (2017SGR 1120 and 2017SGR 622). The authors declare that they have no conflict of interest.

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Zivanovic, G., Arenas, C. & Mestres, F. Adaptation of Drosophila subobscura chromosomal inversions to climatic variables: the Balkan natural population of Avala. Genetica 149, 155–169 (2021). https://doi.org/10.1007/s10709-021-00125-7

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