Lab Meeting Feb. 14th: Mouse Hybrid Zones

Posted on Posted in Lab Meetings

We’ll meet this Thursday at 4PM. Below the fold, I’m including a list of papers on the emerging model systems – Ficedula flycatchers, Heliconius butterflies, sticklebacks, and mice – that we plan to discuss this semester. Note that this list of papers is not comprehensive (it’s really just a list of the papers I read while preparing a recent grant); its my expectation that people will bring new papers on these groups to the table throughout the semester.

Since I’ve been delinquent in getting this list you, I’m going to lead this week’s discussion. We’re going to start off with two studies of gene flow across house mouse hybrid zones:

Payseur, B. A., J. G. Krenz, and M. W. Nachman. 2004. Differential patterns of introgression across the X chromosome in a hybrid zone between two species of house mice. Evolution 58:2064–2078. [doi link]

Macholán, M., P. Munclinger, M. Šugerková, P. Dufková, B. Bímová, E. Božíková, J. Zima, and J. Piálek. 2007. Genetic analysis of autosomal and x-linked markers across a  mouse hybrid zone. Evolution 61:746–771. [doi link]

Don’t forget to bring other recent papers to share!


Borge, T., K. Lindroos, P. Nádvorník, A. C. Syvanen, and G. P. Saetre. 2005. Amount of introgression in flycatcher hybrid zones reflects regional differences in pre and post-zygotic barriers to gene exchange. Journal of Evolutionary Biology 18:1416–1424.

Ellegren, H., L. Gustafsson, and B. C. Sheldon. 1996. Sex ratio adjustment in relation to paternal attractiveness in a wild bird population. Proceedings Of The National Academy Of Sciences Of The United States Of America 93:11723–11728.

Ellegren, H., L. Smeds, R. Burri, P. I. Olason, N. Backström, T. Kawakami, A. Künstner, H. Mäkinen, K. Nadachowska-Brzyska, A. Qvarnström, S. Uebbing, and J. B. W. Wolf. 2012. The genomic landscape of species divergence in Ficedula flycatchers. Nature 491:756–760.

Qvarnström, A., A. M. Rice, and H. Ellegren. 2010. Speciation in Ficedula flycatchers. Philosophical Transactions Of The Royal Society B-Biological Sciences 365:1841–1852.

Qvarnström, A., and R. I. Bailey. 2008. Speciation through evolution of sex-linked genes. Heredity 102:4–15.

Qvarnström, A., T. Pärt, and B. C. Sheldon. 2000. Adaptive plasticity in mate preference linked to differences in reproductive effort. Nature 405:344–347.

Rice, A. M., A. Rudh, H. Ellegren, and A. Qvarnström. 2010. A guide to the genomics of ecological speciation in natural animal populations. Ecology Letters 14:9–18.

Saether, S. A., G.-P. Saetre, T. Borge, C. Wiley, N. Svedin, G. Andersson, T. Veen, J. Haavie, M. R. Servedio, S. Bures, M. Král, M. B. Hjernquist, L. Gustafsson, J. Träff, and A. Qvarnström. 2007. Sex chromosome-linked species recognition and evolution of reproductive isolation in flycatchers. Science 318:95–97.

Saetre, G.-P., and S. A. Saether. 2010. Ecology and genetics of speciation in Ficedula flycatchers. Molecular Ecology 19:1091–1106.

Veen, T., T. Borge, S. C. Griffith, G. P. Saetre, S. Bures, L. Gustafsson, and B. C. Sheldon. 2001. Hybridization and adaptive mate choice in flycatchers. Nature 411:45–50.

Wiley, C., A. Qvarnström, G. Andersson, T. Borge, and G.-P. Saetre. 2009. Postzygotic isolation over multiple generations of hybrid descendents in a natural hybrid zone: how well do single-generation estimates reflect reproductive isolation? Evolution 63:1731–1739.


Baxter, S. W., N. J. Nadeau, L. S. Maroja, P. Wilkinson, B. A. Counterman, A. Dawson, M. Beltran, S. Perez-Espona, N. Chamberlain, L. Ferguson, R. Clark, C. Davidson, R. Glithero, J. Mallet, W. O. McMillan, M. Kronforst, M. Joron, R. H. ffrench-Constant, and C. D. Jiggins. 2010. Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in the Heliconius melpomene Clade. PLoS Genetics 6:e1000794.

Brower, A. V. Z. 2013. Introgression of wing pattern alleles and speciation via homoploid hybridization in Heliconius butterflies: a review of evidence from the genome. Proceedings of the Royal Society B-Biological Sciences 280:20122302.

Daniels, E. V., and R. D. Reed. 2012. Xanthurenic acid is a pigment in Junonia coenia butterfly wings. Biochemical Systematics and Ecology 44:161–163.

Daniels, E. V., K. A. Mooney, and R. D. Reed. 2012. Seasonal wing colour plasticity varies dramatically between buckeye butterfly populations in different climatic zones. Ecological Entomology 37:155–159.

Finkbeiner, S. D., A. D. Briscoe, and R. D. Reed. 2012. The benefit of being a social butterfly: communal roosting deters predation. Proceedings of the Royal Society B-Biological Sciences 279:2769–2776.

Hines, H., R. Papa, M. Ruiz, A. Papanicolaou, C. Wang, H. Nijhout, W. McMillan, and R. Reed. 2012. Transcriptome analysis reveals novel patterning and pigmentation genes underlying Heliconius butterfly wing pattern variation. BMC Genomics 13:288.

Mallet, J., and K. K. Dasmahapatra. 2012. Hybrid zones and the speciation continuum in Heliconius butterflies. Molecular Ecology 21:5643–5645.

Martin, A., R. Papa, N. J. Nadeau, R. I. Hill, B. A. Counterman, G. Halder, C. D. Jiggins, M. R. Kronforst, A. D. Long, W. O. McMillan, and R. D. Reed. 2012. Diversification of complex butterfly wing patterns by repeated regulatory evolution of a Wnt ligand. Proceedings of the ….

Nadeau, N. J., A. Whibley, R. T. Jones, J. W. Davey, K. K. Dasmahapatra, S. W. Baxter, M. A. Quail, M. Joron, R. H. ffrench-Constant, M. L. Blaxter, J. Mallet, and C. D. Jiggins. 2012. Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing. Philosophical Transactions Of The Royal Society B-Biological Sciences 367:343–353.

Nadeau, N. J., S. H. Martin, K. M. Kozak, and C. Salazar. 2013. Genome-wide patterns of divergence and gene flow across a butterfly radiation. Molecular … 22:814–826.

Reed, R. D., R. Papa, A. Martin, H. M. Hines, B. A. Counterman, C. Pardo-Diaz, C. D. Jiggins, N. L. Chamberlain, M. R. Kronforst, R. Chen, G. Halder, H. F. Nijhout, and W. O. McMillan. 2011. optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science 333:1137–1141.


Bierne, N., J. Welch, E. Loire, F. Bonhomme, and P. David. 2011. The coupling hypothesis: why genome scans may fail to map local adaptation genes. Molecular Ecology 20:2044–2072.

Britton-Davidian, J., F. Fel-clair, J. Lopez, P. Alibert, and P. Boursot. 2005. Postzygotic isolation between the two European subspecies of the house mouse: estimates from fertility patterns in wild and laboratory-bred hybrids. Biological Journal Of The Linnean Society 84:379–393.

Campbell, P., J. M. Good, and M. W. Nachman. 2013. Meiotic Sex Chromosome Inactivation is Disrupted in Sterile Hybrid Male House Mice. Genetics.

Campbell, P., J. M. Good, M. D. Dean, P. K. Tucker, and M. W. Nachman. 2012. The contribution of the Y chromosome to hybrid male sterility in house mice. Genetics 191:1271–1281.

Dod, B., L. S. Jermiin, P. Boursot, V. H. Chapman, J. T. Nielsen, and F. Bonhomme. 1993. Counterselection on sex chromosomes in the Mus musculus European hybrid zone. Journal of Evolutionary Biology 6:529–546.

Duvaux, L., K. Belkhir, M. Boulesteix, and P. Boursot. 2011. Isolation and gene flow: inferring the speciation history of European house mice. Molecular Ecology 20:5248–5264.

Ganem, G., C. Litel, and T. Lenormand. 2008. Variation in mate preference across a house mouse hybrid zone. Heredity 100:594–601.

Geraldes, A., P. Basset, B. Gibson, K. L. Smith, B. Harr, H.-T. Yu, N. Bulatova, Y. Ziv, and M. W. Nachman. 2008. Inferring the history of speciation in house mice from autosomal, X-linked, Y-linked and mitochondrial genes. Molecular Ecology 17:5349–5363.

Good, J. M., M. A. Handel, and M. W. Nachman. 2008a. Asymmetry and polymorphism of hybrid male sterility during the early stages of speciation in house mice. Evolution 62:50–65.

Good, J. M., M. D. Dean, and M. W. Nachman. 2008b. A complex genetic basis to X-linked hybrid male sterility between two species of house mice. Genetics 179:2213–2228.

Harr, B., and L. M. Turner. 2010. Genome-wide analysis of alternative splicing evolution among Mus subspecies. Molecular Ecology 19 Suppl 1:228–239.

Macholán, M., P. Munclinger, M. Šugerková, P. Dufková, B. Bímová, E. Božíková, J. Zima, and J. Piálek. 2007. Genetic analysis of autosomal and x-linked markers across a  mouse hybrid zone. Evolution 61:746–771.

Melo-Ferreira, J., P. C. Alves, J. Rocha, N. Ferrand, and P. Boursot. 2011. Interspecific x-chromosome and mitochonrial DNA introgression in the Iberian Hare: selection or allele surfing. Evolution 65:1956–1968.

Nachman, M. W., and B. A. Payseur. 2012. Recombination rate variation and speciation: theoretical predictions and empirical results from rabbits and mice. Philosophical Transactions Of The Royal Society B-Biological Sciences 367:409–421.

Nunes, A. C., J. Catalan, J. Lopez, M. D. G. Ramalhinho, M. D. L. Mathias, and J. Britton-Davidian. 2011. Fertility assessment in hybrids between monobrachially homologous Rb races of the house mouse from the island of Madeira: implications for modes of chromosomal evolution. Heredity 106:348–356.

Oka, A., T. Aoto, Y. Totsuka, R. Takahashi, M. Ueda, A. Mita, N. Sakurai-Yamatani, H. Yamamoto, S. Kuriki, N. Takagi, K. Moriwaki, and T. Shiroishi. 2007. Disruption of genetic interaction between two autosomal regions and the X chromosome causes reproductive isolation between mouse strains derived from different subspecies. Genetics 175:185–197.

Payseur, B. A., and H. E. Hoekstra. 2005. Signatures of reproductive isolation in patterns of single nucleotide diversity across inbred strains of mice. Genetics 171:1905–1916.

Payseur, B. A., and M. Place. 2007. Searching the genomes of inbred mouse strains for incompatibilities that reproductively isolate their wild relatives. The Journal of heredity 98:115–122.

Payseur, B. A., J. G. Krenz, and M. W. Nachman. 2004. Differential patterns of introgression across the X chromosome in a hybrid zone between two species of house mice. Evolution 58:2064–2078.

Staubach, F., A. Lorenc, P. W. Messer, K. Tang, D. A. Petrov, and D. Tautz. 2012. Genome patterns of selection and introgression of haplotypes in natural populations of the house mouse (Mus musculus). PLoS Genetics 8:e1002891.

Teeter, K. C., L. M. Thibodeau, Z. Gompert, C. A. Buerkle, M. W. Nachman, and P. K. Tucker. 2009. The variable genomic architecture of isolation between hybridizing species of house mice. Evolution 64:472–485.

Tucker, P. K., R. D. Sage, J. Warner, A. C. Wilson, and E. M. Eicher. 1992. Abrupt cline for sex chromosomes in a hybrid zone between two species of mice. Evolution:1146–1163.

Turner, L. M., D. J. Schwahn, and B. Harr. 2012. Reduced male fertility is common but highly variable in form and severity in a natural house mouse hybrid zone. Evolution 66:443–458.

Wang, L., K. Luzynski, J. E. Pool, V. Janoušek, P. Dufková, M. M. Vysko?ilová, K. C. Teeter, M. W. Nachman, P. Munclinger, M. Macholán, J. Piálek, and P. K. Tucker. 2011. Measures of linkage disequilibrium among neighbouring SNPs indicate asymmetries across the house mouse hybrid zone. Molecular Ecology 20:2985–3000.

White, M. A., M. Stubbings, B. L. Dumont, and B. A. Payseur. 2012. Genetics and evolution of hybrid male sterility in house mice. Genetics 191:917–934.


Albert, A. Y. K., S. Sawaya, T. H. Vines, A. K. Knecht, C. T. Miller, B. R. Summers, S. Balabhadra, D. M. Kingsley, and D. Schluter. 2008. The genetics of adaptive shape shift in stickleback: pleiotropy and effect size. Evolution 62:76–85.

Ba?bura, J., and T. C. M. Bakker. 1995. Lateral Plate Morph Genetics Revisited: Evidence for a Fourth Morph in Three-Spined Sticklebacks. Behaviour 132:1153–1171.

Barrett, R. D. H., S. M. Rogers, and D. Schluter. 2008. Natural selection on a major armor gene in threespine stickleback. Science 322:255–257.

Bell, M. A. 1995. Intraspecific systematics of Gasterosteus aculeatus populations: implications for behavioral ecology. Behaviour 132:1131–1152.

Bell, M. A., W. E. Aguirre, and N. J. Buck. 2004. Twelve years of contemporary armor evolution in a threespine stickleback population. Evolution 58:814–824.

Colosimo, P. F., C. L. Peichel, K. Nereng, B. K. Blackman, M. D. Shapiro, D. Schluter, and D. M. Kingsley. 2004. The genetic architecture of parallel armor plate reduction in threespine sticklebacks. PLoS Biology 2:E109.

Colosimo, P. F., K. E. Hosemann, S. Balabhadra, G. Villarreal, M. Dickson, J. Grimwood, J. Schmutz, R. M. Myers, D. Schluter, and D. M. Kingsley. 2005. Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 307:1928–1933.

Cresko, W. A., A. Amores, C. Wilson, J. Murphy, M. Currey, P. Phillips, M. A. Bell, C. B. Kimmel, and J. H. Postlethwait. 2004. Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations. Proceedings Of The National Academy Of Sciences Of The United States Of America 101:6050–6055.

Cresko, W. A., K. L. McGuigan, P. C. Phillips, and J. H. Postlethwait. 2007. Studies of threespine stickleback developmental evolution: progress and promise. Genetica 129:105–126.

Hendry, A. P., E. B. Taylor, and J. D. McPhail. 2002. Adaptive divergence and the balance between selection and gene flow: lake and stream stickleback in the misty system. Evolution 56:1199–1216.

Hohenlohe, P. A., S. Bassham, P. D. Etter, N. Stiffler, E. A. Johnson, and W. A. Cresko. 2010. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genetics 6:e1000862–.

Jones, F. C., C. Brown, J. M. Pemberton, and V. A. Braithwaite. 2006. Reproductive isolation in a threespine stickleback hybrid zone. Journal of Evolutionary Biology 19:1531–1544.

Jones, F. C., M. G. Grabherr, Y. F. Chan, P. Russell, E. Mauceli, J. Johnson, R. Swofford, M. Pirun, M. C. Zody, S. White, E. Birney, S. Searle, J. Schmutz, J. Grimwood, M. C. Dickson, R. M. Myers, C. T. Miller, B. R. Summers, A. K. Knecht, S. D. Brady, H. Zhang, A. A. Pollen, T. Howes, C. Amemiya, Broad Institute Genome Sequencing Platform & Whole Genome Assembly Team, J. Baldwin, T. Bloom, D. B. Jaffe, R. Nicol, J. Wilkinson, E. S. Lander, F. Di Palma, K. Lindblad-Toh, and D. M. Kingsley. 2012a. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484:55–61.

Jones, F. C., Y. F. Chan, J. Schmutz, J. Grimwood, S. D. Brady, A. M. Southwick, D. M. Absher, R. M. Myers, T. E. Reimchen, B. E. Deagle, D. Schluter, and D. M. Kingsley. 2012b. A genome-wide SNP genotyping array reveals patterns of global and repeated species-pair divergence in sticklebacks. Current biology : CB 22:83–90.

Kimmel, C. B., B. Ullmann, C. Walker, C. Wilson, M. Currey, P. C. Phillips, M. A. Bell, J. H. Postlethwait, and W. A. Cresko. 2005. Evolution and development of facial bone morphology in threespine sticklebacks. Proceedings Of The National Academy Of Sciences Of The United States Of America 102:5791–5796.

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Kingsley, D., K. Hosemann, P. Colosimo, and B. Summers. 2004b. A simple and efficient microinjection protocol for making transgenic sticklebacks. Behaviour 141:1345–1355.

Kitano, J., J. A. Ross, S. Mori, M. Kume, F. C. Jones, Y. F. Chan, D. M. Absher, J. Grimwood, J. Schmutz, R. M. Myers, D. M. Kingsley, and C. L. Peichel. 2009. A role for a neo-sex chromosome in stickleback speciation. Nature 461:1079–1083.

Malek, T. B., J. W. Boughman, I. Dworkin, and C. L. Peichel. 2012. Admixture mapping of male nuptial colour and body shape in a recently formed hybrid population of threespine stickleback. Molecular Ecology 21:5265–5279.

Malhi, R. S., G. Rhett, and A. M. Bell. 2006. Mitochondrial DNA evidence of an early Holocene population expansion of threespine sticklebacks from Scotland. Molecular Phylogenetics and Evolution 40:148–154.

Mäkinen, H. S., J. M. Cano, and J. Merilä. 2006. Genetic relationships among marine and freshwater populations of the European three-spined stickleback (Gasterosteus aculeatus) revealed by microsatellites. Molecular Ecology 15:1519–1534.

McKinnon, J. S., S. Mori, B. K. Blackman, L. David, D. M. Kingsley, L. Jamieson, J. Chou, and D. Schluter. 2004. Evidence for ecology’s role in speciation. Nature 429:294–298.

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Raeymaekers, J. A. M., J. K. J. Van Houdt, M. H. D. Larmuseau, S. Geldof, and F. A. M. Volckaert. 2006. Divergent selection as revealed by PST and QTL-based FST in three-spined stickleback (Gasterosteus aculeatus) populations along a coastal-inland gradient. Molecular Ecology 16:891–905.

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