Genomics of Adaptation and Speciation

winter semester 2019
15 Oct 2018 - 9 Feb 2019

Prof. Dr. Jochen Wolf
Dr. Ricardo J Pereira

Course Description

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:
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 lead its discussion. However, everyone is expected to read the selected paper and contribute to the discussion.


This seminar assumes that students are confortable with key concepts of the following disciplines: 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.





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

Session 1: The geography and demography of divergence
22 Oct 2018; led by R. Pereira and XX

Key concepts:

Research articles:

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. link

Review articles:

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. 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–

Session 2: Genetic basis of post-zygotic intrinsic isolation
29 Oct 2018; led by R. Pereira and XX

Key concepts:

Research articles:

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. 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

Review articles:

Presgraves, D. C. (2010). The molecular evolutionary basis of species formation. Nature Reviews Genetics, 11(3), 175–180. link

Presgraves, D. C. (2008). Sex chromosomes and speciation in Drosophila. Trends in Genetics, 24(7), 336–343. link

Session 3: Cyto-nuclear incompatibilities: an extension of DMIs
5 Nov 2018; led by R. Pereira and XX

Key concepts:

Research articles:

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/

Review articles:

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. link

Session 4: Genetic basis of prezygotic isolation
12 Nov 2018; led by R. Pereira and XX

Key concepts:

Research articles:

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

Review articles:

Kirkpatrick, M., & Ravigne, V. (2002). Speciation by natural and sexual selection: Models and experiments. American Naturalist, 159(S3), S22–S35. link

Maan, M. E., & Seehausen, O. (2011). Ecology, sexual selection and speciation. Ecology Letters, 14(6), 591–602. link

Session 5: The genetic basis of adaptation
19 Nov 2018; led by R. Pereira and XX

Key concepts:

Research articles:

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. link

Review articles:

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

Session 6: The genetic basis of postzygotic extrinsic isolation
26 Nov 2018; led by J. Wolf and XX

Key concepts:

Research articles:

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. 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. 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

Session 7: Chromosomal speciation
3 Dec 2018; led by J. Wolf and XX

Key concepts:

Research articles:

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

Review articles:

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

Session 8: The genomic landscape of speciation
10 Dec 2018; led by J. Wolf and XX

Key concepts:

Research articles:

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

Session 9: Ecological Speciation: speciation with gene flow and divergent selection
17 Dec 2018; led by J. Wolf and XX

Key concepts:

Research articles:

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. link

Session 10: The evolutionary consequences of hybridization
14 Jan 2019; led by J. Wolf and XX

Key concepts:

Research articles:

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

Review articles:

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. link

Session 11: Hybrid zones as windows into speciation and adaptation
21 Jan 2019; led by J. Wolf and XX

Key concepts:

Research articles:

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. 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. 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).

Review articles:

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. 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.