Positive selection and precipitation effects on the mitochondrial NADH dehydrogenase subunit 6 gene in brown hares (Lepus europaeus) under a phylogeographic perspective
Autoři:
Milomir Stefanović aff001; Mihajla Djan aff001; Nevena Veličković aff001; Dejan Beuković aff002; Vukan Lavadinović aff003; Chavdar Dinev Zhelev aff004; Yasin Demirbaş aff005; Ladislav Paule aff006; Csongor István Gedeon aff007; Zissis Mamuris aff008; Annika Posautz aff009; Christoph Beiglböck aff009; Anna Kübber-Heiss aff009; Franz Suchentrunk aff009
Působiště autorů:
Department of Biology and Ecology, Faculty of Sciences, University of Novi Sad, Novi Sad, Serbia
aff001; Faculty of Agriculture, University of Novi Sad, Novi Sad, Serbia
aff002; Faculty of Forestry, University of Belgrade, Belgrade, Serbia
aff003; Southwestern State Forest Enterprise Blagoevgrad, Blagoevgrad, Bulgaria
aff004; Faculty of Science and Arts, University of Kırıkkale, Kırıkkale, Turkey
aff005; Faculty of Forestry, Technical University, Zvolen, Slovakia
aff006; Institute for Soil Sciences and Agricultural Chemistry, Hungarian Academy of Sciences, Budapest, Hungary
aff007; Department of Biochemistry and Biotechnology, University of Thessaly, Larrisa, Greece
aff008; Research Institute of Wildlife Ecology, University of Veterinary Medicine Vienna, Vienna, Austria
aff009
Vyšlo v časopise:
PLoS ONE 14(11)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0224902
Souhrn
Previous studies in hares and jackrabbits have indicated that positive selection has shaped the genetic diversity of mitochondrial genes involved in oxidative phosphorylation, which may affect cellular energy production and cause regional adaptation to different environmental (climatic) pressures. In the present study, we sequenced the NADH dehydrogenase subunit 6 (MT-ND6) gene of 267 brown hares (L. europaeus) from Europe and Asia Minor and tested for positive selection and adaptations acting on amino acid sequences (protein variants). Molecular diversity indices and spatial clustering were assessed by DnaSP, Network, and Geneland, while the presence of selection signals was tested by codeml in PAML, and by using the Datamonkey Adaptive Evolution web server. The SPSS software was used to run multinomial regression models to test for possible effects of climate parameters on the currently obtained protein variants. Fifty-eight haplotypes were revealed with a haplotype diversity of 0.817, coding for 17 different protein variants. The MT-ND6 phylogeographic pattern as determined by the nucleotide sequences followed the earlier found model based on the neutrally evolving D-loop sequences, and reflected the earlier found phylogeographic Late Pleistocene scenario. Based on several selection tests, only one codon position consistently proved to be under positive selection. It did occur exclusively in the evolutionarily younger hares from Europe and it gave rise to several protein variants from the southeastern and south-central Balkans. The occurrence of several of those variants was significantly favored under certain precipitation conditions, as proved by our multinomial regression models. Possibly, the great altitudinal variation in the Balkans may have lead to bigger changes in precipitation across that region and this may have imposed an evolutionarily novel selective pressure on the protein variants and could have led to regional adaptation.
Klíčová slova:
Haplotypes – Molecular evolution – Europe – Evolutionary genetics – Mitochondrial DNA – Phylogeography – Hares – Evolutionary adaptation
Zdroje
1. Consuegra S, John E, Verspoor E, De Leaniz CG. Patterns of natural selection acting on the mitochondrial genome of a locally adapted fish species. Genetics Selection Evolution. 2015;47(1): 58.
2. Avise JC. Molecular markers, natural history and evolution. Springer Science & Business Media; 2012.
3. Ballard JW, Whitlock MC. The incomplete natural history of mitochondria. Molecular ecology. 2004;13(4): 729–44. doi: 10.1046/j.1365-294x.2003.02063.x 15012752
4. Meiklejohn CD, Montooth KL, Rand DM. Positive and negative selection on the mitochondrial genome. Trends in Genetics. 2007;23(6): 259–63. doi: 10.1016/j.tig.2007.03.008 17418445
5. Ballard JW, Melvin RG. Linking the mitochondrial genotype to the organismal phenotype. Molecular Ecology. 2010;19(8): 1523–39. doi: 10.1111/j.1365-294X.2010.04594.x 20345689
6. Ben Slimen H, Awadi A, Tolesa ZG, Knauer F, Alves PC, Makni M, et al. Positive selection on the mitochondrial ATP synthase 6 and the NADH dehydrogenase 2 genes across 22 hare species (genus Lepus). Journal of Zoological Systematics and Evolutionary Research. 2018;56(3): 428–43.
7. Ben Slimen H, Schaschl H, Knauer F, Suchentrunk F. Selection on the mitochondrial ATP synthase 6 and the NADH dehydrogenase 2 genes in hares (Lepus capensis L., 1758) from a steep ecological gradient in North Africa. BMC Evolutionary Biology. 2017;17(1): 46. doi: 10.1186/s12862-017-0896-0 28173765
8. da Fonseca RR, Johnson WE, O'Brien SJ, Ramos MJ, Antunes A. The adaptive evolution of the mammalian mitochondrial genome. BMC Genomics. 2008;9(1): 119.
9. Gu P, Liu W, Yao YF, Ni QY, Zhang MW, Li DY, et al. Evidence of adaptive evolution of alpine pheasants to high-altitude environment from mitogenomic perspective. Mitochondrial DNA Part A. 2016;27(1): 455–62.
10. Melo-Ferreira J, Vilela J, Fonseca MM, da Fonseca RR, Boursot P, Alves PC. The elusive nature of adaptive mitochondrial DNA evolution of an arctic lineage prone to frequent introgression. Genome Biology and Evolution. 2014;6(4): 886–96. doi: 10.1093/gbe/evu059 24696399
11. Morales HE, Pavlova A, Joseph L, Sunnucks P. Positive and purifying selection in mitochondrial genomes of a bird with mitonuclear discordance. Molecular Ecology. 2015;24(11): 2820–37. doi: 10.1111/mec.13203 25876460
12. Sharma LK, Lu J, Bai Y. Mitochondrial respiratory complex I: structure, function and implication in human diseases. Current Medicinal Chemistry. 2009;16(10): 1266–77. doi: 10.2174/092986709787846578 19355884
13. Kumar S. Patterns of nucleotide substitution in mitochondrial protein coding genes of vertebrates. Genetics. 1996;143(1): 537–48. 8722802
14. Bai Y, Attardi G. The mtDNA‐encoded ND6 subunit of mitochondrial NADH dehydrogenase is essential for the assembly of the membrane arm and the respiratory function of the enzyme. The EMBO journal. 1998;17(16): 4848–58. doi: 10.1093/emboj/17.16.4848 9707444
15. Yuan Y, Wang W, Li H, Yu Y, Tao J, Huang S, et al. Nonsense and missense mutation of mitochondrial ND6 gene promotes cell migration and invasion in human lung adenocarcinoma. BMC Cancer. 2015;15(1): 346.
16. Schapira AH. Mitochondrial disease. The Lancet. 2006;368(9529): 70–82.
17. Yu L, Wang X, Ting N, Zhang Y. Mitogenomic analysis of Chinese snub-nosed monkeys: Evidence of positive selection in NADH dehydrogenase genes in high-altitude adaptation. Mitochondrion. 2011;11(3): 497–503. doi: 10.1016/j.mito.2011.01.004 21292038
18. Ning T, Xiao H, Li J, Hua S, Zhang YP. Adaptive evolution of the mitochondrial ND6 gene in the domestic horse. Genetics and Molecular Research. 2010;9(1): 144–50. doi: 10.4238/vol9-1gmr705 20198570
19. Flux JE, Angermann R. The hares and jackrabbits. Rabbits, hares and pikas. Status survey and conservation action plan. 1990;4: 61–94.
20. Ashrafzadeh MR, Djan M, Szendrei L, Paulauskas A, Scandura M, Bagi Z, et al. Large-scale mitochondrial DNA analysis reveals new light on the phylogeography of Central and Eastern-European Brown hare (Lepus europaeus Pallas, 1778). PloS one. 2018;13(10): e0204653. doi: 10.1371/journal.pone.0204653 30286121
21. Djan M, Stefanović M, Veličković N, Lavadinović V, Alves PC, Suchentrunk F. Brown hares (Lepus europaeus Pallas, 1778) from the Balkans: a refined phylogeographic model. Hystrix, the Italian Journal of Mammalogy. 2017;28(2): 1–8.
22. Kasapidis P, Suchentrunk F, Magoulas A, Kotoulas G. The shaping of mitochondrial DNA phylogeographic patterns of the brown hare (Lepus europaeus) under the combined influence of Late Pleistocene climatic fluctuations and anthropogenic translocations. Molecular Phylogenetics and Evolution. 2005;34(1): 55–66. doi: 10.1016/j.ympev.2004.09.007 15579381
23. Fickel J, Hauffe HC, Pecchioli E, Soriguer R, Vapa L, Pitra C. Cladogenesis of the European brown hare (Lepus europaeus Pallas, 1778). European journal of wildlife research. 2008;54(3): 495.
24. Stamatis C, Suchentrunk F, Moutou KA, Giacometti M, Haerer G, Djan M, et al. Phylogeography of the brown hare (Lepus europaeus) in Europe: a legacy of south‐eastern Mediterranean refugia?. Journal of Biogeography. 2009;36(3): 515–28.
25. Sert H, Slimen HB, Erdoğan A, Suchentrunk F. Mitochondrial HVI sequence variation in Anatolian hares (Lepus europaeus Pallas, 1778). Mammalian Biology. 2009;74(4): 286–97.
26. Antoniou A, Magoulas A, Platis P, Kotoulas G. Assessing the genetic landscape of a contact zone: the case of European hare in northeastern Greece. Genetica. 2013;141(1–3): 23–40. doi: 10.1007/s10709-013-9703-z 23381134
27. Slimen HB, Suchentrunk F, Stamatis C, Mamuris Z, Sert H, Alves PC, et al. Population genetics of cape and brown hares (Lepus capensis and L. europaeus): A test of Petter's hypothesis of conspecificity. Biochemical Systematics and Ecology. 2008;36(1): 22–39.
28. Demirbaş Y, Albayrak İ, Koca AÖ, Stefanović M, Knauer F, Suchentrunk F. Spatial genetics of brown hares (Lepus europaeus Pallas, 1778) from Turkey: Different gene pool architecture on either side of the Bosphorus?. Mammalian Biology. 2019;94: 77–85.
29. Fickel J, Schmidt A, Putze M, Spittler H, Ludwig A, Streich WJ, et al. Genetic structure of populations of European brown hare: implications for management. The Journal of Wildlife Management. 2005;69(2): 760–70.
30. Hartl GB, Suchentrunk F, Nadlinger K, Willing R. An integrative analysis of genetic differentiation in the brown hare Lepus europaeus based on morphology, allozymes, and mitochondrial DNA. Acta Theriologica. 1993;38: 33–.
31. Mamuris Z, Sfougaris AI, Stamatis C, Suchentrunk F. Assessment of genetic structure of Greek brown hare (Lepus europaeus) populations based on variation in random amplified polymorphic DNA (RAPD). Biochemical Genetics. 2002;40(9–10): 323–38. doi: 10.1023/a:1020260819629 12392170
32. Sert H, Suchentrunk F, Erdoğan A. Genetic diversity within Anatolian brown hares (Lepus europaeus Pallas, 1778) and differentiation among Anatolian and European populations. Mammalian Biology. 2005;70(3): 171–86.
33. Suchentrunk F, Michailov C, Markov G, Haiden A. Population genetics of Bulgarian brown hares Lepus europaeus: allozymic diversity at zoogeographical crossroads. Acta Theriologica. 2000;45(1): 1–2.
34. Suchentrunk F, Mamuris Z, Sfougaris AI, Stamatis C. Biochemical genetic variability in brown hares (Lepus europaeus) from Greece. Biochemical Genetics. 2003;41(5–6): 127–40. doi: 10.1023/a:1023354709392 12834043
35. Vapa L, Djan M, Obreht D, Hammer S, Suchentrunk F. Allozyme variability of brown hares (Lepus europaeus) from the Vojvodina (Serbia), compared to central and south eastern European populations. Acta Zoologica Academiae Scientiarum Hungaricae. 2007;53(1): 75–87.
36. Strzała T, Stamatis C, Kosowska B, Moska M, Marszałek-Kruk B, Mamuris Z. Genetic variability of the Polish brown hare (Lepus europaeus) based on PCR-RFLP mtDNA analysis (preliminary results). Electronic Journal of Polish Agricultural Universities. Series Veterinary Medicine. 2008;11(1).
37. Giannoulis T, Plageras D, Stamatis C, Chatzivagia E, Tsipourlianos A, Birtsas P, et al. Islands and hybrid zones: combining the knowledge from “Natural Laboratories” to explain phylogeographic patterns of the European brown hare. BMC Evolutionary Biology. 2019;19(1): 17. doi: 10.1186/s12862-019-1354-y 30630408
38. Zagwijn WH. An analysis of Eemian climate in western and central Europe. Quaternary Science Reviews. 1996;15(5–6): 451–69.
39. Russell DW, Sambrook J. Molecular cloning: a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; 2001.
40. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. InNucleic acids symposium series 1999 (Vol. 41, No. 41, pp. 95–98). [London]: Information Retrieval Ltd., c1979-c2000.
41. Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25(11): 1451–2. doi: 10.1093/bioinformatics/btp187 19346325
42. Excoffier L, Lischer HE. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources. 2010;10(3): 564–7. doi: 10.1111/j.1755-0998.2010.02847.x 21565059
43. Bandelt HJ, Forster P, Röhl A. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution. 1999;16(1): 37–48. doi: 10.1093/oxfordjournals.molbev.a026036 10331250
44. Guillot G, Mortier F, Estoup A. GENELAND: a computer package for landscape genetics. Molecular Ecology Notes. 2005;5(3): 712–5.
45. Manolopoulou I, Hille A, Emerson B. BPEC: An R Package for Bayesian Phylogeographic and Ecological Clustering. arXiv preprint arXiv:1604.01617. 2016.
46. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution. 2007;24(8): 1586–91. doi: 10.1093/molbev/msm088 17483113
47. Krogh A, Larsson B, Von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. Journal of Molecular Biology. 2001;305(3): 567–80. doi: 10.1006/jmbi.2000.4315 11152613
48. Zhang Y. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics. 2008;9(1): 40.
49. McGuffin LJ, Bryson K, Jones DT. The PSIPRED protein structure prediction server. Bioinformatics. 2000;16(4): 404–5. doi: 10.1093/bioinformatics/16.4.404 10869041
50. Balloux F, Handley LJ, Jombart T, Liu H, Manica A. Climate shaped the worldwide distribution of human mitochondrial DNA sequence variation. Proceedings of the Royal Society B: Biological Sciences. 2009;276(1672): 3447–55. doi: 10.1098/rspb.2009.0752 19586946
51. Foote AD, Morin PA, Durban JW, Pitman RL, Wade P, Willerslev E, Gilbert MT, da Fonseca RR. Positive selection on the killer whale mitogenome. Biology Letters. 2010;7(1): 116–8. doi: 10.1098/rsbl.2010.0638 20810427
52. Garvin MR, Bielawski JP, Gharrett AJ. Positive Darwinian selection in the piston that powers proton pumps in complex I of the mitochondria of Pacific salmon. PloS One. 2011;6(9): e24127. doi: 10.1371/journal.pone.0024127 21969854
53. Holt IJ, editor. Genetics of mitochondrial diseases. Oxford University Press; 2003.
54. Fan W, Waymire KG, Narula N, Li P, Rocher C, Coskun PE, et al. A mouse model of mitochondrial disease reveals germline selection against severe mtDNA mutations. Science. 2008;319(5865): 958–62. doi: 10.1126/science.1147786 18276892
55. Wilson DE, Reeder DM, editors. Mammal species of the world: a taxonomic and geographic reference. JHU Press; 2005.
56. Zhelev C. Status and influence of some ecological factors on the stocks of brown hare (Lepus capensis Linnaeus, 1758) in lowland habitats in Bulgaria. PhD Thesis, Faculty of Forestry, Sofia, Bulgaria. 2015.
57. Pickarski N, Kwiecien O, Djamali M, Litt T. Vegetation and environmental changes during the last interglacial in eastern Anatolia (Turkey): a new high-resolution pollen record from Lake Van. Palaeogeography, Palaeoclimatology, Palaeoecology. 2015;435: 145–58.
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