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Small-scale intraspecific patterns of adaptive immunogenetic polymorphisms and neutral variation in Lake Superior lake trout

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Abstract

Many fishes express high levels of intraspecific variability, often linked to resource partitioning. Several studies show that a species’ evolutionary trajectory of adaptive divergence can undergo reversals caused by changes in its environment. Such a reversal in neutral genetic and morphological variation among lake trout Salvelinus namaycush ecomorphs appears to be underway in Lake Superior. However, a water depth gradient in neutral genetic divergence was found to be associated with intraspecific diversity in the lake. To investigate patterns of adaptive immunogenetic variation among lake trout ecomorphs, we used Illumina high-throughput sequencing. The population’s genetic structure of the major histocompatibility complex (MHC Class IIβ exon 2) and 18 microsatellite loci were compared to disentangle neutral and selective processes at a small geographic scale. Both MHC and microsatellite variation were partitioned more by water depth stratum than by ecomorph. Several metrics showed strong clustering by water depth in MHC alleles, but not microsatellites. We report a 75% increase in the number of MHC alleles shared between the predominant shallow and deep water ecomorphs since a previous lake trout MHC study at the same locale (c. 1990s data). This result is consistent with the reverse speciation hypothesis, although adaptive MHC polymorphisms persist along an ecological gradient. Finally, results suggested that the lake trout have multiple copies of the MHC II locus consistent with a historic genomic duplication event. Our findings indicated that conservation approaches for this species could focus on managing various ecological habitats by depth, in addition to regulating the fisheries specific to ecomorphs.

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Acknowledgements

Two anonymous reviewers and the handling editor of Immunogenetics provided helpful comments on this manuscript. M. McBride, L. Anstey, and C. Angelidis (Marine Gene Probe lab, Dalhousie University) helped with microsatellite genotyping work at various stages of the project. We thank S. Sivertson, E. Strom, and B. Strom for their hospitality at Washington and Barnam Islands, adjacent to Isle Royale. J. Pyatskowit, C.R. Bronte, M.S. Zimmerman, H.R. Quinlan, and J.D. Glase provided cheerful and able assistance with the Isle Royale fieldwork. This research was funded by the Great Lakes Fishery Commission grant 2005_BEN_44001.

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  1. Marine Gene Probe Lab, Department of Biology, Dalhousie University, 1355 Oxford Street, PO Box 15000, Halifax, NS, B3H 4J1, Canada

    Shauna M. Baillie, Riley R. Hemstock & Paul Bentzen

  2. Great Lakes Fishery Commission, 2100 Commonwealth Boulevard, Ann Arbor, MI, 48105, USA

    Andrew M. Muir

  3. Department of Fisheries and Wildlife, Center for Systems Integration and Sustainability, Michigan State University, East Lansing, MI, 48824, USA

    Charles C. Krueger

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  1. Shauna M. Baillie
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S.M.B. wrote the article based on R.H.’s Honours Thesis work, which focused on MHC diversity among lake trout at Isle Royale, Lake Superior. MHC labwork and genotyping was performed by S.M.B. and R.H. Microsatellite labwork and genotyping was performed by S.M.B. at the latter stages of the project. S.M.B., P.B., C.C.K., and A.M.M. designed the study and managed the project. C.C.K. and A.M.M. obtained funding from the Great Lakes Fishery Commission and performed fieldwork to collect and process contemporary samples. All authors read, edited, and approved this version of the manuscript.

Corresponding author

Correspondence to Shauna M. Baillie.

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Funding

This research was funded by the Great Lakes Fishery Commission grant 2005_BEN_44001.

Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent

Informed consent was obtained from all individual participants included in the study. Additional informed consent was obtained from all individual participants for whom identifying information is included in this article.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Sampling and handling of fish was in accordance with the guidelines for the care and use of fishes by the American Fisheries Society (http://fisheries.org/docs/wp/Guidelines-for-Use-of-Fishes.pdf).

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Baillie, S.M., Hemstock, R.R., Muir, A.M. et al. Small-scale intraspecific patterns of adaptive immunogenetic polymorphisms and neutral variation in Lake Superior lake trout. Immunogenetics 70, 53–66 (2018). https://doi.org/10.1007/s00251-017-0996-4

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