Genomics of Adaptation and Speciation

summer semester 2021
12 April 2021 - 16 July 2021

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.


As this course will take place online, I've created a Slack workspace ( The invitation to join the Slack will be sent by email to all the students accepted in the course. This workspace is intended to increase interaction among students, which usually happens before or after the class. Please use this space to: share new articles on each topic, share resources that are helpful to you when preparing for the class, coordinate presentations with you colleagues, ask questions to myself or to your colleagues. I encourage everyone to post on #channels rather that through private messaging, so that everyone can contribute to the discussion.




Every week, Monday, 8:30-10:00, CET


During this semester, this seminar will take place online, through a Zoom link to be posted soon. Install Zoom here.
Personal Meeting ID: 974 699 3678
The password and invite link will be sent to all participants by email.


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. This will be particularly challenging during remote teaching, so make sure that you have your video and microphone on during the Zoom session.
The final grading is based both on the presentation (50%) and on the student's participation in the discussions 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 encouraged to suggest papers beyond this list, as long as it covers the same topic and one of the key concepts. The chosen paper must be announced one week before the discussion, in order to give sufficient time for everyone to prepare it.
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 and assigment of topics
19 April 2020, from 8:30 to 10:00; led by R. Pereira

Session 1: The geography and demography of divergence
26 April; speaker: X; moderators: X & X

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
Nolen, Z. J., B. Yildirim, I. Irisarri, S. Liu, C. Groot Crego, D. B. Amby, F. Mayer, M. T. P. Gilbert, and R. J. Pereira. 2020. Historical isolation facilitates species radiation by sexual selection: Insights from Chorthippus grasshoppers. Molecular Ecology 29:4985–5002.

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
3 May; speaker: X; moderators: X

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

Moyle, L., and T. Nakazato. 2010. Hybrid incompatibility “snowballs” between Solanum species. Science 329:1521. link

Review articles:

Meisel, R. P., and T. Connallon. 2013. The faster-X effect: integrating theory and data. Trends Genet. 29:537–544. Elsevier Ltd. link

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
10 May; speaker: X; moderators: X & X

Key concepts:

Research articles:

Healy, T. M., and R. S. Burton. 2020. Strong selective effects of mitochondrial DNA on the nuclear genome. Proceedings of the National Academy of Sciences 117:6616–6621. National Academy of Sciences. link

Barreto, F. S., E. T. Watson, T. G. Lima, C. S. Willett, S. Edmands, W. Li, and R. S. Burton. 2018. Genomic signatures of mitonuclear coevolution across populations of Tigriopus californicus. Nature Publishing Group 2:1250–1257. 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/

Case, A. L., F. R. Finseth, C. M. Barr, and L. Fishman. 2016. Selfish evolution of cytonuclear hybrid incompatibility in Mimulus. Proc Biol Sci 283:20161493–

Ricardo Pereira, Thiago Lima, N Pierce, et al. Recovery from hybrid breakdown reveals a complex genetic architecture of mitonuclear incompatibilities. Authorea. November 30, 2020. DOI: 10.22541/au.160672149.99010965/v1

Meiklejohn CD, Holmbeck MA, Siddiq MA, Abt DN, Rand DM, Montooth KL (2013) An Incompatibility between a Mitochondrial tRNA and Its Nuclear-Encoded tRNA Synthetase Compromises Development and Fitness in Drosophila. Plos Genetics, 9,e1003238.

Review articles:

Sloan, D. B., J. M. Warren, A. M. Williams, Z. Wu, S. E. Abdel-Ghany, A. J. Chicco, and J. C. Havird. 2018. Cytonuclear integration and co-evolution. Nat Rev Genet 1–14. Springer US. 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. link

Session 4: Genetic basis of prezygotic isolation
17 May; speaker: X; moderators: X & X

Key concepts:

Research articles:

Yang, Y., M. R. Servedio, and C. L. Richards-Zawacki. 2019. Imprinting sets the stage for speciation. Nature 1–14. Springer US.

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

Xu, M., and K. L. Shaw. 2019. Genetic coupling of signal and preference facilitates sexual isolation during rapid speciation. Proc Biol Sci 286:20191607–8.

Marques, D. A., K. Lucek, M. P. Haesler, A. F. Feller, J. I. Meier, C. E. Wagner, L. Excoffier, and O. Seehausen. 2016. Genomic landscape of early ecological speciation initiated by selection on nuptial colour. Molecular Ecology 26:7–

Merrill, R. M., P. Rastas, S. H. Martin, M. C. Melo, S. Barker, J. Davey, W. O. McMillan, and C. D. Jiggins. 2019. Genetic dissection of assortative mating behavior. 17:e2005902–21.

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
31 May; speaker: X; moderators: X & X

Key concepts:

Research articles:

Chen, P., and J. Zhang. 2020. Antagonistic pleiotropy conceals molecular adaptations in changing environments. Nature Publishing Group 1–11. Springer US. link

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
14 June; speaker: X; moderators: X & X

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
21 June; speaker: X; moderators: X

Key concepts:

Research articles:

Todesco, M., G. L. Owens, N. Bercovich, J.-S. X. B. L. X. G. x000E9, S. Soudi, D. O. Burge, K. Huang, K. L. Ostevik, E. B. M. Drummond, I. Imerovski, K. Lande, M. A. Pascual-Robles, M. Nanavati, M. Jahani, W. Cheung, S. E. Staton, S. X. P. M. X. os, R. Nielsen, L. A. Donovan, J. M. Burke, S. Yeaman, and L. H. Rieseberg. 2020. Massive haplotypes underlie ecotypic differentiation in sunflowers. Nature 1–30. Springer US.

Faria, R., P. Chaube, H. E. Morales, T. Larsson, A. R. Lemmon, E. M. Lemmon, M. Rafajlović, M. Panova, M. Ravinet, K. Johannesson, A. M. Westram, and R. K. Butlin. 2019. Multiple chromosomal rearrangements in a hybrid zone between Littorina saxatilisecotypes. Molecular Ecology 28:1375–1393. link

Coughlan, J. M., and J. H. Willis. 2019. Dissecting the role of a large chromosomal inversion in life history divergence throughout the Mimulus guttatusspecies complex. Molecular Ecology 28:1343–

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

Christmas, M. J., A. Wallberg, I. Bunikis, A. Olsson, O. Wallerman, and M. T. Webster. 2019. Chromosomal inversions associated with environmental adaptation in honeybees. Molecular Ecology 28:1358–1374. 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
28 Jun; speaker: all; moderators: X & X

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
5 July; speaker: X; moderators: X & X

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

Riesnkch, 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
12 July; speaker: X; moderators: X & x

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
19 July; speaker: X; moderators: X & X

Key concepts:

Research articles:

Powell, D. L., M. García-Olazábal, M. Keegan, P. Reilly, K. Du, A. P. Díaz-Loyo, S. Banerjee, D. Blakkan, D. Reich, P. Andolfatto, G. G. Rosenthal, M. Schartl, and M. Schumer. 2020. Natural hybridization reveals incompatible alleles that cause melanoma in swordtail fish. Science 368:731.

Pulido-Santacruz, P., A. Aleixo, and J. T. Weir. 2018. Morphologically cryptic Amazonian bird species pairs exhibit strong postzygotic reproductive isolation. Proc Biol Sci 285:20172081–9.

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.