The Genomic Consistency of the Loss of Anadromy in an Arctic Fish (Salvelinus alpinus)

Sarah Salisbury* (Corresponding Author), Gregory R. McCracken, Robert Perry, Donald Keefe, Kara K. S. Layton, Tony Kess, Cameron M. Nugent, Jong S. Leong, Ian R. Bradbury, Ben F. Koop, Moira M. Ferguson, Daniel E. Ruzzante

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

4 Citations (Scopus)
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Abstract

The potentially significant genetic consequences associated with the loss of migratory capacity of diadromous fishes that have become landlocked in freshwater are poorly understood. Consistent selective pressures associated with freshwater residency may drive repeated differentiation both between allopatric landlocked and anadromous populations and within landlocked populations (resulting in sympatric morphs). Alternatively, the strong genetic drift anticipated in isolated landlocked populations could hinder consistent adaptation, limiting genetic parallelism. Understanding the degree of genetic parallelism underlying differentiation has implications for both the predictability of evolution and management practices. We employed an 87k single-nucleotide polymorphism (SNP) array to examine the genetic characteristics of landlocked and anadromous Arctic char (Salvelinus alpinus) populations from five drain-ages within Labrador, Canada. One gene was detected as an outlier between sympatric, size-differentiated morphs in each of two landlocked lakes. While no single locus differentiated all replicate pairs of landlocked and anadromous populations, several SNPs, genes, and paralogs were consistently detected as outliers in at least 70% of these pairwise comparisons. A significant C-score suggested that the amount of shared outlier SNPs across all paired landlocked and anadromous populations was greater than expected by chance. Our results indicate that despite their isolation, selection due to the loss of diadromy may drive consistent genetic responses in landlocked populations.

Original languageEnglish
Pages (from-to)617-635
Number of pages19
JournalThe American Naturalist
Volume199
Issue number5
Early online date31 Mar 2022
DOIs
Publication statusPublished - 1 May 2022

Bibliographical note

We thank our editor, J. A. Lau, associate editor K. E. Lotterhos, as well as two anonymous reviewers whose suggestions greatly improved this work. We greatly appreciate S. Avery, J. Callahan, S. Duffy, S. Hann, L. Pike, R. Solomon, and A. Walsh for their indispensable help with fieldwork. We thank Parks Canada for allowing us access to the Torngat Mountains National Park and the Nunatsiavut Government for allowing us to collect samples from their lands. We thank A. Belay at Mount Sinai Hospital for help with sequencing, A. Messmer for help with genotyping, and S. Lehnert for insightful data analysis suggestions. We also thank the Institute for Biodiversity, Ecosystem Science, and Sustainability of the Department of Environment and Conservation of the Government of Labrador and Newfoundland for funding for this project; the Natural Sciences and Engineering Research Council of Canada for the Strategic Grant STPGP 430198 and Discovery Grant awarded to D.E.R. and for the Canada Graduate Scholarships–Doctoral awarded to S.J.S.; the Killam Trust for the Level 2 Izaak awarded to S.J.S.; and the Government of Nova Scotia for the graduate scholarship awarded to S.J.S.

Data Availability Statement

Data and Code Availability
Genepop files of SNP data as well as metadata are available in the Dryad Digital Repository (https://doi.org/10.5061/dryad.cz8w9gj42; Salisbury et al. 2022). Genepop files of SNP data for Ramah, Brooklyn, and Eskar North locations have been published in the Dryad Digital Repository (https://doi.org/10.5061/dryad.cz8w9gj1f).

Online enhancements: supplemental PDF, data file. Dryad data: https://doi.org/10.5061/dryad.cz8w9gj42.

Keywords

  • SNPs
  • allopatry
  • anadromy
  • incipient speciation
  • landlocked
  • parallelism
  • PARALLEL EVOLUTION
  • GENE DIVERSITY ANALYSIS
  • CHARR
  • POPULATION-STRUCTURE
  • R PACKAGE
  • LABRADOR
  • SELECTION
  • EXPRESSION
  • ECOLOGICAL GENOMICS
  • INSIGHTS

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