Westram, Anja MISTA ; Rafajlović, Marina; Chaube, Pragya; Faria, Rui; Larsson, Tomas; Panova, Marina; Ravinet, Mark; Blomberg, Anders; Mehlig, Bernhard; Johannesson, Kerstin; Butlin, Roger
Adaptive divergence and speciation may happen despite opposition by gene flow. Identifying the genomic basis underlying divergence with gene flow is a major task in evolutionary genomics. Most approaches (e.g., outlier scans) focus on genomic regions of high differentiation. However, not all genomic architectures potentially underlying divergence are expected to show extreme differentiation. Here, we develop an approach that combines hybrid zone analysis (i.e., focuses on spatial patterns of allele frequency change) with system-specific simulations to identify loci inconsistent with neutral evolution. We apply this to a genome-wide SNP set from an ideally suited study organism, the intertidal snail Littorina saxatilis, which shows primary divergence between ecotypes associated with different shore habitats. We detect many SNPs with clinal patterns, most of which are consistent with neutrality. Among non-neutral SNPs, most are located within three large putative inversions differentiating ecotypes. Many non-neutral SNPs show relatively low levels of differentiation. We discuss potential reasons for this pattern, including loose linkage to selected variants, polygenic adaptation and a component of balancing selection within populations (which may be expected for inversions). Our work is in line with theory predicting a role for inversions in divergence, and emphasizes that genomic regions contributing to divergence may not always be accessible with methods purely based on allele frequency differences. These conclusions call for approaches that take spatial patterns of allele frequency change into account in other systems.
We are very grateful to people who helped with fieldwork, snail processing, and DNA extractions, particularly Laura Brettell, Mårten Duvetorp, Juan Galindo, Anne-Lise Liabot and Irena Senčić. We would also like to thank Magnus Alm Rosenblad and Mats Töpel for their contribution to assembling the Littorina saxatilis genome, Carl André, Pasi Rastas, and Romain Villoutreix for discussion, and two anonymous reviewers for their helpful comments on the manuscript. We are grateful to RapidGenomics for library preparation and sequencing. We thank the Natural Environment Research Council, the European Research Council and the Swedish Research Councils VR and Formas (Linnaeus grant to the Centre for Marine Evolutionary Biology and Tage Erlander Guest Professorship) for funding. P.C. was funded by the University of Sheffield Vice-chancellor's India scholarship. R.F. is funded by the European Union's Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement no. 706376. M. Raf. was supported by the Adlerbert Research Foundation.
Westram AM, Rafajlović M, Chaube P, et al. Clines on the seashore: The genomic architecture underlying rapid divergence in the face of gene flow. Evolution Letters. 2018;2(4):297-309. doi:10.1002/evl3.74
Westram, A. M., Rafajlović, M., Chaube, P., Faria, R., Larsson, T., Panova, M., … Butlin, R. (2018). Clines on the seashore: The genomic architecture underlying rapid divergence in the face of gene flow. Evolution Letters. Wiley. https://doi.org/10.1002/evl3.74
Westram, Anja M, Marina Rafajlović, Pragya Chaube, Rui Faria, Tomas Larsson, Marina Panova, Mark Ravinet, et al. “Clines on the Seashore: The Genomic Architecture Underlying Rapid Divergence in the Face of Gene Flow.” Evolution Letters. Wiley, 2018. https://doi.org/10.1002/evl3.74.
A. M. Westram et al., “Clines on the seashore: The genomic architecture underlying rapid divergence in the face of gene flow,” Evolution Letters, vol. 2, no. 4. Wiley, pp. 297–309, 2018.
Westram AM, Rafajlović 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(4), 297–309.
Westram, Anja M., et al. “Clines on the Seashore: The Genomic Architecture Underlying Rapid Divergence in the Face of Gene Flow.” Evolution Letters, vol. 2, no. 4, Wiley, 2018, pp. 297–309, doi:10.1002/evl3.74.
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