The genomic consequences of hybridization

Abstract

In the past decade, advances in genome sequencing have allowed researchers to uncover the history of hybridization in diverse groups of species, including our own. Although the field has made impressive progress in documenting the extent of natural hybridization, both historical and recent, there are still many unanswered questions about its genetic and evolutionary consequences. Recent work has suggested that the outcomes of hybridization in the genome may be in part predictable, but many open questions about the nature of selection on hybrids and the biological variables that shape such selection have hampered progress in this area. We synthesize what is known about the mechanisms that drive changes in ancestry in the genome after hybridization, highlight major unresolved questions, and discuss their implications for the predictability of genome evolution after hybridization.

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110. 110.

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114. 114.

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215. 215.

     Schiffman JS, Ralph PL. System drift and speciation. bioRxiv. 2018.

     Not in our library10.1101/231209

216. 216.

     Schilthuizen M, Giesbers MC, Beukeboom LW. Haldane's rule in the 21st century. Heredity. 2011;107:95-102.

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217. 217.

     Schluter D. Ecological Character Displacement in Adaptive Radiation. 2000.

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218. 218.

     Schneemann H. The geometry and genetics of hybridization. bioRxiv. 2019.

     Not in our library10.1101/862235

219. 219.
     High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species · 2014

     No notice
220. 220.

     Schumer M, Cui R, Rosenthal GG, Andolfatto P. Reproductive isolation of hybrid populations driven by genetic incompatibilities. PLOS Genetics. 2015;11:e1005041.

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221. 221.

     Schumer M, Cui R, Powell DL, Rosenthal GG, Andolfatto P. Ancient hybridization and genomic stabilization in a swordtail fish. Molecular Ecology. 2016;25:2661-2679.

     Not in our library10.1111/mec.13602

222. 222.

     Schumer M, Powell DL, Delclós PJ, Squire M, Cui R, Andolfatto P, Rosenthal GG. Assortative mating and persistent reproductive isolation in hybrids. PNAS. 2017;114:10936-10941.

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223. 223.

     Schumer M, Xu C, Powell DL, Durvasula A, Skov L, Holland C, Blazier JC, Sankararaman S, Andolfatto P, Rosenthal GG, Przeworski M. Natural selection interacts with recombination to shape the evolution of hybrid genomes. Science. 2018;360:656-660.

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224. 224.

     Schumer M. Versatile simulations of admixture and accurate local ancestry inference with mixnmatch and ancestryinfer. Molecular Ecology Resources. 2019;20:1141-1151.

     Not in our library10.1111/1755-0998.13175

225. 225.

     Schumerlab. Software Heritage. 2021.

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226. 226.

     Scordato ESC, Smith CCR, Semenov GA, Liu Y, Wilkins MR, Liang W, Rubtsov A, Sundev G, Koyama K, Turbek SP, Wunder MB, Stricker CA, Safran RJ. Migratory divides coincide with reproductive barriers across replicated avian hybrid zones above the tibetan plateau. Ecology Letters. 2020;23:231-241.

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227. 227.

     Sedghifar A, Brandvain Y, Ralph P, Coop G. The spatial mixing of genomes in secondary contact zones. Genetics. 2015;201:243-261.

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228. 228.

     Sedghifar A, Brandvain Y, Ralph P. Beyond clines: lineages and haplotype blocks in hybrid zones. Molecular Ecology. 2016;25:2559-2576.

     Not in our library10.1111/mec.13677

229. 229.

     Seehausen O. Hybridization and adaptive radiation. Trends in Ecology & Evolution. 2004;19:198-207.

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230. 230.

     Selz OM, Seehausen O. Interspecific hybridization can generate functional novelty in cichlid fish. PNAS. 2019;286:20191621.

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231. 231.

     Setter D, Mousset S, Cheng X, Nielsen R, DeGiorgio M, Hermisson J. VolcanoFinder: genomic scans for adaptive introgression. PLOS Genetics. 2019;16:e1008867.

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232. 232.

     Shaw DD, Wilkinson P. Chromosome differentiation, hybrid breakdown and the maintenance of a narrow hybrid zone in Caledia. Chromosoma. 1980;80:1-31.

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233. 233.

     Shchur V, Svedberg J, Medina P, Corbett-Detig R, Nielsen R. On the distribution of tract lengths during adaptive introgression. G3: Genes, Genomes, Genetics. 2020;10:3663-3673.

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234. 234.

     Shen XX, Opulente DA, Kominek J, Zhou X, Steenwyk JL, Buh KV, Haase MAB, Wisecaver JH, Wang M, Doering DT, Boudouris JT, Schneider RM, Langdon QK, Ohkuma M, Endoh R, Takashima M, Manabe RI, Čadež N, Libkind D, Rosa CA, DeVirgilio J, Hulfachor AB, Groenewald M, Kurtzman CP, Hittinger CT, Rokas A. Tempo and mode of genome evolution in the budding yeast subphylum. Cell. 2018;175:1533-1545.

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235. 235.

     Shorter JR, Odet F, Aylor DL, Pan W, Kao CY, Fu CP, Morgan AP, Greenstein S, Bell TA, Stevans AM, Feathers RW, Patel S, Cates SE, Shaw GD, Miller DR, Chesler EJ, McMillian L, O'Brien DA, Villena FP. Male infertility is responsible for nearly half of the extinction observed in the mouse collaborative cross. Genetics. 2017;206:557-572.

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236. 236.

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237. 237.

     Singhal S, Leffler EM, Sannareddy K, Turner I, Venn O, Hooper DM, Strand AI, Li Q, Raney B, Balakrishnan CN, Griffith SC, McVean G, Przeworski M. Stable recombination hotspots in birds. Science. 2015;350:928-932.

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238. 238.

     Slatkin M, Lande R. Segregation variance after hybridization of isolated populations. Genetical Research. 1994;64:51-56.

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239. 239.

     Sloan DB, Havird JC, Sharbrough J. The on-again, off-again relationship between mitochondrial genomes and species boundaries. Molecular Ecology. 2017;26:2212-2236.

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240. 240.

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241. 241.

     Smith KL, Hale JM, Kearney MR, Austin JJ, Melville J. Molecular patterns of introgression in a classic hybrid zone between the australian tree frogs, Litoria ewingii and L. Paraewingi: evidence of a tension zone. Molecular Ecology. 2013;22:1869-1883.

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242. 242.

     Smukowski Heil CS, Large CRL, Patterson K, Hickey AS, Yeh CC, Dunham MJ. Temperature preference can Bias parental genome retention during hybrid evolution. PLOS Genetics. 2019;15:e1008383.

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243. 243.

     Smukowski Heil C, Patterson K, Hickey AS, Alcantara E, Dunham MJ. Transposable element mobilization in interspecific yeast hybrids. Genome Biology and Evolution. 2021;13:evab033.

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244. 244.

     Soltis DE. Advances in the study of polyploidy since plant speciation. New Phytologist. 2004;161:173-191.

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245. 245.

     Song Y, Endepols S, Klemann N, Richter D, Matuschka FR, Shih CH, Nachman MW, Kohn MH. Adaptive introgression of anticoagulant rodent poison resistance by hybridization between old world mice. Current Biology. 2011;21:1296-1301.

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246. 246.

     Soria-Carrasco V, Gompert Z, Comeault AA, Farkas TE, Parchman TL, Johnston JS, Buerkle CA, Feder JL, Bast J, Schwander T, Egan SP, Crespi BJ, Nosil P. Stick insect genomes reveal natural selection's role in parallel speciation. Science. 2014;344:738-742.

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247. 247.
     Variation in recombination frequency and distribution across eukaryotes: patterns and processes · 2017

     Corrected
248. 248.
     Genome Patterns of Selection and Introgression of Haplotypes in Natural Populations of the House Mouse (Mus musculus) · 2012

     No notice
249. 249.

     Steensels J, Gallone B, Verstrepen KJ. Interspecific hybridization as a driver of fungal evolution and adaptation. Nature Reviews Microbiology. 2021;19:485-500.

     Not in our library10.1038/s41579-021-00537-4

250. 250.
     Phenotypic novelty in experimental hybrids is predicted by the genetic distance between species of cichlid fish · 2009

     No notice
251. 251.

     Stelkens R, Seehausen O. Genetic distance between species predicts novel trait expression in their hybrids. Evolution. 2009;63:884-897.

     Not in our library10.1111/j.1558-5646.2008.00599.x

252. 252.

     Storchová R, Reif J, Nachman MW. Female heterogamety and speciation: reduced introgression of the z chromosome between two species of nightingales. Evolution. 2010;64:456-471.

     Not in our library10.1111/j.1558-5646.2009.00841.x

253. 253.

     Stryjewski KF, Sorenson MD. Mosaic genome evolution in a recent and rapid avian radiation. Nature Ecology & Evolution. 2017;1:1912-1922.

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254. 254.

     Suarez-Gonzalez A, Lexer C, Cronk QCB. Adaptive introgression: a plant perspective. Biology Letters. 2018;14:20170688.

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255. 255.

     Svedin N, Wiley C, Veen T, Gustafsson L, Qvarnström A. Natural and sexual selection against hybrid flycatchers. PNAS. 2008;275:735-744.

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256. 256.

     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.

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257. 257.

     Taylor SA, White TA, Hochachka WM, Ferretti V, Curry RL, Lovette I. Climate-mediated movement of an avian hybrid zone. Current Biology. 2014;24:671-676.

     Not in our library10.1016/j.cub.2014.01.069

258. 258.

     Teeter KC, Payseur BA, Harris LW, Bakewell MA, Thibodeau LM, O'Brien JE, Krenz JG, Sans-Fuentes MA, Nachman MW, Tucker PK. Genome-wide patterns of gene flow across a house mouse hybrid zone. Genome Research. 2008;18:67-76.

     Not in our library10.1101/gr.6757907

259. 259.

     Telis N, Aguilar R, Harris K. Selection against archaic hominin genetic variation in regulatory regions. Nature Ecology & Evolution. 2020;4:1558-1566.

     Not in our library10.1038/s41559-020-01284-0

260. 260.

     Tenaillon O. The utility of Fisher's Geometric Model in Evolutionary Genetics. Annual Review of Ecology, Evolution, and Systematics. 2014;45:179-201.

     Not in our library10.1146/annurev-ecolsys-120213-091846

261. 261.

     Thibert-Plante X, Hendry AP. Five questions on ecological speciation addressed with individual-based simulations. Journal of Evolutionary Biology. 2009;22:109-123.

     Not in our library10.1111/j.1420-9101.2008.01627.x

262. 262.

     Thompson KA. Patterns, predictors, and consequences of dominance in hybrids. bioRxiv. 2019a.

     Not in our library10.1101/818658

263. 263.

     Thompson KA, Osmond MM, Schluter D. Parallel genetic evolution and speciation from standing variation. Evolution Letters. 2019b;3:129-141.

     Not in our library10.1002/evl3.106

264. 264.

     Thompson KA. Experimental hybridization studies suggest that pleiotropic alleles commonly underlie adaptive divergence between natural populations. The American Naturalist. 2020;196:E16-E22.

     Not in our library10.1086/708722

265. 265.

     Todesco M, Owens GL, Bercovich N, Légaré JS, Soudi S, Burge DO, Huang K, Ostevik KL, Drummond EBM, Imerovski I, Lande K, Pascual-Robles MA, Nanavati M, Jahani M, Cheung W, Staton SE, Muños S, Nielsen R, Donovan LA, Burke JM, Yeaman S, Rieseberg LH. Massive haplotypes underlie ecotypic differentiation in sunflowers. Nature. 2020;584:602-607.

     Not in our library10.1038/s41586-020-2467-6

266. 266.
     Evidence for mito-nuclear and sex-linked reproductive barriers between the hybrid Italian sparrow and its parent species. · 2014

     Not checked
267. 267.

     Tulchinsky AY, Johnson NA, Watt WB, Porter AH. Hybrid incompatibility arises in a sequence-based bioenergetic model of transcription factor binding. Genetics. 2014;198:1155-1166.

     Not in our library10.1534/genetics.114.168112

268. 268.

     Turelli M. The causes of Haldane's rule. Science. 1998;282:889-891.

     Not in our library10.1126/science.282.5390.889

269. 269.

     Turissini DA, Matute DR. Fine scale mapping of genomic introgressions within the Drosophila yakuba clade. PLOS Genetics. 2017;13:e1006971.

     Not in our library10.1371/journal.pgen.1006971

270. 270.
     Genomic Islands of Speciation in Anopheles gambiae · 2005

     No notice
271. 271.

     Turner LM, Schwahn DJ, Harr B. Reduced male fertility is common but highly variable in form and severity in a natural house mouse hybrid zone. Evolution. 2012;66:443-458.

     Not in our library10.1111/j.1558-5646.2011.01445.x

272. 272.

     Turner LM, Harr B. Genome-wide mapping in a house mouse hybrid zone reveals hybrid sterility loci and Dobzhansky-Muller interactions. eLife. 2014;3:e02504.

     Not in our library10.7554/elife.02504

273. 273.

     Uecker H, Setter D, Hermisson J. Adaptive gene introgression after secondary contact. Journal of Mathematical Biology. 2015;70:1523-1580.

     Not in our library10.1007/s00285-014-0802-y

274. 274.

     Veller C. Recombination, variance in genetic relatedness, and selection against introgressed DNA. bioRxiv. 2019.

     Not in our library10.1101/846147

275. 275.

     Vernot B, Akey JM. Resurrecting surviving neandertal lineages from modern human genomes. Science. 2014;343:1017-1021.

     Not in our library10.1126/science.1245938

276. 276.

     Vickrey AI, Bruders R, Kronenberg Z, Mackey E, Bohlender RJ, Maclary ET, Maynez R, Osborne EJ, Johnson KP, Huff CD, Yandell M, Shapiro MD. Introgression of regulatory alleles and a missense coding mutation drive plumage pattern diversity in the rock pigeon. eLife. 2018;7:e34803.

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277. 277.
     Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling · 2016

     No notice
278. 278.

     Walter GM, Richards TJ, Wilkinson MJ, Blows MW, Aguirre JD, Ortiz-Barrientos D. Loss of ecologically important genetic variation in late generation hybrids reveals links between adaptation and speciation. Evolution Letters. 2020;4:302-316.

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279. 279.

     Wang RJ, White MA, Payseur BA. The pace of hybrid incompatibility evolution in house mice. Genetics. 2015;201:229-242.

     Not in our library10.1534/genetics.115.179499

280. 280.

     Wang S, Rohwer S, Delmore K, Irwin DE. Cross-decades stability of an avian hybrid zone. Journal of Evolutionary Biology. 2019;32:1242-1251.

     Not in our library10.1111/jeb.13524

281. 281.

     Wellenreuther M, Bernatchez L. Eco-Evolutionary genomics of chromosomal inversions. Trends in Ecology & Evolution. 2018;33:427-440.

     Not in our library10.1016/j.tree.2018.04.002

282. 282.

     Westram AM, Faria R, Johannesson K, Butlin R. Using replicate hybrid zones to understand the genomic basis of adaptive divergence. Molecular Ecology. 2021;30:3797-3814.

     Not in our library10.1111/mec.15861

283. 283.

     Whitney KD, Randell RA, Rieseberg LH. Adaptive introgression of herbivore resistance traits in the weedy sunflower Helianthus annuus. The American Naturalist. 2006;167:794-807.

     Not in our library10.1086/504606

284. 284.

     Wu C-I. The genic view of the process of speciation. Journal of Evolutionary Biology. 2001;14:851-865.

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285. 285.

     Yamaguchi R, Otto SP. Insights from Fisher’s geometric model on the likelihood of speciation under different histories of environmental change. bioRxiv. 2020.

     Not in our library10.1101/596866

286. 286.

     Yanchukov A. Hybridization of Bombina bombina and B. variegata (anura, Discoglossidae) at a sharp ecotone in western Ukraine: comparisons across transects and over time. Evolution. 2006;60:583-600.

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287. 287.

     Yang C-H, Scarpino SV. Reproductive barriers as a byproduct of gene network evolution. bioRxiv. 2020.

     Not in our library10.1101/2020.06.12.147322

288. 288.

     Zeberg H, Pääbo S. The major genetic risk factor for severe COVID-19 is inherited from neanderthals. Nature. 2020;587:610-612.

     Not in our library10.1038/s41586-020-2818-3

289. 289.

     Zhang Z, Bendixsen DP, Janzen T, Nolte AW, Greig D, Stelkens R. Recombining your way out of trouble: the genetic architecture of hybrid fitness under environmental stress. Molecular Biology and Evolution. 2020;37:167-182.

     Not in our library10.1093/molbev/msz211

290. 290.

     Zuellig MP, Sweigart AL. A two‐locus hybrid incompatibility is widespread, polymorphic, and active in natural populations of Mimulus *. Evolution. 2018;72:2394-2405.

     Not in our library10.1111/evo.13596

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