Interview with the author: Chromosome polymorphisms track trans‐Atlantic divergence and secondary contact in Atlantic salmon

Populations of salmon in the eastern and western Atlantic ocean diverged more than 600,000 years ago. They survived in isolated refugia during the glacial maxima, and later expanded their ranges. When colonizing northern areas after the retreat of the glaciers, eastern and western populations came back into contact. Lehnert et al. studied the genome-wide consequences of secondary contact, with a particular focus on regions of the genome near chromosome rearrangements. One chromosomal rearrangement shows evidence of European ancestry in North American individuals, suggesting that secondary contact occurred during the colonization of northern part of the species’ range. However, another chromosomal rearrangement showed a contrasting pattern: evidence of a derived North American chromosome fusion. In both rearrangements, the authors find evidence of natural selection, suggesting that chromosomal rearrangements may serve an adaptive role in salmon. Below, we go behind the scenes with Dr. Sarah Lehnert, currently Postdoctoral Fellow at Fisheries and Oceans Canada, to learn more about the findings of the paper and the work that went into this research. You can find the associated paper here: https://onlinelibrary.wiley.com/doi/10.1111/mec.15065

Atlantic salmon (Salmo salar) Gaspe Peninsulsa, Quebec, Canada. October 2017.
Photo credit: Nick Hawkins

What led to your interest in this topic / what was the motivation for this study? 
Atlantic salmon populations across the North Atlantic have been declining in recent decades. Our lab is interested in better characterizing genetic structure and diversity of salmon populations in North America to improve conservation and management. When we started this project, I was interested in identifying genomic regions associated with large-scale differences among individuals across populations. We were particularly interested in identifying genomic variation associated with historical secondary contact (~10,000 years ago) between European and North American Atlantic salmon. These groups diverged >600,000 years ago and mitochondrial evidence suggest contact has occurred but genomic evidence is limited. For our project, we investigated if and how secondary contact has influenced contemporary population structure and considered the implications for salmon management and conservation.

What led to your interest in this topic / what was the motivation for this study? 
Atlantic salmon populations across the North Atlantic have been declining in recent decades. Our lab is interested in better characterizing genetic structure and diversity of salmon populations in North America to improve conservation and management. When we started this project, I was interested in identifying genomic regions associated with large-scale differences among individuals across populations. We were particularly interested in identifying genomic variation associated with historical secondary contact (~10,000 years ago) between European and North American Atlantic salmon. These groups diverged >600,000 years ago and mitochondrial evidence suggest contact has occurred but genomic evidence is limited. For our project, we investigated if and how secondary contact has influenced contemporary population structure and considered the implications for salmon management and conservation.

What difficulties did you run into along the way? 
We first investigated genomic regions that showed large-scale inter-individual variation across North American populations. One difficulty was that many approaches are designed to investigate population level differences rather than individual differences. By using methods that allow the investigation of individual variation in addition to population level differences, this enabled us to resolve karyotypic differences within populations that may have been missed by other analyses. This led us to identify variation in two chromosomal rearrangements (translocation and fusion). The next difficulty was trying to understand why these rearrangements show different geographic structure and different levels of diversity. Through additional analyses and by incorporating European samples, we determined that variation in each chromosomal rearrangement evolved through different mechanisms.

What is the biggest or most surprising finding from this study? 
Our work suggests that Atlantic salmon within rivers in North America have different numbers of chromosomes. This corroborates earlier karyotyping studies in a few rivers, but our study is the first to show genomic evidence of chromosome variation at the continental scale and our work also identifies which chromosomes are responsible for this variation and how this variation came to be. What was most exciting to me was being able to use SNP data to understand the different evolutionary histories of these chromosomal rearrangements. Our study revealed an interesting story as we found that variation in one chromosomal rearrangement was introduced from European salmon coming to North America whereas variation in the other chromosomal rearrangement evolved within North America independently.

Moving forward, what are the next steps for this research?
We found that chromosome variation exists in North American Atlantic salmon and our next step is to further understand why this variation exists. Our study suggested that these regions were under selection and thus we hypothesize that chromosome variation may relate to life history diversity or local adaptation. In other salmonids, chromosomal rearrangements have been associated with important traits such as migration phenotype. The fusion identified in our study has recently been suggested to be associated with precipitation within a single river system. Therefore, we plan to sample a wider range of populations in North America and examine environmental and life history variation associated with karyotype differences at a continental scale

What would your message be for students about to start their first research projects in this topic? 
My advice would be to read new papers but also old papers on your study system. By reading older papers, I learned that some earlier studies had identified karyotype variation within and between Atlantic salmon populations. This was not often discussed in more recent population genetic studies that focused on microsatellites or SNPs. Reading older karyotyping studies on Atlantic salmon in conjunction with new papers (reviews) on chromosomal variation helped me formulate hypotheses and interpret the patterns we were finding in the genome. It can be easy to focus on recent literature, but older work can often help shed a different light on unresolved questions.

What have you learned about science over the course of this project? 
Through this work, I have learned that variation in chromosome structure is prevalent across taxa. Dobzhansky highlighted this as early as the 1930s but the field of genetics moved away from this earlier focus on chromosome level differences. Only recently have we started to appreciate how important chromosomal structure variation may be to adaptation. Within the last decade, chromosomal inversions have been associated with complex phenotypes such as mating tactics in the ruff and migration strategy in species like cod, warblers, and rainbow trout. Although inversions have recently garnered a lot of attention, our study also highlights the importance of variation in chromosomal fusions and translocations, which have not been identified within many animal populations to date.

Describe the significance of this research for the general scientific community in one sentence.
Our research demonstrates variability in chromosomal translocations and fusions within populations of a vertebrate species that may play a role in adaptation and highlights how historical events (glaciations and secondary contact) can influence contemporary diversity.

Describe the significance of this research for your scientific community in one sentence. 
Our work suggests that differences in chromosome number are prevalent in Atlantic salmon populations and this potentially adaptive variation can provide information about different evolutionary events, highlighting the importance of such genetic variation to salmonid populations management.

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