Genetic admixture drives climate adaptation in the bank vole

. 2024 Jul 15 ; 7 (1) : 863. [epub] 20240715

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid39009753

Grantová podpora
20-11058S Grantová Agentura České Republiky (Grant Agency of the Czech Republic)

Odkazy

PubMed 39009753
PubMed Central PMC11251159
DOI 10.1038/s42003-024-06549-z
PII: 10.1038/s42003-024-06549-z
Knihovny.cz E-zdroje

Genetic admixture introduces new variants at relatively high frequencies, potentially aiding rapid responses to environmental changes. Here, we evaluate its role in adaptive variation related to climatic conditions in bank voles (Clethrionomys glareolus) in Britain, using whole-genome data. Our results reveal loci showing excess ancestry from one of the two postglacial colonist populations inconsistent with overall admixture patterns. Notably, loci associated with climate adaptation exhibit disproportionate amounts of excess ancestry, highlighting the impact of admixture between colonist populations on local adaptation. The results suggest strong and localized selection on climate-adaptive loci, as indicated by steep clines and/or shifted cline centres, during population replacement. A subset, including a haemoglobin gene, is associated with oxidative stress responses, underscoring a role of oxidative stress in local adaptation. Our study highlights the important contribution of admixture during secondary contact between populations from distinct climatic refugia enriching adaptive diversity. Understanding these dynamics is crucial for predicting future adaptive capacity to anthropogenic climate change.

Zobrazit více v PubMed

Bitter MC, Kapsenberg L, Gattuso J-P, Pfister CA. Standing genetic variation fuels rapid adaptation to ocean acidification. Nat. Commun. 2019;10:5821. doi: 10.1038/s41467-019-13767-1. PubMed DOI PMC

Jones FC, et al. The genomic basis of adaptive evolution in threespine sticklebacks. Nature. 2012;484:55–61. doi: 10.1038/nature10944. PubMed DOI PMC

Lai Y-T, et al. Standing genetic variation as the predominant source for adaptation of a songbird. Proc. Natl Acad. Sci. USA. 2019;116:2152–2157. doi: 10.1073/pnas.1813597116. PubMed DOI PMC

Matuszewski S, Hermisson J, Kopp M. Catch me if you can: adaptation from standing genetic variation to a moving phenotypic optimum. Genetics. 2015;200:1255–1274. doi: 10.1534/genetics.115.178574. PubMed DOI PMC

Reid NM, et al. The genomic landscape of rapid repeated evolutionary adaptation to toxic pollution in wild fish. Science. 2016;354:1305–1308. doi: 10.1126/science.aah4993. PubMed DOI PMC

Hedrick PW. Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation. Mol. Ecol. 2013;22:4606–4618. doi: 10.1111/mec.12415. PubMed DOI

Lenormand T. Gene flow and the limits to natural selection. Trends Ecol. Evol. 2002;17:183–189. doi: 10.1016/S0169-5347(02)02497-7. DOI

Hewitt G. The genetic legacy of the Quaternary ice ages. Nature. 2000;405:907–913. doi: 10.1038/35016000. PubMed DOI

de Lafontaine G, Napier JD, Petit RJ, Hu FS. Invoking adaptation to decipher the genetic legacy of past climate change. Ecology. 2018;99:1530–1546. doi: 10.1002/ecy.2382. PubMed DOI

de Carvalho D, et al. Admixture facilitates adaptation from standing variation in the European aspen (Populus tremula L.), a widespread forest tree. Mol. Ecol. 2010;19:1638–1650. doi: 10.1111/j.1365-294X.2010.04595.x. PubMed DOI

Escalante MA, Marková S, Searle JB, Kotlík P. Genic distribution modelling predicts adaptation of the bank vole to climate change. Commun. Biol. 2022;5:981. doi: 10.1038/s42003-022-03935-3. PubMed DOI PMC

Martins K, et al. Landscape genomics provides evidence of climate-associated genetic variation in Mexican populations of Quercus rugosa. Evol. Appl. 2018;11:1842–1858. doi: 10.1111/eva.12684. PubMed DOI PMC

Gompert Z, Buerkle CA. A powerful regression-based method for admixture mapping of isolation across the genome of hybrids. Mol. Ecol. 2009;18:1207–1224. doi: 10.1111/j.1365-294X.2009.04098.x. PubMed DOI

Norris LC, et al. Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets. Proc. Natl Acad. Sci. USA. 2015;112:815–820. doi: 10.1073/pnas.1418892112. PubMed DOI PMC

Song Y, et al. Adaptive introgression of anticoagulant rodent poison resistance by hybridization between Old World mice. Curr. Biol. 2011;21:1296–1301. doi: 10.1016/j.cub.2011.06.043. PubMed DOI PMC

Barnes I, Matheus P, Shapiro B, Jensen D, Cooper A. Dynamics of Pleistocene population extinctions in Beringian brown bears. Science. 2002;295:2267–2270. doi: 10.1126/science.1067814. PubMed DOI

Brace S, et al. The colonization history of British water vole (Arvicola amphibius (Linnaeus, 1758)): origins and development of the Celtic fringe. Proc. R. Soc. B. 2016;283:20160130. doi: 10.1098/rspb.2016.0130. PubMed DOI PMC

Dolby GA, et al. Sea-level driven glacial-age refugia and post-glacial mixing on subtropical coasts, a palaeohabitat and genetic study. Proc. R. Soc. B. 2016;283:20161571. doi: 10.1098/rspb.2016.1571. PubMed DOI PMC

Kotlík P, Marková S, Konczal M, Wiesław B, Searle JB. Genomics of end-Pleistocene population replacement in a small mammal. Proc. R. Soc. B. 2018;285:20172624. doi: 10.1098/rspb.2017.2624. PubMed DOI PMC

Marková S, et al. High genomic diversity in the bank vole at the northern apex of a range expansion: The role of multiple colonizations and end-glacial refugia. Mol. Ecol. 2020;29:1730–1744. doi: 10.1111/mec.15427. PubMed DOI

Searle JB, et al. The Celtic fringe of Britain: insights from small mammal phylogeography. Proc. R. Soc. B. 2009;276:4287–4294. doi: 10.1098/rspb.2009.1422. PubMed DOI PMC

Lanier HC, Gunderson AM, Weksler M, Fedorov VB, Olson LE. Comparative phylogeography highlights the double-edged sword of climate change faced by arctic- and alpine-adapted mammals. PLoS One. 2015;10:e0118396. doi: 10.1371/journal.pone.0118396. PubMed DOI PMC

Moritz C, et al. Identification and dynamics of a cryptic suture zone in tropical rainforest. Proc. R. Soc. B. 2009;276:1235–1244. doi: 10.1098/rspb.2008.1622. PubMed DOI PMC

Szymura JM, Barton NH. Genetic analysis of a hybrid zone between the fire-bellied toads, Bombina bombina and B. variegata, near Cracow in southern Poland. Evolution. 1986;40:1141–1159. PubMed

Gompert Z, Buerkle CA. Bayesian estimation of genomic clines. Mol. Ecol. 2011;20:2111–2127. doi: 10.1111/j.1365-294X.2011.05074.x. PubMed DOI

Fitzpatrick BM. Alternative forms for genomic clines. Ecol. Evol. 2013;3:1951–1966. doi: 10.1002/ece3.609. PubMed DOI PMC

Menon M, et al. Tracing the footprints of a moving hybrid zone under a demographic history of speciation with gene flow. Evol. Appl. 2020;13:195–209. doi: 10.1111/eva.12795. PubMed DOI PMC

Del-Rio G, et al. Displaced clines in an avian hybrid zone (Thamnophilidae: Rhegmatorhina) within an Amazonian interfluve. Evolution. 2022;76:455–475. doi: 10.1111/evo.14377. PubMed DOI

Caeiro-Dias G, Brelsford A, Meneses-Ribeiro M, Crochet P-A, Pinho C. Hybridization in late stages of speciation: Strong but incomplete genome-wide reproductive isolation and ‘large Z-effect’ in a moving hybrid zone. Mol. Ecol. 2023;32:4362–4380. doi: 10.1111/mec.17035. PubMed DOI

Hodel RGJ, Massatti R, Knowles LL. Hybrid enrichment of adaptive variation revealed by genotype–environment associations in montane sedges. Mol. Ecol. 2022;31:3722–3737. doi: 10.1111/mec.16502. PubMed DOI PMC

Hall SJG. Haemoglobin polymorphism in the bank vole, Clethrionomys glareolus, in Britain. J. Zool. 1979;187:153–160. doi: 10.1111/j.1469-7998.1979.tb03939.x. DOI

Kotlík P, et al. Adaptive phylogeography: functional divergence between haemoglobins derived from different glacial refugia in the bank vole. Proc. R. Soc. B. 2014;281:20140021. doi: 10.1098/rspb.2014.0021. PubMed DOI PMC

Strážnická M, Marková S, Searle JB, Kotlík P. Playing hide-and-seek in beta-globin genes: gene conversion transferring a beneficial mutation between differentially expressed gene duplicates. Genes. 2018;9:492. doi: 10.3390/genes9100492. PubMed DOI PMC

Birnie-Gauvin K, Costantini D, Cooke SJ, Willmore WG. A comparative and evolutionary approach to oxidative stress in fish: A review. Fish. Fish. 2017;18:928–942. doi: 10.1111/faf.12215. DOI

Chaudhry S, Sidhu GPS. Climate change regulated abiotic stress mechanisms in plants: a comprehensive review. Plant Cell Rep. 2022;41:1–31. doi: 10.1007/s00299-021-02759-5. PubMed DOI

Metcalfe NB, Alonso-Alvarez C. Oxidative stress as a life-history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death. Funct. Ecol. 2010;24:984–996. doi: 10.1111/j.1365-2435.2010.01750.x. DOI

Paital B, et al. Longevity of animals under reactive oxygen species stress and disease susceptibility due to global warming. World J. Biol. Chem. 2016;7:110–127. doi: 10.4331/wjbc.v7.i1.110. PubMed DOI PMC

Lennon JJ, Koleff P, GreenwooD JJD, Gaston KJ. The geographical structure of British bird distributions: diversity, spatial turnover and scale. J. Anim. Ecol. 2001;70:966–979. doi: 10.1046/j.0021-8790.2001.00563.x. DOI

Mayes J. Changing regional climatic gradients in the United Kingdom. Geogr. J. 2000;166:125–138. doi: 10.1111/j.1475-4959.2000.tb00013.x. DOI

Marková, S. et al. Data from: Local adaptation and future climate vulnerability in a wild rodent. Dryad. 10.5061/dryad.kwh70rz96 (2023). PubMed PMC

Marková S, et al. Local adaptation and future climate vulnerability in a wild rodent. Nat. Commun. 2023;14:7840. doi: 10.1038/s41467-023-43383-z. PubMed DOI PMC

Capblancq T, Lachmuth S, Fitzpatrick MC, Keller SR. From common gardens to candidate genes: exploring local adaptation to climate in red spruce. N. Phytol. 2023;237:1590–1605. doi: 10.1111/nph.18465. PubMed DOI PMC

Chen Y, Gao Y, Huang X, Li S, Zhan A. Local environment-driven adaptive evolution in a marine invasive ascidian (Molgula manhattensis) Ecol. Evol. 2021;11:4252–4266. doi: 10.1002/ece3.7322. PubMed DOI PMC

Du FK, Wang T, Wang Y, Ueno S, de Lafontaine G. Contrasted patterns of local adaptation to climate change across the range of an evergreen oak, Quercus aquifolioides. Evol. Appl. 2020;13:2377–2391. doi: 10.1111/eva.13030. PubMed DOI PMC

Ma L, et al. Rapid and strong population genetic differentiation and genomic signatures of climatic adaptation in an invasive mealybug. Divers. Distrib. 2020;26:610–622. doi: 10.1111/ddi.13053. DOI

Ruiz Miñano M, et al. Population genetic differentiation and genomic signatures of adaptation to climate in an abundant lizard. Heredity. 2022;128:271–278. doi: 10.1038/s41437-022-00518-0. PubMed DOI PMC

Gompert Z, Buerkle CA. bgc: Software for Bayesian estimation of genomic clines. Mol. Ecol. Resour. 2012;12:1168–1176. doi: 10.1111/1755-0998.12009.x. PubMed DOI

Forester BR, Lasky JR, Wagner HH, Urban DL. Comparing methods for detecting multilocus adaptation with multivariate genotype–environment associations. Mol. Ecol. 2018;27:2215–2233. doi: 10.1111/mec.14584. PubMed DOI

Hamilton JA, Miller JM. Adaptive introgression as a resource for management and genetic conservation in a changing climate. Conserv. Biol. 2016;30:33–41. doi: 10.1111/cobi.12574. PubMed DOI

Sung C-J, Bell KL, Nice CC, Martin NH. Integrating Bayesian genomic cline analyses and association mapping of morphological and ecological traits to dissect reproductive isolation and introgression in a Louisiana Iris hybrid zone. Mol. Ecol. 2018;27:959–978. doi: 10.1111/mec.14481. PubMed DOI

Parchman TL, et al. The genomic consequences of adaptive divergence and reproductive isolation between species of manakins. Mol. Ecol. 2013;22:3304–3317. doi: 10.1111/mec.12201. PubMed DOI

Anderson TM, et al. Molecular and evolutionary history of melanism in North American gray wolves. Science. 2009;323:1339–1343. doi: 10.1126/science.1165448. PubMed DOI PMC

Huerta-Sánchez E, et al. Altitude adaptation in Tibetans caused by introgression of Denisovan-like DNA. Nature. 2014;512:194–197. doi: 10.1038/nature13408. PubMed DOI PMC

vonHoldt B, Fan Z, Vecchyo DO-D, Wayne RK. EPAS1 variants in high altitude Tibetan wolves were selectively introgressed into highland dogs. PeerJ. 2017;5:e3522. doi: 10.7717/peerj.3522. PubMed DOI PMC

Barton NH, Hewitt GM. Analysis of hybrid zones. Annu. Rev. Ecol. Syst. 1985;16:113–148. doi: 10.1146/annurev.es.16.110185.000553. DOI

Buggs RJA. Empirical study of hybrid zone movement. Heredity. 2007;99:301–312. doi: 10.1038/sj.hdy.6800997. PubMed DOI

Dvořáková, V., Horníková, M., Němcová, L., Marková, S. & Kotlík, P. Regulatory variation in functionally polymorphic globin genes of the bank vole: a possible role for adaptation. Front. Ecol. Evol. 7, 514 (2020).

Lee N, et al. The role of fucoxanthin as a potent Nrf2 activator via Akt/GSK-3β/Fyn axis against amyloid-β peptide-induced oxidative damage. Antioxidants. 2023;12:629. doi: 10.3390/antiox12030629. PubMed DOI PMC

Mathur A, Rizvi F, Kakkar P. PHLPP2 down regulation influences nuclear Nrf2 stability via Akt-1/Gsk3β/Fyn kinase axis in acetaminophen induced oxidative renal toxicity: Protection accorded by morin. Food Chem. Toxicol. 2016;89:19–31. doi: 10.1016/j.fct.2016.01.001. PubMed DOI

Alfaleh MA, et al. Extracellular matrix detached cancer cells resist oxidative stress by increasing histone demethylase KDM6 activity. Saudi J. Biol. Sci. 2024;31:103871. doi: 10.1016/j.sjbs.2023.103871. PubMed DOI PMC

Salmond RJ, Filby A, Qureshi I, Caserta S, Zamoyska R. T-cell receptor proximal signaling via the Src-family kinases, Lck and Fyn, influences T-cell activation, differentiation, and tolerance. Immunol. Rev. 2009;228:9–22. doi: 10.1111/j.1600-065X.2008.00745.x. PubMed DOI

Saminathan H, et al. Fyn kinase mediates pro-inflammatory response in a mouse model of endotoxemia: relevance to translational research. Eur. J. Pharmacol. 2020;881:173259. doi: 10.1016/j.ejphar.2020.173259. PubMed DOI PMC

Mkaddem SB, et al. Lyn and Fyn function as molecular switches that control immunoreceptors to direct homeostasis or inflammation. Nat. Commun. 2017;8:246. doi: 10.1038/s41467-017-00294-0. PubMed DOI PMC

Salminen A, Kaarniranta K, Hiltunen M, Kauppinen A. Histone demethylase Jumonji D3 (JMJD3/KDM6B) at the nexus of epigenetic regulation of inflammation and the aging process. J. Mol. Med. 2014;92:1035–1043. doi: 10.1007/s00109-014-1182-x. PubMed DOI

Chatterjee, S. Chapter Two - Oxidative Stress, Inflammation, and Disease. In Oxidative Stress and Biomaterials (eds. Dziubla, T. & Butterfield, D. A.) 35–58 (Academic Press, 2016). 10.1016/B978-0-12-803269-5.00002-4.

Damal Villivalam S, et al. A necessary role of DNMT3A in endurance exercise by suppressing ALDH1L1‐mediated oxidative stress. EMBO J. 2021;40:e106491. doi: 10.15252/embj.2020106491. PubMed DOI PMC

Crowley JL, Smith TC, Fang Z, Takizawa N, Luna EJ. Supervillin reorganizes the actin cytoskeleton and increases invadopodial efficiency. Mol. Biol. Cell. 2009;20:948–962. doi: 10.1091/mbc.e08-08-0867. PubMed DOI PMC

Kuwabara Y, et al. A human FLII gene variant alters sarcomeric actin thin filament length and predisposes to cardiomyopathy. Proc. Natl Acad. Sci. USA. 2023;120:e2213696120. doi: 10.1073/pnas.2213696120. PubMed DOI PMC

Watanabe T, Wang S, Kaibuchi K. IQGAPs as key regulators of actin-cytoskeleton dynamics. Cell Struct. Funct. 2015;40:69–77. doi: 10.1247/csf.15003. PubMed DOI

Bamburg JR, et al. ADF/cofilin-actin rods in neurodegenerative diseases. Curr. Alzheimer Res. 2010;7:241–250. doi: 10.2174/156720510791050902. PubMed DOI PMC

Farah ME, Sirotkin V, Haarer B, Kakhniashvili D, Amberg DC. Diverse protective roles of the actin cytoskeleton during oxidative stress. Cytoskeleton. 2011;68:340–354. doi: 10.1002/cm.20516. PubMed DOI PMC

Miriyala S, et al. Novel role of 4-hydroxy-2-nonenal in AIFm2-mediated mitochondrial stress signaling. Free Radic. Biol. Med. 2016;91:68–80. doi: 10.1016/j.freeradbiomed.2015.12.002. PubMed DOI PMC

Lu J, et al. Activation of AIFM2 enhances apoptosis of human lung cancer cells undergoing toxicological stress. Toxicol. Lett. 2016;258:227–236. doi: 10.1016/j.toxlet.2016.07.002. PubMed DOI

Breuza L, et al. Proteomics of endoplasmic reticulum-Golgi intermediate compartment (ERGIC) membranes from brefeldin A-treated HepG2 cells identifies ERGIC-32, a new cycling protein that interacts with human Erv46. J. Biol. Chem. 2004;279:47242–47253. doi: 10.1074/jbc.M406644200. PubMed DOI

Choi SS, et al. Flightless-1 inhibits ER stress-induced apoptosis in colorectal cancer cells by regulating Ca2+ homeostasis. Exp. Mol. Med. 2020;52:940–950. doi: 10.1038/s12276-020-0448-3. PubMed DOI PMC

Jofre GI, Rosenthal GG. A narrow window for geographic cline analysis using genomic data: Effects of age, drift, and migration on error rates. Mol. Ecol. Resour. 2021;21:2278–2287. doi: 10.1111/1755-0998.13428. PubMed DOI PMC

McFarlane SE, Senn HV, Smith SL, Pemberton JM. Locus-specific introgression in young hybrid swarms: Drift may dominate selection. Mol. Ecol. 2021;30:2104–2115. doi: 10.1111/mec.15862. PubMed DOI

Akopyan M, et al. Genetic and phenotypic evidence of a contact zone between divergent colour morphs of the iconic red-eyed treefrog. Mol. Ecol. 2020;29:4442–4456. doi: 10.1111/mec.15639. PubMed DOI

Jahner JP, Parchman TL, Matocq MD. Multigenerational backcrossing and introgression between two woodrat species at an abrupt ecological transition. Mol. Ecol. 2021;30:4245–4258. doi: 10.1111/mec.16056. PubMed DOI

Rheindt FE, Edwards SV. Genetic introgression: An integral but neglected component of speciation in birds. Auk. 2011;128:620–632. doi: 10.1525/auk.2011.128.4.620. DOI

Kelly E, Phillips BL. Targeted gene flow for conservation. Conserv. Biol. 2016;30:259–267. doi: 10.1111/cobi.12623. PubMed DOI

Meek MH, et al. Understanding local adaptation to prepare populations for climate change. BioScience. 2023;73:36–47. doi: 10.1093/biosci/biac101. DOI

Martin BT, et al. Contrasting signatures of introgression in North American box turtle (Terrapene spp.) contact zones. Mol. Ecol. 2020;29:4186–4202. doi: 10.1111/mec.15622. PubMed DOI

Purcell S, et al. PLINK: A tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 2007;81:559–575. doi: 10.1086/519795. PubMed DOI PMC

Price AL, et al. Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet. 2006;38:904–909. doi: 10.1038/ng1847. PubMed DOI

Alexander DH, Novembre J, Lange K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 2009;19:1655–1664. doi: 10.1101/gr.094052.109. PubMed DOI PMC

Martin BT, Chafin TK, Douglas MR, Douglas ME. ClineHelpR: an R package for genomic cline outlier detection and visualization. BMC Bioinforma. 2021;22:501. doi: 10.1186/s12859-021-04423-x. PubMed DOI PMC

Legendre, P. & Legendre, L. Numerical Ecology (Elsevier, 2012).

Fick SE, Hijmans RJ. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 2017;37:4302–4315. doi: 10.1002/joc.5086. DOI

Oksanen, J. et al. vegan: Community Ecology Package. R package version 2.6-4. https://CRAN.R-project.org/package=vegan (2022).

Dormann CF, et al. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography. 2013;36:27–46. doi: 10.1111/j.1600-0587.2012.07348.x. DOI

MacDougall A, et al. UniRule: a unified rule resource for automatic annotation in the UniProt Knowledgebase. Bioinformatics. 2020;36:4643–4648. doi: 10.1093/bioinformatics/btaa485. PubMed DOI PMC

Thomas PD, et al. PANTHER: Making genome-scale phylogenetics accessible to all. Protein Sci. 2022;31:8–22. doi: 10.1002/pro.4218. PubMed DOI PMC

Mi H, Thomas P. PANTHER pathway: an ontology-based pathway database coupled with data analysis tools. Methods Mol. Biol. 2009;563:123–140. doi: 10.1007/978-1-60761-175-2_7. PubMed DOI PMC

Binns D, et al. QuickGO: a web-based tool for Gene Ontology searching. Bioinformatics. 2009;25:3045–3046. doi: 10.1093/bioinformatics/btp536. PubMed DOI PMC

Massicotte, P. & South, A. rnaturalearth: World Map Data from Natural Earth. R package version 1.0.1. https://CRAN.R-project.org/package=rnaturalearth (2023).

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...