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Rate of change for the thermal adapted inversions in Drosophila subobscura

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Abstract

The changes of chromosomal inversion polymorphism composition of Drosophila subobscura in samples from Apatin (Serbia) were studied in a 24-years interval (1994–2018). The variation was significant for all autosomes and directional, increasing the inversions considered as ‘warm’, whereas those reported as ‘cold’ decreased. Furthermore, the Chromosomal Thermal Index (CTI), which allows studying the thermal adaptation of the whole karyotype increased significantly in that period of time. These results were in agreement with the indicators of global warming in Apatin: a trend to increase of the mean, maximum and minimum (this latter even significant) temperatures, and an erratic pattern of rainfall (also usual in global warming). The deviations from the Wright–Fisher model of genetic drift were used to consider the possible effect of migration or selection as evolutionary factors responsible for the change in inversion frequencies. To quantify approximately the rate of change in the frequencies, for each kind of inversions (‘cold’, ‘warm’ and ‘non-thermal adapted’), the difference in frequency between the Apatin samples obtained in 1994 and 2018 was computed and then it was divided by the number of years elapsed. This rate was always higher (from twice as many as thirty times more depending on the autosome) for thermal adapted inversions (‘cold’ or ‘warm’) than the ‘non-thermal’ adapted. From this study, it could be concluded that the chromosomal inversions of D. subobscura could change (in composition and frequencies) in a predictable direction and a rather ‘rapid’ rhythm to adapt to the global warming scenario.

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References

  • Alexandri P, Triantafyllidis A, Papakostas S, Chatzinikos E, Platis P, Papageorgiou N et al (2012) The Balkans and the colonization of Europe: the post-glacial range expansion of the wild boar, Sus scrofa. J Biogeogr 39:713–723

    Article  Google Scholar 

  • Araúz P, Mestres F, Pegueroles C, Arenas C, Tzannidakis G, Krimbas CB, Serra L (2009) Tracking the origin of the American colonization by Drosophila subobscura: genetic 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 

  • 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  CAS  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 

  • Begon M (1976) Temporal variations in the reproductive condition of Drosophila obscura Fallén and D. subobscura Collin. Oecologia 23:31–47

    Article  PubMed  Google Scholar 

  • Begon M (1977) The effective size of a natural Drosophila subobscura population. Heredity 38:13–18

    Article  CAS  PubMed  Google Scholar 

  • Begon M, Krimbas CB, Loukas M (1980) The genetics of Drosophila subobscura populations. XV. Effective size of a natural population estimated by three independent methods. Heredity 45:335–350

    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 

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

    Article  CAS  PubMed  Google Scholar 

  • Cook J, Oreskes N, Doran PT et al. (2016) Consensus on consensus: a synthesis of consensus estimates on human-caused global warming. Environ Res Lett 11: Article ID 048002

  • Crow JF, Kimura M (1970) An introduction to population genetics theory. Harper & Row Publishers, New York

    Google Scholar 

  • Dobzhansky Th (1970) Genetics of the evolutionary process. Columbia University Press, New York

    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 

  • Gilchrist GW, Huey RB, Serra L (2001) Rapid evolution of wing size cline in Drosophila subobscura. Genetica 112–113:273–286

    Article  PubMed  Google Scholar 

  • Gingerich PD (1983) Rates of evolution: effects of time and temporal scaling. Science 222:159–161

    Article  CAS  PubMed  Google Scholar 

  • Haldane JBS (1949) Suggestions as to quantitative measurement of rates of evolution. Evolution 3:51–56

    Article  CAS  PubMed  Google Scholar 

  • Heckel G, Burri R, Fink S, Desmet JF, Excoffier L (2005) Genetic structure and colonization processes in European populations of the common vole, M. arvalis. Evolution 59:2231–2242

    Article  CAS  PubMed  Google Scholar 

  • Hendry AP, Kinnison MT (1999) Perspective: the pace of modern life: measuring rates of contemporary microevolution. Evolution 53:1637–1653

    Article  PubMed  Google Scholar 

  • Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Huey RB, Gilchrist GW, Carlson ML, Berrigan D, Serra L (2000) Rapid evolution of a geographic cline in size in an introduced fly. Science 287:308–309

    Article  CAS  PubMed  Google Scholar 

  • IPCC (2014) Climate Change 2014. Synthesis Report. In: Core Writing Team, Pachauri RK, Meyer LA (eds) Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change IPCC, Geneva, Switzerland

  • Kindler C, Graciá E, Fritz U (2018) Extra-Mediterranean glacial refuges in barred and common grass snakes (Natrix helvetica, N. natrix). Sci Rep 8:1821

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Krimbas CB (1992) The inversion polymorphism of Drosophila subobscura. In: Krimbas CB, Powell JR (eds) Drosophila inversion polymorphism. CRC Press, 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, Müller E (1958) Weitere Untersuchungen uber die chromosomale Struktur und die naturlichen Strukturtypen von Drosophila subobscura. Chromosoma 9:559–570

    Article  PubMed  Google Scholar 

  • Kurbalija-Novicic Z, Jelic M, Savic T, Savic-Veselinovic M, Dimitrijevic D, Jovanovic M et al (2013) Effective population size in Drosophila subobscura: ecological and molecular approaches. J Biol Res 19:65–74

    Google Scholar 

  • Latorre A, Hernandez C, Martinez D, Castro JA, Ramón M, Moya A (1992) Population structure and mitochondrial DNA gene flow in Old World populations of Drosophila subobscura. Heredity 68:15–24

    Article  CAS  PubMed  Google Scholar 

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

    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, Serra L (1991) Lethal allelism in Drosophila subobscura: difficulties in the estimation of certain population parameters. J Zool Syst Evolut-forsch 29:264–279

    Article  Google Scholar 

  • Mestres F, Pegueroles G, Prevosti A, Serra L (1990) Colonization of America by D. subobscura: lethal genes and the problem of the O5 inversion. Evolution 44:1823–1836

    CAS  PubMed  Google Scholar 

  • Mestres F, Balanyà J, Segarra C, Prevosti A, Serra L (1992) Colonization of America by D. subobscura: analysis of the O5 inversions from Europe and America and their implications for the colonizing process. Evolution 46:1564–1568

    CAS  PubMed  Google Scholar 

  • Mestres F, Serra L, Ayala FJ (1995) Colonization of the Americas by D. subobscura: lethal-gene allelism and association with chromosomal arrangements. Genetics 140:1297–1305

    CAS  PubMed  PubMed Central  Google Scholar 

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

    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 

  • Pascual M, Aquadro CF, Soto V, Serra L (2001) Microsatellite variation in colonizing and Palearctic populations of Drosophila subobscura. Mol Biol Evol 18:731–740

    Article  CAS  PubMed  Google Scholar 

  • Pegueroles G, Papaceit M, Quintana A, Guillén A, Prevosti A, Serra L (1995) An experimental study of evolution in progress: clines for quantitative traits in colonizing and Palearctic populations of Drosophila. Evol Ecol 9:453–465

    Article  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 

  • Powell JR (1992) Inversion polymorphism in Drosophila pseudoobscura and Drosophila persimilis. In: Krimbas CB, Powell JR (eds) Drosophila inversion polymorphism. CRC Press, Boca Raton (FL), USA, pp 73–126

    Google Scholar 

  • Powell JR (1997) Progress and prospects in evolutionary biology. The Drosophila model. Oxford University Press, New York

    Google Scholar 

  • Prevosti A, Serra L, Ribó G, Aguadé M, Sagarra E, Monclús M, García MP (1985) The colonization of Drosophila subobscura in Chile. II. Clines in the chromosomal arrangements. Evolution 39:838–844

    Article  PubMed  Google Scholar 

  • Prevosti A, Ribó G, Serra L, Aguadé M, Balañá J, Monclús 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, Balañá 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, Berlin, pp 114–129

    Chapter  Google Scholar 

  • 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 

  • Rezende EL, Balanyà J, Rodríguez-Trelles F, Rego C, Fragata I, Matos M et al (2010) Climate change and chromosomal inversions in Drosophila subobscura. Clim Res 43:103–114

    Article  Google Scholar 

  • Ripple WJ, Wolf C, Newsome TM et al (2017) World scientists’ warning to humanity: a second notice. Bioscience 67:1026–1028

    Article  Google Scholar 

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

    Article  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

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zivanovic G, Mestres F (2010) Viabilities of Drosophila subobscura homo- and heterokaryo-types 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  PubMed Central  Google Scholar 

  • Zivanovic G, Andjelkovic M, Marinkovic D (2002) Chromosomal inversion polymorphism of Drosophila subobscura from south-eastern part of Europe. J Zool Syst Evol Res 40:201–204

    Article  Google Scholar 

  • Zivanovic G, Arenas C, Mestres F (2007) The genetic structure of Balkan populations of Drosophila subobscura. Hereditas 144:120–128

    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 

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Acknowledgements

We want to dedicate this research to Prof. A. Prevosti on the occasion of the centenary of his birth (1919–2019). We especially thank the comments and suggestions of the anonymous reviewers who clearly improved the earlier version of the manuscript. This research was financially supported by grants from the Ministry of Education, Science and Technological Development of the Republic of Serbia (Grant Number 173025), the Ministerio de Economía y Competitividad, Spain (CTM2017-88080 AEI/FEDER, UE) and the Generalitat de Catalunya, Spain (2017SGR 1120 and 2017SGR 622).

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  1. Department of Genetics, Institute for Biological Research “Sinisa Stankovic”, University of Belgrade, Belgrade, Serbia

    Goran Zivanovic

  2. Departament de Genètica, Microbiologia i Estadística, Secció Estadística, Universitat de Barcelona, Barcelona, Spain

    Conxita Arenas

  3. Departament de Genètica, Microbiologia i Estadística, Secció Genètica Biomèdica, Evolució i Desenvolupament, Facultat de Biologia, Universitat de Barcelona, Av. Diagonal, 643, 08028, Barcelona, Spain

    Francesc Mestres

  4. IRBio – Institut de Recerca de la Biodiversitat, Universitat de Barcelona, Barcelona, Spain

    Francesc Mestres

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  1. Goran Zivanovic
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Zivanovic, G., Arenas, C. & Mestres, F. Rate of change for the thermal adapted inversions in Drosophila subobscura. Genetica 147, 401–409 (2019). https://doi.org/10.1007/s10709-019-00078-y

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