201. The genetic basis for ecological adaptation of the Atlantic herring revealed by genome sequencing
- Author
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Xinming Liang, Chengcheng Shi, Xun Xu, Nima Rafati, Guangyi Fan, He Zhang, Wenbin Chen, Chungang Feng, Marcel Martin, Björn Nystedt, Diana Ekman, Mats E. Pettersson, Michele Casini, Patric Jern, Nils Ryman, Kailong Ma, Carl-Johan Rubin, Xin Liu, Ulla Gustafson, Xiao Zhan, Simon Ming-Yuen Lee, Yuanyuan Fu, Jacques Dainat, Leif Andersson, Martina Blass, Marc P. Höppner, Linda Laikre, Markus Sällman Almén, Alvaro Martinez Barrio, Sangeet Lamichhaney, Arild Folkvord, Barrio AM, Lamichhaney S, Fan G, Rafati N, Pettersson M, Zhang H, Dainat J, Ekman D, Höppner M, Jern P, Martin M, Nystedt B, Liu X, Chen W, Liang X, Shi C, Fu Y, Ma K, Zhan X, Feng C, Gustafson U, Rubin CJ, Sällman Almén M, Blass M, Casini M, Folkvord A, Laikre L, Ryman N, Ming-Yuen Lee S, Xu X, and Andersson L
- Subjects
0106 biological sciences ,0301 basic medicine ,QH301-705.5 ,Science ,Adaptation, Biological ,Atlantic herring ,Genomics ,010603 evolutionary biology ,01 natural sciences ,Genome ,General Biochemistry, Genetics and Molecular Biology ,DNA sequencing ,03 medical and health sciences ,Herring ,genetic adaptation ,Animals ,Seawater ,Biology (General) ,Atlantic Ocean ,Saline Waters ,Natural selection ,General Immunology and Microbiology ,Brackish water ,biology ,Atlantic herring, adaptation, whole genome sequencing, natural selection ,Ecology ,General Neuroscience ,fungi ,Fishes ,Genetic Variation ,natural selection ,General Medicine ,biology.organism_classification ,Spawn (biology) ,Genetics, Population ,030104 developmental biology ,Genomics and Evolutionary Biology ,Medicine ,Other ,Research Article - Abstract
Ecological adaptation is of major relevance to speciation and sustainable population management, but the underlying genetic factors are typically hard to study in natural populations due to genetic differentiation caused by natural selection being confounded with genetic drift in subdivided populations. Here, we use whole genome population sequencing of Atlantic and Baltic herring to reveal the underlying genetic architecture at an unprecedented detailed resolution for both adaptation to a new niche environment and timing of reproduction. We identify almost 500 independent loci associated with a recent niche expansion from marine (Atlantic Ocean) to brackish waters (Baltic Sea), and more than 100 independent loci showing genetic differentiation between spring- and autumn-spawning populations irrespective of geographic origin. Our results show that both coding and non-coding changes contribute to adaptation. Haplotype blocks, often spanning multiple genes and maintained by selection, are associated with genetic differentiation. DOI: http://dx.doi.org/10.7554/eLife.12081.001, eLife digest The Atlantic herring is one of the most common fish in the world and has been a crucial food resource in northern Europe. One school of herring may comprise billions of fish, but previous studies had only revealed very few genetic differences in herring from different geographic regions. This was unexpected since Atlantic herring is one of the few marine species that can reproduce throughout the brackish Baltic Sea, which can be about a tenth as salty as the Atlantic Ocean. This unexpected finding could be explained in at least two different ways. Firstly, perhaps Atlantic herring are flexible enough to adapt to very different environments (i.e. high or low salinity) without much genetic change. Secondly, the previous studies only looked at a handful of sites in the Atlantic herring’s genome and so it is possible that genetic differences at other genes control this fish’s adaptation instead. Now, Martinez Barrio, Lamichhaney, Fan, Rafati et al. have sequenced entire genomes from groups of Atlantic herring and revealed hundreds of sites that are associated with adaptation to the Baltic Sea. The analysis also identified a number of genes that control when these fish reproduce by comparing herring that spawn in the autumn with those that spawn in spring. This is important because natural populations must carefully time when they reproduce to maximize the survival of their young. These new findings provide compelling evidence that changes in protein-coding genes and stretches of DNA that regulate the expression of other genes both contribute to adaptation in herrings. The analysis also clearly shows that variants of genes that contribute to adaptation were likely to evolve over time by accumulating multiple sequence changes affecting the same gene. Furthermore, these gene variants essentially form a rich “tool-box” that underlies the Atlantic herring’s adaptation to its environment, and different subpopulations of herring were found to have their own optimal sets of gene variants. For instance, autumn-spawning herring and spring-spawning herring from the Baltic Sea both have gene variants that favor adaptation to low salinity. However, autumn-spawning Baltic herring also share gene variants that favor spawning in the autumn with autumn-spawning herring from the North Sea, but not with spring-spawning Baltic herring. The next step will be to study how the 500 or so genes identified affect adaptation at the molecular level. This will likely involve experiments with other model fish such as zebrafish and sticklebacks. Finally, these new findings can be directly applied to monitor stocks of herring to make herring fisheries more sustainable. DOI: http://dx.doi.org/10.7554/eLife.12081.002
- Published
- 2016