Chromosomal rearrangements and diversification on environmental gradients
(A Marie Curie IF research project by Rui Faria within Roger Butlin's group, at Sheffield University , UK)
‘I call this experiment “replaying life’s tape.” You press the rewind button and, making sure you thoroughly erase everything that actually happened, go back to any time and place in the past . . . . Then let the tape run again to see if the repetition looks at all like the original’.
Stephan Jay Gould (1990). Wonderful Life: The Burgess Shale and the Nature of History
Background
Rocky shores usually comprise a heterogeneous environment with steep gradients of several physical factors and biological interactions, providing a natural laboratory to study local adaptation and ecological speciation. The marine gastropods of the genus Littorina, in particular L. saxatilis, have been increasingly recognised as one of the most interesting model systems to study these processes in the intertidal zone. Multiple ecotype pairs (‘Crab’ and ‘Wave’) of this species have independently diverged across the intertidal gradient of different geographic regions (Sweden, UK and Spain), as a response to similar selective pressures (crab predation and wave exposure, respectively). Despite the evidence in favour of parallel phenotypic divergence and reproductive isolation between L. saxatilis ecotypes, until the beginning of this project the main genomic regions influenced by natural selection and their distribution across the genome were largely unknown. Moreover, although the importance of chromosomal rearrangements (e.g. inversions) in adaptation and speciation is widely recognized, knowledge about their role in adaptation and speciation was still limited to some taxa and had not yet been thoroughly investigated in molluscs. Benefiting from genomic resources that became available for L. saxatilis (e.g. reference genome and linkage map), INVERTIDAL tried to fill this gap by assessing the impact of inversions on the origin of phenotypic diversity observed in L. saxatilis.
Goals
Leveraging on the potential of the L. saxatilis system and of emerging genomic tools, four main goals were defined: i) test for the presence of chromosomal rearrangements, inversions in particular, in this system; ii) evaluate the role of inversions in local adaptation, ecotype evolution and reproductive isolation between L. saxatilis ecotypes; iii) quantify the level of sharedness of inversions involved in adaptation and diversification among countries; and iv) assess the main processes contributing for a sharedness of inversions (standing genetic variation in the ancestral population that expanded versus gene flow).
Fieldwork
Pictures of Prof. Butlin team during field and lab work in Vigo Spain.
Main Results
Using Linkage disequilibrium information from a capture-targeted sequencing approach for ~380 individuals collected across a hybrid zone in Sweden (left) we identified 17 candidate inversions in this system (right)
Outreach
2018. Contribution to the Evolution Letters blog about one of our manuscripts in Littorina saxatilis: Speciation on the beach: solving the mystery of the most misidentified marine organism in the world
2018. Speciation at your beach. Activity where we presented the local L. saxatilis ecotypes in one of our sampling sites to people visiting a rocky beach in Thorwnick UK, aiming to stimulate their evolutionary thinking to explain how was local biodiversity generated.
2018. Discovery night at the Animal and Plant Sciences Department, University of Sheffield.
2017. Discovery night at the Animal and Plant Sciences Department, University of Sheffield
Publications (related with this project)
• Katherine E. Hearn, Eva L. Koch, Sean Stankowski, Roger K. Butlin1, Faria R#1, Kerstin Johannesson1, Anja M. Westram1 (2022). Differing associations between sex determination and sex-linked inversions in two ecotypes of Littorina saxatilis. Evolution Letters (in press)
1. equal contribution as last authors (listed alphabetically)
• E.L. Koch, H. Morales, J. Larsson, A.M. Westram, Faria R, A.R. Lemmon, E.M. Lemmon, K. Johannesson, R.K. Butlin (2021) Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis. Evolution Letters 5, 96-213. https://doi.org/10.1002/evl3.227
• Westram AM, Faria R, Butlin RK, Johannesson K (2021) Using replicate hybrid zones to understand the genomic basis of adaptive divergence. Molecular Ecology 30, 3797-3814.
• Westram AM, Faria R, Butlin R, Johannesson J. (2020) Inversions and evolution. In: Encyclopedia Life Sciences - eLS, John Wiley & Sons, Ltd: Chichester. https://doi.org/10.1002/9780470015902.a0029007
• Morales HE, Faria R, Johannesson K, Larsson T, Panova M, Westram AM, Butlin JK. (2019) Genomic architecture of parallel ecological divergence: beyond a single environmental contrast. Science Advances 5, eaav9963
• Faria R, Johannesson K, Butlin R, Westram A. (2019) Evolving inversions. Trends in Ecology and Evolution 34, 239-248
(authors listed alphabetically)
• Faria R#, Chaube P, Morales H, Larsson T, Lemmon AR, Lemmon EM, Rafajlovic M, Panova M, Ravinet M, Johannesson K, Westram AM, Butlin RK. (2019) Multiple chromosomal rearrangements in a hybrid zone between Littorina saxatilis ecotypes. Molecular Ecology 28, 1375-1393
• García-Souto D, Alonso S, Costa D, Eirín-López JM, Rolán-Álvarez E, Faria R, Galindo J, Pasantes JJ. (2018) Karyotype characterization of nine periwinkle species (Gastropoda, Littorinidae). Genes 9, 517.
•Westram AM, Rafajlovic M, Chaube P, Faria R, Larsson T, Panova M, Ravinet M, Blomberg A, Mehlig B, Johannesson K, Butlin R (2018) Clines on the seashore: The genomic architecture underlying rapid divergence in the face of gene flow. Evolution Letters 2, 297-309.
• Faria R#, Triant D, PerdomoSabogal A, Overduin B, Bleidorn C, Santana C, Langenberger D, Dall’Olio G, Indrischek H, Aerts J, et al. (2018) Introducing evolutionary biologists to the analysis of big data: guidelines to organize extended bioinformatics training courses. Evolution: Education and Outreach 11:8.
• Ravinet M, Faria R, Butlin RK, Galindo J, Bierne N, Rafajlovic M, Noor MAF, Mehlig B, Westram AM. Interpreting the genomic landscape of speciation: finding barriers to gene flow. Journal of Evolutionary Biology 30, 1450– 1477.
• Marques JP, Sotelo G, Larsson T, Johannesson K, Panova M, Faria R# (2017) Comparative mitogenomic analysis of three species of periwinkles: Littorina fabalis, L. obtusata and L. saxatilis. Marine Genomics 32, 41-47.
Project funded by the European Union’s Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement No 706376.