Speciation may occur when the genomes of two populations accumulate genetic incompatibilities and/or chromosomal rearrangements that prevent inter-breeding in nature. Chromosome stability is critical for survival and faithful transmission of the genome, and hybridization can compromise this. However, the role of chromosomal stability on hybrid incompatibilities has rarely been tested in recently diverged populations. Here, we test for chromosomal instability in hybrids between nascent species, the 'dwarf' and 'normal' lake whitefish (Coregonus clupeaformis). We examined chromosomes in pure embryos, and healthy and malformed backcross embryos. While pure individuals displayed chromosome numbers corresponding to the expected diploid number (2n = 80), healthy backcrosses showed evidence of mitotic instability through an increased variance of chromosome numbers within an individual. In malformed backcrosses, extensive aneuploidy corresponding to multiples of the haploid number (1n = 40, 2n = 80, 3n = 120) was found, suggesting meiotic breakdown in their F1 parent. However, no detectable chromosome rearrangements between parental forms were identified. Genomic instability through aneuploidy thus appears to contribute to reproductive isolation between dwarf and normal lake whitefish, despite their very recent divergence (approx. 15-20 000 generations). Our data suggest that genetic incompatibilities may accumulate early during speciation and limit hybridization between nascent species.

Département de Biologie Institut de Biologie Intégrative et des Systèmes Université Laval Québec Canada G1V 0A6

Laboratory of Fish Genetics Institute of Animal Physiology and Genetics Czech Academy of Sciences 277 21 Libe˘chov Czech Republic

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Coyne J, Orr HA. 2004. Speciation. Sunderland, MA: Sinauer Associates, Inc.

Seehausen O, et al. 2014. Genomics and the origin of species. Nat. Rev. Genet. 15, 176–192. (10.1038/nrg3644) PubMed DOI

Coyne J, Orr HA. 1997. ‘'Patterns of speciation in Drosophila‘‘ revisited. Evolution 51, 295–303. (10.2307/2410984) PubMed DOI

Muller HJ. 1939. Reversibility in evolution considered from the standpoint of genetics. Biol. Rev. 14, 261–280. (10.1111/j.1469-185X.1939.tb00934.x) DOI

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

Noor MA, Grams KL, Bertucci LA, Reiland J. 2001. Chromosomal inversions and the reproductive isolation of species. Proc. Natl Acad. Sci. USA 98, 12 084–12 088. (10.1073/pnas.221274498) PubMed DOI PMC

Rieseberg LH. 2001. Chromosomal rearrangements and speciation. Trends Ecol. Evol. 16, 351–358. (doi:1016/S0169-5347(01)02187-5) PubMed

Faria R, Navarro A. 2010. Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends Ecol. Evol. 25, 660–669. (10.1016/j.tree.2010.07.008) PubMed DOI

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

Pinney E. 1918. A Study of the relation of the behavior of the chromatin to development and heredity in teleost hybrids. J. Morphol. 31, 225–291. (10.1002/jmor.1050310202) DOI

White M. 1969. Chromosomal rearrangements and speciation in animals. Annu. Rev. Genet. 3, 75–98. (10.1007/s10577-013-9377-5) DOI

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

Pialek J, Hauffe HC, Searle JB. 2005. Chromosomal variation in the house mouse. Biol. J. Linn. Soc. 84, 535–563. (10.1111/j.1095-8312.2005.00454.x) DOI

Hauffe HC, Gimenez MD, Searle JB. 2012. Chromosomal hybrid zones in the house mouse. In Evolution of the house mouse (eds Macholán M, Baird SJE, Munclinger P, Pialek J.), pp. 407–430. Cambridge, UK: Cambridge University Press.

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. USA 110, E468–E477. (10.1073/pnas.1219126110) PubMed DOI PMC

Via S. 2009. Natural selection in action during speciation. Proc. Natl Acad. Sci. USA 106(Suppl. 1), 9939–9946. (10.1073/pnas.0901397106) PubMed DOI PMC

Bernatchez L, et al. 2010. On the origin of species: insights from the ecological genomics of lake whitefish. Phil. Trans. R. Soc. B 365, 1783–1800. (10.1098/rstb.2009.0274) PubMed DOI PMC

Jacobsen MW, Hansen MM, Orlando L, Bekkevold D, Bernatchez L, Willerslev E, Gilbert MTP. 2012. Mitogenome sequencing reveals shallow evolutionary histories and recent divergence time between morphologically and ecologically distinct European whitefish (Coregonus spp.). Mol. Ecol. 21, 2727–2742. (10.1111/j.1365-294X.2012.05561.x) PubMed DOI

Bateson W. 1909. Heredity and variation in modern lights. In Darwin and modern science (ed. Seward AC.), pp. 85–101. Cambridge, UK: Cambridge University Press.

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

Bernatchez L. 2004. Ecological theory of adaptive radiation: an empirical assessment from coregonine fishes (Salmoniformes). In Evolution illuminated: salmon and their relatives (eds Hendry AP, Stearns SC.), pp. 175–207. Oxford, UK: Oxford University Press.

Gagnaire P-A, Pavey SA, Normandeau E, Bernatchez L. 2013. The genetic architecture of reproductive isolation during speciation-with-gene-flow in lake whitefish species pairs assessed by RAD sequencing. Evolution 67, 2483–2497. (10.1111/evo.12075) PubMed DOI

Renaut S, Nolte AW, Rogers SM, Derome N, Bernatchez L. 2011. SNP signatures of selection on standing genetic variation and their association with adaptive phenotypes along gradients of ecological speciation in lake whitefish species pairs (Coregonus spp.). Mol. Ecol. 20, 545–559. (10.1111/j.1365-294X.2010.04952.x) PubMed DOI

Lu G, Bernatchez L. 1998. Experimental evidence for reduced hybrid viability between dwarf and normal ecotypes of lake whitefish (Coregonus clupeaformis Mitchill). Proc. R. Soc. Lond. B 265, 1025–1030. (10.1098/rspb.1998.0394) DOI

Rogers SM, Bernatchez L. 2006. The genetic basis of intrinsic and extrinsic post-zygotic reproductive isolation jointly promoting speciation in the lake whitefish species complex (Coregonus clupeaformis). J. Evol. Biol. 19, 1979–1994. (10.1111/j.1420-9101.2006.01150.x) PubMed DOI

Renaut S, Bernatchez L. 2011. Transcriptome-wide signature of hybrid breakdown associated with intrinsic reproductive isolation in lake whitefish species pairs (Coregonus spp. Salmonidae). Heredity 106, 1003–1011. (10.1038/hdy.2010.149) PubMed DOI PMC

Landry CR, Hartl DL, Ranz JM. 2007. Genome clashes in hybrids: insights from gene expression. Heredity 99, 483–493. (10.1038/sj.hdy.6801045) PubMed DOI

Dion-Côté A-M, 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

Renaut S, Nolte AW, Bernatchez L. 2010. Mining transcriptome sequences towards identifying adaptive single nucleotide polymorphisms in lake whitefish species pairs (Coregonus spp. Salmonidae). Mol. Ecol. 19(Suppl. 1), 115–131. (10.1111/j.1365-294X.2009.04477.x) PubMed DOI

Feder JL, Gejji R, Powell THQ, Nosil P. 2011. Adaptive chromosomal divergence driven by mixed geographic mode of evolution. Evolution 65, 2157–2170. (10.1111/j.1558-5646.2011.01321.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

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

Lindsley DL, et al. 1972. Segmental aneuploidy and the genetic gross structure of the Drosophila genome. Genetics 71, 157–184. PubMed PMC

Torres EM, Williams BR, Amon A. 2008. Aneuploidy: cells losing their balance. Genetics 179, 737–746. (10.1534/genetics.108.090878) PubMed DOI PMC

Barbero JL. 2011. Sister chromatid cohesion control and aneuploidy. Cytogenet. Genome Res. 133, 223–233. (10.1159/000323507) PubMed DOI

Renaut S, Nolte A, Bernatchez L. 2009. Gene expression divergence and hybrid misexpression between lake whitefish species pairs (Coregonus spp. Salmonidae). Mol. Biol. Evol. 26, 925–936. (10.1093/molbev/msp017) PubMed DOI

Völker M, Rab P, Kullmann H. 2005. Karyotype differentiation in chromaphyosemion killifishes (Cyprinodontiformes, Nothobranchiidae). I: Chromosome banding patterns of C. alpha, C. kouamense and C. lugens. Genetica 125, 33–41. (10.1007/s10709-005-4267-1) PubMed DOI

Fujiwara A, Nishida-Umehara C, Sakamoto T, Okamoto N, Nakayama I, Abe S. 2001. Improved fish lymphocyte culture for chromosome preparation. Genetica 111, 77–89. (10.1023/A:1013788626712) PubMed DOI

Yano A, Nicol B, Jouanno E, Quillet E, Fostier A, Guyomard R, Guiguen Y. 2012. The sexually dimorphic on the Y-chromosome gene (sdY) is a conserved male-specific Y-chromosome sequence in many salmonids. Evol. Appl. 6, 486–496. (10.1111/eva.12032) PubMed DOI PMC

Davidson WS, Huang TK, Fujiki K, Schalburg von KR, Koop BF. 2009. The sex determining loci and sex chromosomes in the family Salmonidae. Sex Dev. 3, 78–87. (10.1159/000223073) PubMed DOI

R Core Team. 2012. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

Phillips RB, Reed KM, Rab P. 1996. Revised karyotypes and chromosome banding of coregonid fishes from the Laurentian Great Lakes. Can. J. Zool. 74, 323–329. (10.1139/z96-040) DOI

Völker M, Rab P. In press. Direct chromosome preparation from embryos and larvae. In Fish cytogenetic techniques (Chondrichthyans and Teleosts) (eds Ozouf-Costaz C, Pisano E, Foresti F, Foresti de Almeida Foresto L.). Boca Raton, FL: CRC Press.

Symonová R, Majtánová Z, Sember A, Staaks GB, Bohlen J, Freyhof J, Rábová M, Rab P. 2013. Genome differentiation in a species pair of coregonine fishes: an extremely rapid speciation driven by stress-activated retrotransposons mediating extensive ribosomal DNA multiplications. BMC Evol. Biol. 13, 42 (10.1007/BF02153623) PubMed DOI PMC

Harfe BD, Jinks-Robertson S. 2000. DNA mismatch repair and genetic instability. Annu. Rev. Genet. 34, 359–399. (10.1146/annurev.genet.34.1.359) PubMed DOI

Greig D, Travisano M, Louis EJ, Borts RH. 2003. A role for the mismatch repair system during incipient speciation in Saccharomyces. J. Evol. Biol. 16, 429–437. (10.1046/j.1420-9101.2003.00546.x) 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

Grewal SIS, Jia S. 2007. Heterochromatin revisited. Nat. Rev. Genet. 8, 35–46. (10.1038/nrg2008) PubMed DOI

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

Bayes JJ, Malik HS. 2009. Altered heterochromatin binding by a hybrid sterility protein in Drosophila sibling species. Science 326, 1538–1541. (10.1126/science.1181756) PubMed DOI PMC

Cattani MV, Presgraves DC. 2012. Incompatibility between X chromosome factor and pericentric heterochromatic region causes lethality in hybrids between Drosophila melanogaster and its sibling species. Genetics 191, 549–559. (10.1534/genetics.112.139683) PubMed DOI PMC

Waddington CH. 1942. Canalization of development and the inheritance of acquired characters. Nature 150, 563–565. PubMed

Sheltzer JM, Torres EM, Dunham MJ, Amon A. 2012. Transcriptional consequences of aneuploidy. Proc. Natl Acad. Sci. USA 109, 12 644–12 649. (10.1073/pnas.1209227109) PubMed DOI PMC

Dürrbaum M, Kuznetsova AY, Passerini V, Stingele S, Stoehr G, Storchová Z. 2014. Unique features of the transcriptional response to model aneuploidy in human cells. BMC Genomics 15, 139 (10.1186/1471-2164-15-139) PubMed DOI PMC

Charron G, Leducq J-B, Landry CR. 2014. Chromosomal variation segregates within incipient species and correlates with reproductive isolation. Mol. Ecol. 23, 4362–4372. (10.1111/mec.12864) PubMed DOI

Forejt J, Pialek J, Trachtulec Z. 2012. Hybrid male sterility in mouse subspecific crosses. In Evolution of the house mouse (eds Macholán M, Baird SJE, Munclinger P, Pialek J.), pp. 482–503. Cambridge, UK: Cambridge University Press.

Macholán M, Baird SJE, Munclinger P, Pialek J. (eds). 2012 Evolution of the house mouse. Cambridge, UK: Cambridge University Press.

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 63, 3061–3075. (10.1111/j.1558-5646.2009.00786.x) PubMed DOI

Campbell D, Bernatchez L. 2004. Generic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. Mol. Biol. Evol. 21, 945–956. (10.1093/molbev/msh101) PubMed DOI

Bernatchez L, Dodson JJ. 1991. Phylogeographic structure in mitochondrial DNA of the lake whitefish (Coregonus clupeaformis) and its relation to Pleistocene glaciations. Evolution 45, 1016–1035. PubMed

Gagnaire P-A, Normandeau E, Pavey SA, Bernatchez L. 2012. Mapping phenotypic, expression and transmission ratio distortion QTL using RAD markers in the lake whitefish (Coregonus clupeaformis). Mol. Ecol. 22, 3036–3048. (10.1111/mec.12127) PubMed DOI

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