Genomics of Adaptation and Speciation
summer semester 2022
2 May 2022 - 27 July 2022
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:
- 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 of the 11 sessions consists of a short lecture introducing the core concepts of that topic, followed by the presentation and discussion of current papers.
Each student will present one paper on a topic according to his/her own research interest, and will moderate the discussion of two other sessions.
However, everyone is expected to
read the selected paper and
contribute to the discussion.
The list of papers below shows examples of papers that cover the aimed topics. The student can pick a paper from this list or, preferibly, chose a similar paper from more recent literature. This paper must be approved by the organizer of the course and annouced to the class at least one week before the discussion.
Prerequisites
This seminar assumes that students are confortable with key concepts of the following disciplines:
- Evolution;
- Genetics;
- Population Genetics;
- Phylogenetics.
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.
Contact
- pereira AT bio.lmu.de
- j.wolf AT bio.lmu.de
The communication about this seminar will follow on this
SLACK workspace.
This workspace is intended to increase interaction among students.
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.
Credits
3 ECTS, 2 SWS
Timing
Every week, Monday, 8:30-10:00, CET
Location
Accordingly to the current rules of LMU, this course will take place in presence, in a seminar room to be announced soon. Yet, I have requested a special authorization to the Dean to have this seminar over Zoom. If you haven't done it already, please install Zoom
here. A zoom session might be required if the instructure is sick.
Genomics of Adaptation and Speciation
Meeting ID: 985 4404 1086
Passcode: (to be sent by email)
The password and invite link will be sent to all participants by email.
Grading
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 students can miss a maximum of 1 class for unspecific reasons, or 2 extra classes for health reasons.
The final grading is based both on the presentation (50%) and on the student's participation in the discussions throughout the entire course (50%).
Program
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
28 April, 11am room B 01.015; led by R. Pereira
Session 1: The geography and demography of divergence
9 May; speaker: Collin; moderator: Wenjie
Key concepts:
- The geography of speciation;
- Demographic parameters of speciation;
- Genomic methods in the study of geographic structure.
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. 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.
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. http://doi.org/10.1038/nrg3446
link
Barton, N. H. On the completion of speciation. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 375, 20190530–4 (2020).
link
Session 2: Genetic basis of post-zygotic intrinsic isolation
16 May; speaker: Georgios; moderator: Daniel
Key concepts:
- Post-zygotic and intrinsic mechanisms;
- Underdominance and DMIs;
- The two rules of speciation.
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. 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
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
Martin, S. H., K. S. Singh, I. J. Gordon, K. S. Omufwoko, S. Collins, I. A. Warren, H. Munby, O. Brattström, W. Traut, D. J. Martins, D. AA
. S. Smith, C. D. Jiggins, C. Bass, and R. H. Ffrench-Constant. 2020. Whole-chromosome hitchhiking driven by a male-killing endosymbiont. PLoS Biol 18:e3000610.
Pereira, R. J., Lima, T. G., Pierce-Ward, N. T., Chao, L. & Burton, R. S. Recovery from hybrid breakdown reveals a complex genetic architecture of mitonuclear incompatibilities. Molecular Ecology (2021) doi:10.1111/mec.15985.
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. 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
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�~@~S14. Springer US.
link
Session 3: Genetic basis of prezygotic isolation
23 May; speaker: Arif; moderator: Diana
Key concepts:
- Pre-mating and pre-zygotic mechanisms;
- Sexual selection and assortative mating;
- Sensory drive.
Research articles:
Turbek, S. P., M. Browne, A. S. Di Giacomo, C. Kopuchian, W. M. Hochachka, C. Estalles, D. A. Lijtmaer, P. L. Tubaro, L. F. Silveira, I. J. Lovette, R. J. Safran, S. A. Taylor, and L. Campagna. 2021. Rapid speciation via the evolution of pre-mating isolation in the Iberá Seedeater. Science 371. American Association for the Advancement of Science.
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.
Review articles:
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
Session 4: The genetic basis of adaptation
30 Mar; speaker: Sara; moderator: Serhat
Key concepts:
- Adaptation to the ecological environment;
- Divergent Natural selection and fitness trade-offs;
- Fitness landscape.
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. http://doi.org/10.1038/nature12344
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 5: The genetic basis of postzygotic extrinsic isolation
13 June; speaker: Ysaline; moderators: Arif
Key concepts:
- Underdominance in hybrids;
- Experimental evolution;
- Mesocosmos experiments.
Research articles:
Tusso, S., B. P. S. Nieuwenhuis, B. Weissensteiner, S. Immler, and J. B. W. Wolf. 2021. Experimental evolution of adaptive divergence under varying degrees of gene flow. Nature Publishing Group 5:338�~@~S349.
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
Session 6: Chromosomal speciation
20 June; speaker: Serhat; moderator: Maria L
Key concepts:
- Polyploidization;
- Chromosomal rearrangements;
- Meiotic drive.
Research articles:
Korunes, K. L., C. A. Machado, and M. A. Noor. 2021. Inversions shape the divergence of Drosophila pseudoobscura and D. persimilis on multiple timescales. Evolution, doi: 10.1111/evo.14278. John Wiley & Sons, Ltd.
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
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 7: The genomic landscape of speciation
27 Jun; speakers: Diana and Maria L; moderators: Linde and Georgios
Key concepts:
- The genic view of speciation;
- Heterogeneity of gene flow;
- Hitchhiking and linked selection.
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
Burri, R. et al. Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedulaflycatchers. Genome Research 1–11 (2015) doi:10.1101/gr.196485.115.
link
Session 8: Ecological Speciation: speciation with gene flow and divergent selection
4 Jul; speaker: Linde; moderator: Guadalupe
Key concepts:
- Ecological divergence;
- Reproductive isolation.
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. http://doi.org/10.1038/s41559-017-0082
link
Session 9: The evolutionary consequences of hybridization
11 July; speaker: Daniel; moderator: Sara
Key concepts:
- Reinforcement vs speciation reversal;
- Adaptive introgression;
- Hybrid speciation.
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. http://doi.org/10.1111/j.1420-9101.2012.02599.x
link
Session 10: Hybrid zones as windows into speciation and adaptation
18 July; speaker: Athena; moderators: Collin
Key concepts:
- HWE and LD;
- Geographic and genomic clines;
- Admixture mapping.
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. 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).
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. 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.
Session 11: Emergent topics on speciation and adaptation
25 July; speakers: Guadalupe and Wenjie; moderators: Athena and Ysaline