Genomics of Adaptation and Speciation
summer semester 2021
12 April 2021 - 16 July 2021
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
As this course will take place online, I've created a Slack workspace (genomicsofada-j2e3847.slack.com). 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.
3 ECTS, 2 SWS
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
26 April; speaker: X; moderators: X & X
- 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
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.
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
3 May; speaker: X; moderators: X
- 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
Moyle, L., and T. Nakazato. 2010. Hybrid incompatibility “snowballs” between Solanum species. Science 329:1521. link
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. 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
10 May; speaker: X; moderators: X & X
- Co-adaptation between genetic compartiments;
- Mismatch and hybrid breakdown;
- Mito-, Wolbachia-, and holobiont-incompatibilities.
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/science.1239053.link
Case, A. L., F. R. Finseth, C. M. Barr, and L. Fishman. 2016. Selfish evolution of cytonuclear hybrid incompatibility in Mimulus. Proc Biol Sci 283:20161493–9.link
Ricardo Pereira, Thiago Lima, N Pierce, et al. Recovery from hybrid breakdown reveals a complex genetic architecture of mitonuclear incompatibilities. Authorea. November 30, 2020.
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.
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. http://doi.org/10.1371/journal.pbio.1002226 link
17 May; speaker: X; moderators: X & X
- Pre-mating and pre-zygotic mechanisms;
- Sexual selection and assortative mating;
- Sensory drive.
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 26:7–24.link
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.
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
31 May; speaker: X; moderators: X & X
- Adaptation to the ecological environment;
- Divergent Natural selection and fitness trade-offs;
- Fitness landscape.
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. 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
14 June; speaker: X; moderators: X & X
- 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
21 June; speaker: X; moderators: X
- Chromosomal rearrangements;
- Meiotic drive.
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 28:1343–1357.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
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
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
28 Jun; speaker: all; moderators: X & X
- 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
5 July; speaker: X; moderators: X & X
- 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
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. http://doi.org/10.1038/s41559-017-0082 link
12 July; speaker: X; moderators: X & x
- 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
19 July; speaker: X; moderators: X & X
- HWE and LD;
- Geographic and genomic clines;
- Admixture mapping.
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. 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.