Genomics of Adaptation and Speciation
winter semester 2019
15 Oct 2018 - 9 Feb 2019
Prof. Dr. Jochen Wolf
Dr. Ricardo J Pereira
Species formation has fascinated evolutionary biologists for centuries. How does natural selection lead to local adaptation? Can genetic incompatibilities maintain species borders? How do these processes interact during the continuum of species formation? These questions have remained unanswered largely due to the lack of genomic tools that can be applicable across species. The recent advent of high-throughput sequencing has unlocked these limitations and allows applications to virtually any kind of organism. In this seminar, we will discuss the most recent papers defining new benchmarks in genomics of speciation. We will discuss foundational theory supporting new research questions, advantages of current genomic methodologies, and the limitation defining future advances of the field.
In this master-level course, you will:
- Get familiar with long standing questions and theory on speciation research;
- Understand the advantages and limitations of new genomics methods;
- Identify opportunities for future research.
The program of this seminar covers essential topics on Adaptation and Speciation (see the program below).
Each class consists of a short lecture introducing the core concepts of that topic, followed by the discussion of current papers.
Each student selects a topic according to her/his own research interests, selects a paper from a suggested list or equivalent, and will
However, everyone is expected to
the selected paper and
This seminar assumes that students are confortable with key concepts of the following disciplines:
- Population Genetics;
Previous atendance to these disciplines during undergraduate or master courses is not enforced, but students are expected to do a self-assessment of their background and complement potential caveats with the review articles suggested below or background reading on specific topics.
- pereira AT bio.lmu.de
- j.wolf AT bio.lmu.de
3 ECTS, 2 SWS
Every week, Monday, 9:00-10:30
Biozentrum (room B03.045)
In order to pass, students must lead the discussion of one paper (i.e. presentation of an article) and participate actively in the discussion of any of the other topics.
Thu final grading is based both on the presentation (50%) and on the student's participation in the discussion throughout the entire course (50%).
Below there's a description of the topics addressed in each discussion session, along with a list of key concepts and suggested papers.
Students are free to suggest papers beyond this list, as long as it covers the same topic and one of the key concepts.
The estimated dates of discussion sessions and the initials of the initials of the discussion leader/s are marked below, but note that these are subjected to changes during the course of the semester. Papers chosen for each discussion session are marked in bold
Presentation of the course
15 Oct 2018; led by R. Pereira
22 Oct 2018; led by R. Pereira and XX
- The geography of speciation;
- Demographic parameters of speciation;
- Genomic methods in the study of geographic structure.
Meier, J. I., Sousa, V. C., Marques, D. A., Selz, O. M., Wagner, C. E., Excoffier, L., & Seehausen, O. (2016). Demographic modelling with whole-genome data reveals parallel origin of similar Pundamiliacichlid species after hybridization. Molecular Ecology, 26(1), 123–141. http://doi.org/10.1111/mec.13838 link
Pinho, C., and J. Hey. 2010. Divergence with gene flow: Models and data. Ann. Rev. Ecol. Evol. Syst. 41:215–230. link
Sousa, V., & Hey, J. (2013). Understanding the origin of species with genome-scale data: modelling gene flow. Nature Reviews Genetics, 14(6), 404–414. http://doi.org/10.1038/nrg3446 link
Butlin, R. K., J. Galindo, and J. W. Grahame. 2008. Sympatric, parapatric or allopatric: the most important way to classify speciation? Philos. Trans. R. Soc. Lond., B, Biol. Sci. 363:2997–3007.link
29 Oct 2018; led by R. Pereira and XX
- Post-zygotic and intrinsic mechanisms;
- Underdominance and DMIs;
- The two rules of speciation.
Masly, J. P., & Presgraves, D. C. (2007). High-resolution genome-wide dissection of the two rules of speciation in Drosophila. PLoS Biology, 5(9), e243. http://doi.org/10.1371/journal.pbio.0050243 link
Tang, S., and D. C. Presgraves. 2009. Evolution of the Drosophila nuclear pore complex results in multiple hybrid incompatibilities. Science 323:779–782. link
Corbett-Detig, R. B., J. Zhou, A. G. Clark, D. L. Hartl, and J. F. Ayroles. 2013. Genetic incompatibilities are widespread within species. Nature 504:135–137. link
Presgraves, D. C. (2010). The molecular evolutionary basis of species formation. Nature Reviews Genetics, 11(3), 175–180. http://doi.org/10.1038/nrg2718 link
Presgraves, D. C. (2008). Sex chromosomes and speciation in Drosophila. Trends in Genetics, 24(7), 336–343. http://doi.org/10.1016/j.tig.2008.04.007 link
5 Nov 2018; led by R. Pereira and XX
- Co-adaptation between genetic compartiments;
- Mismatch and hybrid breakdown;
- Mito-, Wolbachia-, and holobiont-incompatibilities.
Ellison, C. K., and R. S. Burton. 2008. Interpopulation hybrid breakdown maps to the mitochondrial genome. Evolution 62:631–638. link
Brucker, R. M., and S. R. Bordenstein. 2013. The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus Nasonia
. Science, doi: 10.1126/science.1239053.link
Burton, R. S., R. J. Pereira, and F. S. Barreto. 2013. Cytonuclear Genomic Interactions and Hybrid Breakdown. Annu Rev Ecol Evol S 44:281–302. link
Rand, D. M., Haney, R. A., & Fry, A. J. (2004). Cytonuclear coevolution: the genomics of cooperation. Tree, 19(12), 645–653. link
Bordenstein, S. R., & Theis, K. R. (2015). Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes. PLoS Biology, 13(8), e1002226–23. http://doi.org/10.1371/journal.pbio.1002226 link
12 Nov 2018; led by R. Pereira and XX
- Pre-mating and pre-zygotic mechanisms;
- Sexual selection and assortative mating;
- Sensory drive.
Seehausen, O., Y. Terai, I. S. Magalhaes, K. L. Carleton, H. D. J. Mrosso, R. Miyagi, I. Van Der Sluijs, M. V. Schneider, M. E. Maan, H. Tachida, H. Imai, and N. Okada. 2008. Speciation through sensory drive in cichlid fish. Nature 455:620–626. link
Conte, G. L., and D. Schluter. 2013. Experimental confirmation that body size determines mate preference via phenotype matching in a stickleback species pair. Evolution 67-5:1477–1484. link
Higgie, M., S. Chenoweth, and M. W. Blows. 2000. Natural Selection and the Reinforcement of Mate Recognition. Science 290:519–521. link
Kirkpatrick, M., & Ravigne, V. (2002). Speciation by natural and sexual selection: Models and experiments. American Naturalist, 159(S3), S22–S35. http://doi.org/10.1086/338370. link
Maan, M. E., & Seehausen, O. (2011). Ecology, sexual selection and speciation. Ecology Letters, 14(6), 591–602. http://doi.org/10.1111/j.1461-0248.2011.01606.x. link
19 Nov 2018; led by R. Pereira and XX
- Adaptation to the ecological environment;
- Divergent Natural selection and fitness trade-offs;
- Fitness landscape.
Burke, M. K., G. Liti, and A. D. Long. 2014. Standing Genetic Variation Drives Repeatable Experimental Evolution in Outcrossing Populations of Saccharomyces cerevisiae
. Molecular Biology and Evolution 31:3228–3239. link
Good, B. H., M. J. McDonald, J. E. Barrick, R. E. Lenski, and M. M. Desai. 2017. The dynamics of molecular evolution over 60,000 generations. Nature 1–17. Nature Publishing Group. doi:10.1038/nature24287 link
Lang, G. I., Rice, D. P., Hickman, M. J., Sodergren, E., Weinstock, G. M., Botstein, D., & Desai, M. M. (2013). Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature, 500(7464), 571–574. http://doi.org/10.1038/nature12344 link
Savolainen, O., M. Lascoux, and J. Merilä. 2013. Ecological genomics of local adaptation. Nat Rev Genet 14:807–820. link
Burke, M. K. 2012. How does adaptation sweep through the genome? Insights from long-term selection experiments. Proc Biol Sci 279:5029. link
Barrick, J. E., and R. E. Lenski. 2013. Genome dynamics during experimental evolution. Nat Rev Genet 14:827–839. Nature Publishing Group. link
26 Nov 2018; led by J. Wolf and XX
- Underdominance in hybrids;
- Experimental evolution;
- Mesocosmos experiments.
Barrett, R. D. H., Rogers, S. M., & Schluter, D. (2008). Natural selection on a major armor gene in threespine stickleback. Science, 322(5899), 255–257. http://doi.org/10.1126/science.1159978 link
McBride, C. S., & Singer, M. C. (2010). Field Studies Reveal Strong Postmating Isolation between Ecologically Divergent Butterfly Populations. PLoS Biology, 8(10), e1000529–17. http://doi.org/10.1371/journal.pbio.1000529 link
Dettman, J. R., C. Sirjusingh, L. M. Kohn, and J. B. Anderson. 2007. Incipient speciation by divergent adaptation and antagonistic epistasis in yeast. Nature 447:585. link
3 Dec 2018; led by J. Wolf and XX
- Chromosomal rearrangements;
- Meiotic drive.
Twyford, A. D., and J. Friedman. 2015. Adaptive divergence in the monkey flower Mimulus guttatusis maintained by a chromosomal inversion. Evolution 69:1476–1486. link
Lowry, D. B., and J. H. Willis. 2010. A widespread chromosomal inversion polymorphism contribute top a major life-history transition, local adaptation, and reproductive isolation. PLoS Biol 8:e1000500. link
Wright, K. M., D. Lloyd, D. B. Lowry, M. R. Macnair, and J. H. Willis. 2013. Indirect evolution of hybrid lethality due to linkage with selected locus in Mimulus guttatus. PLoS Biol 11:e1001497. link
Lai, Z., T. Nakazato, M. Salmaso, J. M. Burke, S. Tang, S. J. Knapp, and L. H. Rieseberg. 2005. Extensive chromosomal repatterning and the evolution of sterility barriers in hybrid sunflower species. Genetics 171:291–303. Genetics. link
Twyford, A. D., M. A. Streisfeld, D. B. Lowry, and J. Friedman. 2015. Genomic studies on the nature of species: adaptation and speciation in Mimulus. Molecular Ecology 24:2601–2609. link
Wellenreuther, M., and L. Bernatchez. 2018. Eco-Evolutionary Genomics of Chromosomal Inversions. Trends in Ecology & Evolution 1–14. Elsevier Ltd. link
10 Dec 2018; led by J. Wolf and XX
- The genic view of speciation;
- Heterogeneity of gene flow;
- Hitchhiking and linked selection.
Vijay, N., C. M. Bossu, J. W. Poelstra, M. H. Weissensteiner, A. Suh, A. P. Kryukov, and J. B. W. Wolf. 2016. Evolution of heterogeneous genome differentiation across multiple contact zones in a crow species complex. Nature Communications 7:1–10. link
Poelstra, J. W., N. Vijay, C. M. Bossu, H. Lantz, B. Ryll, I. Mueller, V. Baglione, P. Unneberg, M. Wikelski, M. G. Grabherr, and J. B. W. Wolf. 2014. The genomic landscape underlying phenotypic integrity in the face of gene flow in crows. Science 344:1410–1414. link
17 Dec 2018; led by J. Wolf and XX
- Ecological divergence;
- Reproductive isolation.
Soria-Carrasco, V., Z. Gompert, A. A. Comeault, T. E. Farkas, T. L. Parchman, J. S. Johnston, C. A. Buerkle, J. L. Feder, J. Bast, T. Schwander, S. P. Egan, B. J. Crespi, and P. Nosil. 2014. Stick Insect Genomes Reveal Natural Selection's Role in Parallel Speciation. Science 344:738–742. link
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, J. Baldwin, T. Bloom, D. B. Jaffe, R. Nicol, J. Wilkinson, E. S. Lander, F. Di Palma, K. Lindblad-Toh, and D. M. Kingsley. 2012. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484:55–61. link
Riesch, R., Muschick, M., Lindtke, D., Villoutreix, R., Comeault, A. A., Farkas, T. E., et al. (2017). Transitions between phases of genomic differentiation during stick-insect speciation. Nature Publishing Group, 1, 1–13. http://doi.org/10.1038/s41559-017-0082 link
14 Jan 2019; led by J. Wolf and XX
- Reinforcement vs speciation reversal;
- Adaptive introgression;
- Hybrid speciation.
Dasmahapatra, K. K., J. R. Walters, A. D. Briscoe, J. W. Davey, A. Whibley, N. J. Nadeau, A. V. Zimin, D. S. T. Hughes, L. C. Ferguson, S. H. Martin, C. Salazar, J. J. Lewis, S. Adler, S.-J. Ahn, D. A. Baker, S. W. Baxter, N. L. Chamberlain, R. Chauhan, B. A. Counterman, T. Dalmay, L. E. Gilbert, K. Gordon, D. G. Heckel, H. M. Hines, K. J. Hoff, P. W. H. Holland, E. Jacquin-Joly, F. M. Jiggins, R. T. Jones, D. D. Kapan, P. Kersey, G. Lamas, D. Lawson, D. Mapleson, L. S. Maroja, A. Martin, S. Moxon, W. J. Palmer, R. Papa, A. Papanicolaou, Y. Pauchet, D. A. Ray, N. Rosser, S. L. Salzberg, M. A. Supple, A. Surridge, A. Tenger-Trolander, H. Vogel, P. A. Wilkinson, D. Wilson, J. A. Yorke, F. Yuan, A. L. Balmuth, C. Eland, K. Gharbi, M. Thomson, R. A. Gibbs, Y. Han, J. C. Jayaseelan, C. Kovar, T. Mathew, D. M. Muzny, F. Ongeri, L.-L. Pu, J. Qu, R. L. Thornton, K. C. Worley, Y.-Q. Wu, M. Linares, M. L. Blaxter, R. H. Ffrench-Constant, M. Joron, M. R. Kronforst, S. P. Mullen, R. D. Reed, S. E. Scherer, S. Richards, J. Mallet, W. O. McMillan, C. D. Jiggins, and H. G. Consortium. 2012. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487:94–98. link
Meier, J. I., D. A. Marques, S. Mwaiko, C. E. Wagner, L. Excoffier, and O. Seehausen. 2017. Ancient hybridization fuels rapid cichlid fish adaptive radiations. Nature Communications 8:14363. link
Lamichhaney, S., J. Berglund, M. S. Almén, K. Maqbool, M. Grabherr, A. Martinez-Barrio, M. Promerová, C.-J. Rubin, C. Wang, N. Zamani, B. R. Grant, P. R. Grant, M. T. Webster, and L. Andersson. 2015. Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature 518:371–375. link
Abbott, R., Albach, D., Ansell, S., Arntzen, J. W., Baird, S. J. E., Bierne, N., et al. (2013). Hybridization and speciation. Journal of Evolutionary Biology, 26(2), 229–246. http://doi.org/10.1111/j.1420-9101.2012.02599.x link
21 Jan 2019; led by J. Wolf and XX
- HWE and LD;
- Geographic and genomic clines;
- Admixture mapping.
Singhal, S., & Bi, K. (2017). History cleans up messes: The impact of time in driving divergence and introgression in a tropical suture zone. Evolution, 25, 4692–12. http://doi.org/10.1111/evo.13278 link
Turner, L. M., & Harr, B. (2014). Genome-wide mapping in a house mouse hybrid zone reveals hybrid sterility loci and Dobzhansky-Muller interactions. Elife, 3, 4803–25. http://doi.org/10.7554/eLife.02504 link
Nadeau, N. J., M. Ruiz, P. Salazar, B. Counterman, J. A. Medina, H. Ortiz-Zuazaga, A. Morrison, W. O. McMillan, C. D. Jiggins, and R. Papa. 2014. Population genomics of parallel hybrid zones in the mimetic butterflies, H. melpomene and H. erato. Genome Research 24:1316–1333. Cold Spring Harbor Lab. link
Rafati, N., J. A. Blanco-Aguiar, C. J. Rubin, S. Sayyab, S. J. Sabatino, S. Afonso, C. Feng, P. C. Alves, R. Villafuerte, N. Ferrand, L. Andersson, and M. Carneiro. 2018. A genomic map of clinal variation across the European rabbit hybrid zone. Molecular Ecology 27:1457–1478. Wiley/Blackwell (10.1111).
Larson, E. L., J. A. Andres, S. M. Bogdanowicz, and R. G. Harrison. 2013. Differential introgression in a mosaic hybrid zone reveals candidate barrier genes. Evolution 67:3653–3661. link
Gompert, Z., & Mandeville, E. G. (2017). Analysis of Population Genomic Data from Hybrid Zones. Annual Review of Ecology. http://doi.org/10.1146/annurev-ecolsys-110316-022652 link
Taylor, S. A., E. L. Larson, and R. G. Harrison. 2015. Hybrid zones: windows on climate change. Trends in Ecology & Evolution 30:398–406. Elsevier Ltd.