Intrinsic postzygotic isolation typically appears as reduced viability or fertility of interspecific hybrids caused by genetic incompatibilities between diverged parental genomes. Dobzhansky-Muller interactions among individual genes, and chromosomal rearrangements causing problems with chromosome synapsis and recombination in meiosis, have both long been considered as major mechanisms behind intrinsic postzygotic isolation. Recent research has, however, suggested that the genetic basis of intrinsic postzygotic isolation can be more complex and involves, for example, overall divergence of the DNA sequence or epigenetic changes. Here, we review the mechanisms of intrinsic postzygotic isolation from genic, chromosomal, genomic, and epigenetic perspectives across diverse taxa. We provide empirical evidence for these mechanisms, discuss their importance in the speciation process, and highlight questions that remain unanswered.

CNRS UMR 8227 Integrative Biology of Marine Models Sorbonne Université Station Biologique de Roscoff 29680 Roscoff France

Department of Algal Development and Evolution Max Planck Institute for Biology 72076 Tuebingen Germany

Department of Biological Sciences Auburn University Auburn Alabama 36849 USA

Department of Ecology and Evolutionary Biology Yale University New Haven Connecticut 06520 USA

Department of Genomics and Evolutionary Biology National Institute of Genetics Mishima Shizuoka 411 8540 Japan

Department of Zoology Faculty of Science Charles University 128 00 Prague Czech Republic

Department of Zoology Stockholm University 106 91 Stockholm Sweden

DIADE University of Montpellier CIRAD IRD 34090 Montpellier France

Institute for Biodiversity and Ecosystem Dynamics Department of Evolutionary and Population Biology University of Amsterdam 1012 Amsterdam The Netherlands

Organismal and Evolutionary Biology Research Programme University of Helsinki 00100 Helsinki Finland

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Albertin W, Marullo P. 2012. Polyploidy in fungi: evolution after whole-genome duplication. Proc Biol Sci 279: 2497–2509. PubMed PMC

Alix K, Gérard PR, Schwarzacher T, Heslop-Harrison JSP. 2017. Polyploidy and interspecific hybridization: partners for adaptation, speciation and evolution in plants. Ann Bot 120: 183–194. 10.1093/aob/mcx079 PubMed DOI PMC

Arévalo L, Gardner S, Campbell P. 2021. Haldane's rule in the placenta: sex-biased misregulation of the Kcnq1 imprinting cluster in hybrid mice. Evolution (N Y) 75: 86–100. 10.1111/evo.14132 PubMed DOI

Ashe A, Colot V, Oldroyd BP. 2021. How does epigenetics influence the course of evolution? Philos Trans R Soc Lond B Biol Sci 376: 20200111. 10.1098/rstb.2020.0111 PubMed DOI PMC

Baker Z, Schumer M, Haba Y, Bashkirova L, Holland C, Rosenthal GG, Przeworski M. 2017. Repeated losses of PRDM9-directed recombination despite the conservation of PRDM9 across vertebrates. eLife 6: 24133. 10.7554/eLife.24133 PubMed DOI PMC

Bank C, Bürger R, Hermisson J. 2012. The limits to parapatric speciation: Dobzhansky–Muller incompatibilities in a continent-island model. Genetics 191: 845–863. 10.1534/genetics.111.137513 PubMed DOI PMC

Barley AJ, Nieto-Montes de Oca A, Manríquez-Morán NL, Thomson RC. 2022. The evolutionary network of whiptail lizards reveals predictable outcomes of hybridization. Science 377: 773–777. 10.1126/science.abn1593 PubMed DOI

Barragan AC, Collenberg M, Wang J, Lee RRQ, Cher WY, Rabanal FA, Ashkenazy H, Weigel D, Chae E. 2021. A truncated singleton NLR causes hybrid necrosis in Arabidopsis thaliana. Mol Biol Evol 38: 557–574. 10.1093/molbev/msaa245 PubMed DOI PMC

Bateson W. 1909. Heredity and variation in modern lights. In Darwin and modern science (ed. Seward AC), pp. 85–101. Cambridge University Press, Cambridge. https://ci.nii.ac.jp/naid/10018121532

Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C, Przeworski M, Coop G, de Massy B. 2010. PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327: 836–840. 10.1126/science.1183439 PubMed DOI PMC

Berdan EL, Aubier TG, Cozzolino S, Faria R, Feder JL, Giménez MD, Joron M, Searle JB, Mérot C. 2023. Structural variants and speciation: multiple processes at play. Cold Spring Harb Perspect Biol 10.1101/cshperspect.a041446 PubMed DOI PMC

Betrán E, Thornton K, Long M. 2002. Retroposed new genes out of the X in Drosophila. Genome Res 12: 1854–1859. 10.1101/gr.604902 PubMed DOI PMC

Bhattacharyya T, Gregorova S, Mihola O, Anger M, Sebestova J, Denny P, Simecek P, Forejt J. 2013. Mechanistic basis of infertility of mouse intersubspecific hybrids. Proc Natl Acad Sci 110: E468–E477. 10.1073/pnas.1219126110 PubMed DOI PMC

Bikard D, Patel D, Le Metté C, Giorgi V, Camilleri C, Bennett MJ, Loudet O. 2009. Divergent evolution of duplicate genes leads to genetic incompatibilities within A. thaliana. Science 323: 623–626. 10.1126/science.1165917 PubMed DOI

Bomblies K, Weigel D. 2007. Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat Rev Genet 8: 382–393. 10.1038/nrg2082 PubMed DOI

Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C, Dangl JL, Weigel D. 2007. Autoimmune response as a mechanism for a Dobzhansky–Muller-type incompatibility syndrome in plants. PLoS Biol 5: e236. 10.1371/journal.pbio.0050236 PubMed DOI PMC

Bozdag GO, Ono J. 2022. Evolution and molecular bases of reproductive isolation. Curr Opin Genet Dev 76: 101952. 10.1016/j.gde.2022.101952 PubMed DOI PMC

Bozdag GO, Ono J, Denton JA, Karakoc E, Hunter N, Leu JY, Greig D. 2021. Breaking a species barrier by enabling hybrid recombination. Curr Biol 31: R180–R181. 10.1016/j.cub.2020.12.038 PubMed DOI

Brekke TD, Good JM. 2014. Parent-of-origin growth effects and the evolution of hybrid inviability in dwarf hamsters. Evolution (N Y) 68: 3134–3148. 10.1111/evo.12500 PubMed DOI PMC

Brown JD, O'Neill RJ. 2010. Chromosomes, conflict, and epigenetics: chromosomal speciation revisited. Annu Rev Genomics Hum Genet 11: 291–316. 10.1146/annurev-genom-082509-141554 PubMed DOI

Burt A, Trivers R. 2006. Genes in conflict: the biology of selfish genetic elements. Harvard University Press, Cambridge, MA.

Butlin RK. 2005. Recombination and speciation. Mol Ecol 14: 2621–2635. 10.1111/j.1365-294X.2005.02617.x PubMed DOI

Campbell P, Good JM, Nachman MW. 2013. Meiotic sex chromosome inactivation is disrupted in sterile hybrid male house mice. Genetics 193: 819–828. 10.1534/genetics.112.148635 PubMed DOI PMC

Castillo DM, Moyle LC. 2022. Hybrid incompatibility between Drosophila virilis and D. lummei is stronger in the presence of transposable elements. J Evol Biol 35: 1319–1334. 10.1111/jeb.14079 PubMed DOI PMC

Charlesworth B. 1992. Evolutionary rates in partially self-fertilizing species. Am Nat 140: 126–148. 10.1086/285406 PubMed DOI

Charlesworth B, Coyne JA, Barton NH. 1987. The relative rates of evolution of sex chromosomes and autosomes. Am Nat 130: 113–146. 10.1086/284701 DOI

Chen C, Chen H, Lin YS, Shen JB, Shan JX, Qi P, Shi M, Zhu MZ, Huang XH, Feng Q, et al. 2014. A two-locus interaction causes interspecific hybrid weakness in rice. Nat Commun 5: 3357. 10.1038/ncomms4357 PubMed DOI PMC

Chou JY, Leu JY. 2010. Speciation through cytonuclear incompatibility: insights from yeast and implications for higher eukaryotes. Bioessays 32: 401–411. 10.1002/bies.200900162 PubMed DOI

Comai L, Madlung A, Josefsson C, Tyagi A. 2003. Do the different parental “heteromes” cause genomic shock in newly formed allopolyploids? Philos Trans R Soc Lond B Biol Sci 358: 1149–1155. 10.1098/rstb.2003.1305 PubMed DOI PMC

Coughlan JM. 2023. The role of hybrid seed inviability in angiosperm speciation. Am J Bot 111: e16135. 10.1002/ajb2.16135 PubMed DOI

Coughlan JM, Matute DR. 2020. The importance of intrinsic postzygotic barriers throughout the speciation process. Philos Trans R Soc Lond B Biol Sci 375: 20190533. 10.1098/rstb.2019.0533 PubMed DOI PMC

Coughlan JM, Wilson Brown M, Willis JH. 2020. Patterns of hybrid seed inviability in the Mimulus guttatus sp. complex reveal a potential role of parental conflict in reproductive isolation. Curr Biol 30: 83–93.e5. 10.1016/j.cub.2019.11.023 PubMed DOI PMC

Cowell F. 2023. 100 years of Haldane's rule. J Evol Biol 36: 337–346. 10.1111/jeb.14112 PubMed DOI PMC

Coyne JA, Orr HA. 1989a. Patterns of speciation in Drosophila. Evolution (N Y) 43: 362. 10.2307/2409213 PubMed DOI

Coyne JA, Orr HA. 1989b. Two rules of speciation. In Speciation and its consequences (ed. Otte D, Endler J), pp. 180–207. Sinauer, Sunderland, MA.

Coyne JA, Orr HA. 1997. “Patterns of speciation in Drosophila” revisited. Evolution (N Y) 51: 295–303. 10.2307/2411143 PubMed DOI

Coyne JA, Orr HA. 2004. Speciation. Sinauer, Sunderland, MA.

Crespi B, Nosil P. 2013. Conflictual speciation: species formation via genomic conflict. Trends Ecol Evol 28: 48–57. 10.1016/j.tree.2012.08.015 PubMed DOI

Darwin C. 1859. On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. John Murray, London, UK. PubMed PMC

Dedukh D, Majtánová Z, Marta A, Pšenička M, Kotusz J, Klíma J, Juchno D, Boron A, Janko K. 2020. Parthenogenesis as a solution to hybrid sterility: the mechanistic basis of meiotic distortions in clonal and sterile hybrids. Genetics 215: 975–987. 10.1534/genetics.119.302988 PubMed DOI PMC

Dion-Côté AM, Barbash DA. 2017. Beyond speciation genes: an overview of genome stability in evolution and speciation. Curr Opin Genet Dev 47: 17–23. 10.1016/j.gde.2017.07.014 PubMed DOI PMC

Dion-Côté AM, Renaut S, Normandeau E, Bernatchez L. 2014. RNA-seq reveals transcriptomic shock involving transposable elements reactivation in hybrids of young lake whitefish species. Mol Biol Evol 31: 1188–1199. 10.1093/molbev/msu069 PubMed DOI

Diop A, Torrance EL, Stott CM, Bobay L-M. 2022. Gene flow and introgression are pervasive forces shaping the evolution of bacterial species. Genome Biol 23: 239. 10.1186/s13059-022-02809-5 PubMed DOI PMC

Dobzhansky T. 1936. Studies on hybrid sterility. II: Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 21: 113–135. 10.1093/genetics/21.2.113 PubMed DOI PMC

Dobzhansky T. 1937. Genetics and the origin of species. Columbia University Press, New York.

Dziasek K, Simon L, Lafon-Placette C, Laenen B, Wärdig C, Santos-González J, Slotte T, Köhler C. 2021. Hybrid seed incompatibility in Capsella is connected to chromatin condensation defects in the endosperm. PLoS Genet 17: e1009370. 10.1371/journal.pgen.1009370 PubMed DOI PMC

Dzur Gejdosova M, Simecek P, Gregorova S, Bhattacharyya T, Forejt J. 2012. Dissecting the genetic architecture of F1 hybrid sterility in house mice. Evolution (N Y) 66: 3321–3335. 10.1111/j.1558-5646.2012.01684.x PubMed DOI

Emerson JJ, Kaessmann H, Betrán E, Long M. 2004. Extensive gene traffic on the mammalian X chromosome. Science 303: 537–540. 10.1126/science.1090042 PubMed DOI

Feder JL, Nosil P. 2009. Chromosomal inversions and species differences: when are genes affecting adaptive divergence and reproductive isolation expected to reside within inversions? Evolution (N Y) 63: 3061–3075. 10.1111/j.1558-5646.2009.00786.x PubMed DOI

Ferree PM, Barbash DA. 2009. Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila. PLoS Biol 7: e1000234. 10.1371/journal.pbio.1000234 PubMed DOI PMC

Fierst JL, Hansen TF. 2010. Genetic architecture and postzygotic reproductive isolation: evolution of Bateson-Dobzhansky-Muller incompatibilities in a polygenic model. Evolution 64: 675–693. 10.1111/j.1558-5646.2009.00861.x PubMed DOI

Fishman L, Sweigart AL. 2018. When two rights make a wrong: the evolutionary genetics of plant hybrid incompatibilities. Annu Rev Plant Biol 69: 707–731. 10.1146/annurev-arplant-042817-040113 PubMed DOI

Fishman L, Stathos A, Beardsley PM, Williams CF, Hill JP. 2013. Chromosomal rearrangements and the genetics of reproductive barriers in mimulus (monkey flowers). Evolution (N Y) 67: 2547–2560. 10.1111/evo.12154 PubMed DOI

Florez-Rueda AM, Fiscalini F, Roth M, Grossniklaus U, Städler T. 2021. Endosperm and seed transcriptomes reveal possible roles for small RNA pathways in wild tomato hybrid seed failure. Genome Biol Evol 13: evab107. 10.1093/gbe/evab107 PubMed DOI PMC

Forejt J. 1996. Hybrid sterility in the mouse. Trends Genet 12: 412–417. 10.1016/0168-9525(96)10040-8 PubMed DOI

Forejt J, Jansa P. 2023. Meiotic recognition of evolutionarily diverged homologs: chromosomal hybrid sterility revisited. Mol Biol Evol 40: msad083. 10.1093/molbev/msad083 PubMed DOI PMC

Forejt J, Jansa P, Parvanov E. 2021. Hybrid sterility genes in mice (Mus musculus): a peculiar case of PRDM9 incompatibility. Trends Genet 37: 1095–1108. 10.1016/j.tig.2021.06.008 PubMed DOI

Frank SA. 1991. Divergence of meiotic drive-suppression systems as an explanation for sex-biased hybrid sterility and inviability. Evolution (N Y) 45: 262–267. PubMed

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. 10.1371/journal.pgen.1007526 PubMed DOI PMC

Fuller ZL, Koury SA, Phadnis N, Schaeffer SW. 2019. How chromosomal rearrangements shape adaptation and speciation: case studies in Drosophila pseudoobscura and its sibling species Drosophila persimilis. Mol Ecol 28: 1283–1301. 10.1111/mec.14923 PubMed DOI PMC

Gao D, Jiang N, Wing RA, Jiang J, Jackson SA. 2015. Transposons play an important role in the evolution and diversification of centromeres among closely related species. Front Plant Sci 6: 216. PubMed PMC

Gavrilets S. 2004. Fitness landscapes and the origin of species. Princeton University Press, Princeton, NJ.

Geist KS, Strassmann JE, Queller DC. 2019. Family quarrels in seeds and rapid adaptive evolution in Arabidopsis. Proc Natl Acad Sci 116: 9463–9468. 10.1073/pnas.1817733116 PubMed DOI PMC

Good JM, Giger T, Dean MD, Nachman MW. 2010. Widespread over-expression of the X chromosome in sterile F1 hybrid mice. PLoS Genet 6: e1001148. 10.1371/journal.pgen.1001148 PubMed DOI PMC

Grant V. 1981. Plant speciation. Columbia University Press, New York.

Gregorova S, Gergelits V, Chvatalova I, Bhattacharyya T, Valiskova B, Fotopulosova V, Jansa P, Wiatrowska D, Forejt J. 2018. Modulation of Prdm9-controlled meiotic chromosome asynapsis overrides hybrid sterility in mice. eLife 7: e34282. 10.7554/eLife.34282 PubMed DOI PMC

Gutierrez-Marcos JF, Pennington PD, Costa LM, Dickinson HG. 2003. Imprinting in the endosperm: a possible role in preventing wide hybridization. Philos Trans R Soc Lond B Biol Sci 358: 1105–1111. 10.1098/rstb.2003.1292 PubMed DOI PMC

Haig D, Grafen A. 1991. Genetic scrambling as a defence against meiotic drive. J Theor Biol 153: 531–558. 10.1016/S0022-5193(05)80155-9 PubMed DOI

Haldane JBS. 1922. Sex ratio and unisexual sterility in hybrid animals. J Genet 12: 101–109. 10.1007/BF02983075 DOI

Hartl DL. 1974. Genetic dissection of segregation distortion. I: Suicide combinations of SD genes. Genetics 76: 477–486. 10.1093/genetics/76.3.477 PubMed DOI PMC

Harumoto T, Fukatsu T. 2022. Perplexing dynamics of Wolbachia proteins for cytoplasmic incompatibility. PLoS Biol 20: e3001644. 10.1371/journal.pbio.3001644 PubMed DOI PMC

Hedrick PW. 1981. The establishment of chromosomal variants. Evolution (N Y) 35: 322–332. 10.2307/2407841 PubMed DOI

Henikoff S, Ahmad K, Malik HS. 2001. The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293: 1098–1102. 10.1126/science.1062939 PubMed DOI

Hill WG, Robertson A. 1966. The effect of linkage on limits to artificial selection. Genet Res 8: 269–294. 10.1017/S0016672300010156 PubMed DOI

Homolka D, Ivanek R, Capkova J, Jansa P, Forejt J. 2007. Chromosomal rearrangement interferes with meiotic X chromosome inactivation. Genome Res 17: 1431–1437. 10.1101/gr.6520107 PubMed DOI PMC

Horard B, Terretaz K, Gosselin-Grenet AS, Sobry H, Sicard M, Landmann F, Loppin B. 2022. Paternal transmission of the Wolbachia CidB toxin underlies cytoplasmic incompatibility. Curr Biol 32: 1319–1331.e5. 10.1016/j.cub.2022.01.052 PubMed DOI

Hufford MB, Seetharam AS, Woodhouse MR, Chougule KM, Ou S, Liu J, Ricci WA, Guo T, Olson A, Qiu Y, et al. 2021. De novo assembly, annotation, and comparative analysis of 26 diverse maize genomes. Science 373: 655–662. 10.1126/science.abg5289 PubMed DOI PMC

Hurst LD, Pomiankowski A. 1991. Causes of sex ratio bias may account for unisexual sterility in hybrids: a new explanation of Haldane's rule and related phenomena. Genetics 128: 841–858. 10.1093/genetics/128.4.841 PubMed DOI PMC

İltaş Ö, Svitok M, Cornille A, Schmickl R, Lafon Placette C. 2021. Early evolution of reproductive isolation: a case of weak inbreeder/strong outbreeder leads to an intraspecific hybridization barrier in Arabidopsis lyrata. Evolution (N Y) 75: 1466–1476. 10.1111/evo.14240 PubMed DOI

Jagannathan M, Yamashita YM. 2021. Defective satellite DNA clustering into chromocenters underlies hybrid incompatibility in Drosophila. Mol Biol Evol 38: 4977–4986. 10.1093/molbev/msab221 PubMed DOI PMC

Janko K, Pačes J, Wilkinson-Herbots H, Costa RJ, Roslein J, Drozd P, Iakovenko N, Rídl J, Hroudová M, Koí J, et al. 2018. Hybrid asexuality as a primary postzygotic barrier between nascent species: on the interconnection between asexuality, hybridization and speciation. Mol Ecol 27: 248–263. 10.1111/mec.14377 PubMed DOI PMC

Janoušek V, Fischerová J, Mořkovský L, Reif J, Antczak M, Albrecht T, Reifová R. 2019. Postcopulatory sexual selection reduces Z-linked genetic variation and might contribute to the large Z effect in passerine birds. Heredity (Edinb) 122: 622–635. 10.1038/s41437-018-0161-3 PubMed DOI PMC

Jhuang HY, Lee HY, Leu JY. 2017. Mitochondrial-nuclear co-evolution leads to hybrid incompatibility through pentatricopeptide repeat proteins. EMBO Rep 18: 87–101. 10.15252/embr.201643311 PubMed DOI PMC

Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS, et al. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97–100. 10.1038/nature09916 PubMed DOI

Jiao WB, Patel V, Klasen J, Liu F, Pecinkova P, Ferrand M, Gy I, Camilleri C, Effgen S, Koornneef M, et al. 2021. The evolutionary dynamics of genetic incompatibilities introduced by duplicated genes in Arabidopsis thaliana. Mol Biol Evol 38: 1225–1240. 10.1093/molbev/msaa306 PubMed DOI PMC

Johnson NA. 2000. Speciation: Dobzhansky-Muller incompatibilities, dominance and gene interactions. Trends Ecol Evol 15: 480–482. 10.1016/S0169-5347(00)01961-3 PubMed DOI

Josefsson C, Dilkes B, Comai L. 2006. Parent-dependent loss of gene silencing during interspecies hybridization. Curr Biol 16: 1322–1328. 10.1016/j.cub.2006.05.045 PubMed DOI

Kao KC, Schwartz K, Sherlock G. 2010. A genome-wide analysis reveals no nuclear Dobzhansky–Muller pairs of determinants of speciation between S. cerevisiae and S. paradoxus, but suggests more complex incompatibilities. PLoS Genet 6: e1001038. 10.1371/journal.pgen.1001038 PubMed DOI PMC

Kaur R, Leigh BA, Ritchie IT, Bordenstein SR. 2022. The Cif proteins from Wolbachia prophage WO modify sperm genome integrity to establish cytoplasmic incompatibility. PLoS Biol 20: e3001584. 10.1371/journal.pbio.3001584 PubMed DOI PMC

Kidwell MG, Novy JB. 1979. Hybrid dysgenesis in Drosophila melanogaster: sterility resulting from gonadal dysgenesis in the P-M system. Genetics 92: 1127–1140. 10.1093/genetics/92.4.1127 PubMed DOI PMC

Kidwell MG, Kidwell JF, Sved JA. 1977. Hybrid dysgenesis in Drosophila melanogaster: a syndrome of aberrant traits including mutation, sterility and male recombination. Genetics 86: 813–833. 10.1093/genetics/86.4.813 PubMed DOI PMC

Kimura K, Kidwell MG. 1994. Differences in P element population dynamics between the sibling species Drosophila melanogaster and Drosophila simulans. Genet Res 63: 27–38. 10.1017/S0016672300032055 PubMed DOI

King M. 1993. Species evolution: the role of chromosome change. Cambridge University Press, New York.

Kocher SD, Tsuruda JM, Gibson JD, Emore CM, Arechavaleta-Velasco ME, Queller DC, Strassmann JE, Grozinger CM, Gribskov MR, San Miguel P, et al. 2015. A search for parent-of-origin effects on honey bee gene expression. G3 (Bethesda) 5: 1657–1662. 10.1534/g3.115.017814 PubMed DOI PMC

Kropáčková L, Piálek J, Gergelits V, Forejt J, Reifová R. 2015. Maternal-foetal genomic conflict and speciation: no evidence for hybrid placental dysplasia in crosses between two house mouse subspecies. J Evol Biol 28: 688–698. 10.1111/jeb.12602 PubMed DOI

Kulmuni J, Westram AM. 2017. Intrinsic incompatibilities evolving as a by-product of divergent ecological selection: considering them in empirical studies on divergence with gene flow. Mol Ecol 26: 3093–3103. 10.1111/mec.14147 PubMed DOI

Kursel LE, Malik HS. 2018. The cellular mechanisms and consequences of centromere drive. Curr Opin Cell Biol 52: 58–65. 10.1016/j.ceb.2018.01.011 PubMed DOI PMC

Lafon-Placette C, Johannessen IM, Hornslien KS, Ali MF, Bjerkan KN, Bramsiepe J, Glöckle BM, Rebernig CA, Brysting AK, Grini PE, et al. 2017. Endosperm-based hybridization barriers explain the pattern of gene flow between Arabidopsis lyrata and Arabidopsis arenosa in Central Europe. Proc Natl Acad Sci 114: E1027–E1035. 10.1073/pnas.1615123114 PubMed DOI PMC

Lafon-Placette C, Hatorangan MR, Steige KA, Cornille A, Lascoux M, Slotte T, Köhler C. 2018. Paternally expressed imprinted genes associate with hybridization barriers in Capsella. Nat Plants 4: 352–357. 10.1038/s41477-018-0161-6 PubMed DOI

Lande R. 1979. Effective deme sizes during long-term evolution estimated from rates of chromosomal rearrangement. Evolution (N Y) 33: 234–251. 10.2307/2407380 PubMed DOI

Laporte M, Le Luyer J, Rougeux C, Dion-Côté A-M, Krick M, Bernatchez L. 2019. DNA methylation reprogramming, TE derepression, and postzygotic isolation of nascent animal species. Sci Adv 5: eaaw1644. 10.1126/sciadv.aaw1644 PubMed DOI PMC

Larson EL, Kopania EEK, Hunnicutt KE, Vanderpool D, Keeble S, Good JM. 2022. Stage-specific disruption of X chromosome expression during spermatogenesis in sterile house mouse hybrids. G3 (Bethesda) 12: jkab407. 10.1093/g3journal/jkab407 PubMed DOI PMC

Laurent S, Salamin N, Robinson-Rechavi M. 2017. No evidence for the radiation time lag model after whole genome duplications in Teleostei. PLoS ONE 12: e0176384. 10.1371/journal.pone.0176384 PubMed DOI PMC

Long Y, Zhao L, Niu B, Su J, Wu H, Chen Y, Zhang Q, Guo J, Zhuang C, Mei M, et al. 2008. Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes. Proc Natl Acad Sci 105: 18871–18876. 10.1073/pnas.0810108105 PubMed DOI PMC

Lu Y, Sandoval A, Voss S, Lai Z, Kneitz S, Boswell W, Boswell M, Savage M, Walter C, Warren W, et al. 2020. Oncogenic allelic interaction in Xiphophorus highlights hybrid incompatibility. Proc Natl Acad Sci 117: 29786–29794. 10.1073/pnas.2010133117 PubMed DOI PMC

Lucek K, Giménez MD, Joron M, Rafajlović M, Searle JB, Walden N, Westram AM, Faria R. 2023. The impact of chromosomal rearrangements in speciation: from micro- to macroevolution. Cold Spring Harb Perspect Biol 10.1101/cshperspect.a041447 PubMed DOI PMC

Luo J, Sun X, Cormack BP, Boeke JD. 2018. Karyotype engineering by chromosome fusion leads to reproductive isolation in yeast. Nature 560: 392–396. 10.1038/s41586-018-0374-x PubMed DOI PMC

Lynch M. 2007. The origins of genome architecture. Sinauer, Sunderland, MA.

Lynch M, Force AG. 2000. The origin of interspecific genomic incompatibility via gene duplication. Am Nat 156: 590–605. 10.1086/316992 PubMed DOI

Mable BK, Alexandrou MA, Taylor MI. 2011. Genome duplication in amphibians and fish: an extended synthesis. J Zool 284: 151–182. 10.1111/j.1469-7998.2011.00829.x DOI

Maheshwari S, Barbash DA. 2011. The genetics of hybrid incompatibilities. Anuu Rev Genet 45: 331–355. 10.1146/annurev-genet-110410-132514 PubMed DOI

Mank JE, Vicoso B, Berlin S, Charlesworth B. 2010. Effective population size and the faster-X effect: empirical results and their interpretation. Evolution (N Y) 64: 663–674. 10.1111/j.1558-5646.2009.00853.x PubMed DOI

Mao Y, Gabel A, Nakel T, Viehöver P, Baum T, Tekleyohans DG, Vo D, Grosse I, Groß-Hardt R. 2020. Selective egg cell polyspermy bypasses the triploid block. eLife 9: e52976. 10.7554/eLife.52976 PubMed DOI PMC

Marks GE. 1966. The origin and significance of intraspecific polyploidy: experimental evidence from solanum chacoense. Evolution (N Y) 20: 552–557. 10.2307/2406589 PubMed DOI

Masly JP, Presgraves DC. 2007. High-resolution genome-wide dissection of the two rules of speciation in Drosophila. PLoS Biol 5: e243. 10.1371/journal.pbio.0050243 PubMed DOI PMC

Masly JP, Jones CD, Noor MAF, Locke J, Orr HA. 2006. Gene transposition as a cause of hybrid sterility in Drosophila. Science 313: 1448–1450. 10.1126/science.1128721 PubMed DOI

McClintock B. 1984. The significance of responses of the genome to challenge. Science 226: 792–801. 10.1126/science.15739260 PubMed DOI

McQuillan MA, Roth TC II, Huynh AV, Rice AM. 2018. Hybrid chickadees are deficient in learning and memory. Evolution (N Y) 72: 1155–1164. 10.1111/evo.13470 PubMed DOI

Meierjohann S, Schartl M. 2006. From Mendelian to molecular genetics: the Xiphophorus melanoma model. Trends Genet 22: 654–661. 10.1016/j.tig.2006.09.013 PubMed DOI

Michalak P. 2009. Epigenetic, transposon and small RNA determinants of hybrid dysfunctions. Heredity (Edinb) 102: 45–50. 10.1038/hdy.2008.48 PubMed DOI

Mizuta Y, Harushima Y, Kurata N. 2010. Rice pollen hybrid incompatibility caused by reciprocal gene loss of duplicated genes. Proc Natl Acad Sci 107: 20417–20422. 10.1073/pnas.1003124107 PubMed DOI PMC

Moore T, Haig D. 1991. Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet 7: 45–49. 10.1016/0168-9525(91)90040-W PubMed DOI

Moran BM, Payne C, Langdon Q, Powell DL, Brandvain Y, Schumer M. 2021. The genomic consequences of hybridization. eLife 10: e69016. 10.7554/eLife.69016 PubMed DOI PMC

Moyle LC, Muir CD, Han MV, Hahn MW. 2010. The contribution of gene movement to the “two rules of speciation.” Evolution (N Y) 64: 1541–1557. 10.1111/j.1558-5646.2010.00990.x PubMed DOI

Muir CD, Hahn MW. 2015. The limited contribution of reciprocal gene loss to increased speciation rates following whole-genome duplication. Am Nat 185: 70–86. 10.1086/679108 PubMed DOI

Muller HJ. 1942. Isolating mechanisms, evolution, and temperature. Biol Symp 6: 71–125.

Muller HJ. 1964. The relation of recombination to mutational advance. Mutat Res 106: 2–9. 10.1016/0027-5107(64)90047-8 PubMed DOI

Müller DG. 1979. Genetic affinity of Ectocarpus siliculosus (Dillw.) Lyngb. from the Mediterranean, North Atlantic and Australia. Phycologia 18: 312–318. 10.2216/i0031-8884-18-4-312.1 DOI

Muller DG, Eichenberger W. 1995. Crossing experiments, lipid composition, and the species concept in Ectocarpus siliculosus and E. Fasciculatus (Phaeophyceae, Ectocarpales). J Phycol 31: 173–176. 10.1111/j.0022-3646.1995.00173.x DOI

Navarro A, Barton NH. 2003. Accumulating postzygotic isolation genes in parapatry: a new twist on chromosomal speciation. Evolution (N Y) 57: 447–459. PubMed

Nei M. 1976. Mathematical models of speciation and genetic distance. In Population genetics and ecology (ed. Karlin S, Nevo E), pp. 723–765. Academic, New York.

Nguyen GN, Yamagata Y, Shigematsu Y, Watanabe M, Miyazaki Y, Doi K, Tashiro K, Kuhara S, Kanamori H, Wu J, et al. 2017. Duplication and loss of function of genes encoding RNA polymerase III subunit C4 causes hybrid incompatibility in rice. G3 (Bethesda) 7: 2565–2575. 10.1534/g3.117.043943 PubMed DOI PMC

Noor MAF. 1997. Genetics of sexual isolation and courtship dysfunction in male hybrids of Drosophila pseudoobscura and Drosophila persimilis. Evolution (N Y) 51: 809–815. 10.2307/2411156 PubMed DOI

Noor MA, Grams KL, Bertucci LA, Reiland J. 2001. Chromosomal inversions and the reproductive isolation of species. Proc Natl Acad Sci 98: 12084–12088. 10.1073/pnas.221274498 PubMed DOI PMC

Nosil P. 2012. Ecological speciation. Oxford University Press, Oxford.

Oneal E, Willis JH, Franks RG. 2016. Disruption of endosperm development is a major cause of hybrid seed inviability between Mimulus guttatus and Mimulus nudatus. New Phytol 210: 1107–1120. 10.1111/nph.13842 PubMed DOI PMC

O'Neill RJ, O'Neill MJ, Graves JA. 1998. Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature 393: 68–72. 10.1038/29985 PubMed DOI

Otto SP, Whitton J. 2000. Polyploid incidence and evolution. Annu Rev Genet 34: 401–437. 10.1146/annurev.genet.34.1.401 PubMed DOI

Patten MM. 2018. Selfish X chromosomes and speciation. Mol Ecol 27: 3772–3782. 10.1111/mec.14471 PubMed DOI

Pires ND, Grossniklaus U. 2014. Different yet similar: evolution of imprinting in flowering plants and mammals. F1000Prime Rep 6: 63. 10.12703/P6-63 PubMed DOI PMC

Poignet M, Johnson Pokorná M, Altmanová M, Majtánová Z, Dedukh D, Albrecht T, Reif J, Osiejuk TS, Reifová R. 2021. Comparison of karyotypes in two hybridizing passerine species: conserved chromosomal structure but divergence in centromeric repeats. Front Genet 12: 768987. 10.3389/fgene.2021.768987 PubMed DOI PMC

Postel Z, Touzet P. 2020. Cytonuclear genetic incompatibilities in plant speciation. Plants 9: 487. 10.3390/plants9040487 PubMed DOI PMC

Powell DL, García-Olazábal M, Keegan M, Reilly P, Du K, Díaz-Loyo AP, Banerjee S, Blakkan D, Reich D, Andolfatto P, et al. 2020. Natural hybridization reveals incompatible alleles that cause melanoma in swordtail fish. Science 368: 731–736. 10.1126/science.aba5216 PubMed DOI PMC

Presgraves DC. 2008. Sex chromosomes and speciation in Drosophila. Trends Genet 24: 336–343. 10.1016/j.tig.2008.04.007 PubMed DOI PMC

Presgraves D. 2009. Drive and sperm: the evolution and genetics of male meiotic drive. In Sperm biology (ed. Birkhead TR, Hosken DJ, Pitnick S), pp. 471–506. Academic, London.

Presgraves DC. 2010. The molecular evolutionary basis of species formation. Nat Rev Genet 11: 175–180. 10.1038/nrg2718 PubMed DOI

Rebernig CA, Lafon-Placette C, Hatorangan MR, Slotte T, Köhler C. 2015. Non-reciprocal interspecies hybridization barriers in the Capsella genus are established in the endosperm. PLoS Genet 11: e1005295. 10.1371/journal.pgen.1005295 PubMed DOI PMC

Rieseberg LH. 2001. Chromosomal rearrangements and speciation. Trends Ecol Evol 16: 351–358. 10.1016/S0169-5347(01)02187-5 PubMed DOI

Rieseberg LH, Blackman BK. 2010. Speciation genes in plants. Ann Bot 106: 439–455. 10.1093/aob/mcq126 PubMed DOI PMC

Rogers DW, McConnell E, Ono J, Greig D. 2018. Spore-autonomous fluorescent protein expression identifies meiotic chromosome mis-segregation as the principal cause of hybrid sterility in yeast. PLoS Biol 16: e2005066. 10.1371/journal.pbio.2005066 PubMed DOI PMC

Rošić S, Köhler F, Erhardt S. 2014. Repetitive centromeric satellite RNA is essential for kinetochore formation and cell division. J Cell Biol 207: 335–349. 10.1083/jcb.201404097 PubMed DOI PMC

Roth M, Florez-Rueda AM, Griesser S, Paris M, Städler T. 2018. Incidence and developmental timing of endosperm failure in post-zygotic isolation between wild tomato lineages. Ann Bot 121: 107–118. 10.1093/aob/mcx133 PubMed DOI PMC

Roth M, Florez-Rueda AM, Städler T. 2019. Differences in effective ploidy drive genome-wide endosperm expression polarization and seed failure in wild tomato hybrids. Genetics 212: 141–152. 10.1534/genetics.119.302056 PubMed DOI PMC

Sandstedt GD, Sweigart AL. 2022. Developmental evidence for parental conflict in driving Mimulus species barriers. New Phytol 236: 1545–1557. 10.1111/nph.18438 PubMed DOI PMC

Sandstedt GD, Wu CA, Sweigart AL. 2021. Evolution of multiple postzygotic barriers between species of the Mimulus tilingii complex. Evolution (N Y) 75: 600–613. 10.1111/evo.14105 PubMed DOI PMC

Santini F, Harmon LJ, Carnevale G, Alfaro ME. 2009. Did genome duplication drive the origin of teleosts? A comparative study of diversification in ray-finned fishes. BMC Evol Biol 9: 194. 10.1186/1471-2148-9-194 PubMed DOI PMC

Satokangas I, Martin SH, Helanterä H, Saramäki J, Kulmuni J. 2020. Multi-locus interactions and the build-up of reproductive isolation. Philos Trans R Soc Lond B Biol Sci 375: 20190543. 10.1098/rstb.2019.0543 PubMed DOI PMC

Sawamura K. 2012. Chromatin evolution and molecular drive in speciation. Int J Evol Biol 2012: 301894. PubMed PMC

Scannell DR, Byrne KP, Gordon JL, Wong S, Wolfe KH. 2006. Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts. Nature 440: 341–345. 10.1038/nature04562 PubMed DOI

Schluter D. 2000. The ecology of adaptive radiation. Oxford University Press, Oxford.

Schluter D, Rieseberg LH. 2022. Three problems in the genetics of speciation by selection. Proc Natl Acad Sci 119: e2122153119. 10.1073/pnas.2122153119 PubMed DOI PMC

Schumer M, Xu C, Powell DL, Durvasula A, Skov L, Holland C, Blazier JC, Sankararaman S, Andolfatto P, Rosenthal GG, et al. 2018. Natural selection interacts with recombination to shape the evolution of hybrid genomes. Science 360: 656–660. 10.1126/science.aar3684 PubMed DOI PMC

Seehausen O, Butlin RK, Keller I, Wagner CE, Boughman JW, Hohenlohe PA, Peichel CL, Saetre GP, Bank C, Brännström A, et al. 2014. Genomics and the origin of species. Nat Rev Genet 15: 176–192. 10.1038/nrg3644 PubMed DOI

Serrato-Capuchina A, D'Agostino ERR, Peede D, Roy B, Isbell K, Wang J, Matute DR. 2021. P-elements strengthen reproductive isolation within the Drosophila simulans species complex. Evolution (N Y) 75: 2425–2440. 10.1111/evo.14319 PubMed DOI PMC

Shropshire JD, Leigh B, Bordenstein SR. 2020. Symbiont-mediated cytoplasmic incompatibility: what have we learned in 50 years? eLife 9: e61989. 10.7554/eLife.61989 PubMed DOI PMC

Slotte T, Huang H, Lascoux M, Ceplitis A. 2008. Polyploid speciation did not confer instant reproductive isolation in Capsella (Brassicaceae). Mol Biol Evol 25: 1472–1481. 10.1093/molbev/msn092 PubMed DOI

Stache B. 1990. Sexual compatability and species concept in Ectocarpus siliculosus (Ectocarpales, Phaeophyceae) from Italy, North Carolina, Chile, and New Zealand. In Evolutionary biogeography of the marine algae of the North Atlantic, pp. 173–186. Springer, Berlin.

Städler T, Florez-Rueda AM, Roth M. 2021. A revival of effective ploidy: the asymmetry of parental roles in endosperm-based hybridization barriers. Curr Opin Plant Biol 61: 102015. 10.1016/j.pbi.2021.102015 PubMed DOI

Stathos A, Fishman L. 2014. Chromosomal rearrangements directly cause underdominant F1 pollen sterility in Mimulus lewisii–Mimulus cardinalis hybrids. Evolution (N Y) 68: 3109–3119. 10.1111/evo.12503 PubMed DOI

Stöck M, Dedukh D, Reifová R, Lamatsch DK, Starostová Z, Janko K. 2021. Sex chromosomes in meiotic, hemiclonal, clonal and polyploid hybrid vertebrates: along the “extended speciation continuum.” Philos Trans R Soc Lond B Biol Sci 376: 20200103. 10.1098/rstb.2020.0103 PubMed DOI PMC

Thompson KA, Brandvain Y, Coughlan JM, Delmore KE, Justen H, Linnen CR, Ortiz-Barrientos D, Rushworth CA, Schneemann H, Schumer M, et al. 2023. The ecology of hybrid incompatibilities. Cold Spring Harb Perspect Biol 10.1101/cshperspect.a041440 PubMed DOI PMC

Turelli M, Orr HA. 1995. The dominance theory of Haldane's rule. Genetics 140: 389–402. 10.1093/genetics/140.1.389 PubMed DOI PMC

Turelli M, Orr HA. 2000. Dominance, epistasis and the genetics of postzygotic isolation. Genetics 154: 1663–1679. 10.1093/genetics/154.4.1663 PubMed DOI PMC

Turelli M, Katznelson A, Ginsberg PS. 2022. Why Wolbachia-induced cytoplasmic incompatibility is so common. Proc Natl Acad Sci 119: e2211637119. 10.1073/pnas.2211637119 PubMed DOI PMC

Van de Peer Y, Maere S, Meyer A. 2009. The evolutionary significance of ancient genome duplications. Nat Rev Genet 10: 725–732. 10.1038/nrg2600 PubMed DOI

Van de Peer Y, Mizrachi E, Marchal K. 2017. The evolutionary significance of polyploidy. Nat Rev Genet 18: 411–424. 10.1038/nrg.2017.26 PubMed DOI

Verhoeven KJF, vonHoldt BM, Sork VL. 2016. Epigenetics in ecology and evolution: what we know and what we need to know. Mol Ecol 25: 1631–1638. 10.1111/mec.13617 PubMed DOI

Vibranovski MD, Zhang Y, Long M. 2009. General gene movement off the X chromosome in the Drosophila genus. Genome Res 19: 897–903. 10.1101/gr.088609.108 PubMed DOI PMC

Vicoso B, Charlesworth B. 2009. Effective population size and the faster-X effect: an extended model. Evolution (NY) 63: 2413–2426. 10.1111/j.1558-5646.2009.00719.x PubMed DOI

Vrana PB, Guan XJ, Ingram RS, Tilghman SM. 1998. Genomic imprinting is disrupted in interspecific Peromyscus hybrids. Nat Genet 20: 362–365. 10.1038/3833 PubMed DOI

Vrana PB, Fossella JA, Matteson P, del Rio T, O'Neill MJ, Tilghman SM. 2000. Genetic and epigenetic incompatibilities underlie hybrid dysgenesis in Peromyscus. Nat Genet 25: 120–124. 10.1038/75518 PubMed DOI

Wade MJ. 2001. Infectious speciation. Nature 409: 675–677. 10.1038/35055648 PubMed DOI

Walia H, Josefsson C, Dilkes B, Kirkbride R, Harada J, Comai L. 2009. Dosage-dependent deregulation of an AGAMOUS-LIKE gene cluster contributes to interspecific incompatibility. Curr Biol 19: 1128–1132. 10.1016/j.cub.2009.05.068 PubMed DOI PMC

Werth CR, Windham MD. 1991. A model for divergent, allopatric speciation of polyploid pteridophytes resulting from silencing of duplicate-gene expression. Am Nat 137: 515–526. 10.1086/285180 DOI

White MJD. 1978. Modes of speciation. W. H. Freeman, San Francisco.

Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, Rieseberg LH. 2009. The frequency of polyploid speciation in vascular plants. Proc Natl Acad Sci 106: 13875–13879. 10.1073/pnas.0811575106 PubMed DOI PMC

Wright S. 1941. On the probability of fixation of reciprocal translocations. Am Nat 75: 513–522. 10.1086/280996 DOI

Yadav V, Sun S, Coelho MA, Heitman J. 2020. Centromere scission drives chromosome shuffling and reproductive isolation. Proc Natl Acad Sci 117: 7917–7928. 10.1073/pnas.1918659117 PubMed DOI PMC

Yamagata Y, Yamamoto E, Aya K, Win KT, Doi K, Sobrizal IT, Kanamori H, Wu J, Matsumoto T, et al. 2010. Mitochondrial gene in the nuclear genome induces reproductive barrier in rice. Proc Natl Acad Sci 107: 1494–1499. 10.1073/pnas.0908283107 PubMed DOI PMC

Yang J, Liu W, Lu X, Fu Y, Li L, Luo Y. 2015. High expression of small GTPase Rab3D promotes cancer progression and metastasis. Oncotarget 6: 11125–11138. 10.18632/oncotarget.3575 PubMed DOI PMC

Yoshida K, Makino T, Yamaguchi K, Shigenobu S, Hasebe M, Kawata M, Kume M, Mori S, Peichel CL, Toyoda A, et al. 2014. Sex chromosome turnover contributes to genomic divergence between incipient stickleback species. PLoS Genet 10: e1004223. 10.1371/journal.pgen.1004223 PubMed DOI PMC

Zeh DW, Zeh JA. 2000. Reproductive mode and speciation: the viviparity-driven conflict hypothesis. Bioessays 22: 938–946. 10.1002/1521-1878(200010)22:10<938::AID-BIES9>3.0.CO;2-9 PubMed DOI

Zhang L, Reifová R, Halenková Z, Gompert Z. 2021. How important are structural variants for speciation? Genes (Basel) 12: 1084. 10.3390/genes12071084 PubMed DOI PMC

Zhu YO, Sherlock G, Petrov DA. 2016. Whole genome analysis of 132 clinical Saccharomyces cerevisiae strains reveals extensive ploidy variation. G3 (Bethesda) 6: 2421–2434. 10.1534/g3.116.029397 PubMed DOI PMC

Zuellig MP, Sweigart AL. 2018. Gene duplicates cause hybrid lethality between sympatric species of Mimulus. PLoS Genet 14: e1007130. 10.1371/journal.pgen.1007130 PubMed DOI PMC

Synthesis and Scope of the Role of Postmating Prezygotic Isolation in Speciation

A cyclical switch of gametogenic pathways in hybrids depends on the ploidy level