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The effects of host quantitative genetic architecture on the gut microbiota composition of Chinook salmon (Oncorhynchus tshawytscha)

Heredity volume 131, pages 43–55 (2023)Cite this article

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Abstract

The microbiota consists of microbes living in or on an organism and has been implicated in host health and function. Environmental and host-related factors were shown to shape host microbiota composition and diversity in many fish species, but the role of host quantitative architecture across populations and among families within a population is not fully characterized. Here, Chinook salmon were used to determine if inter-population differences and additive genetic variation within populations influenced the gut microbiota diversity and composition. Specifically, hybrid stocks of Chinook salmon were created by crossing males from eight populations with eggs from an inbred line created from self-fertilized hermaphrodite salmon. Based on high-throughput sequencing of the 16S rRNA gene, significant gut microbial community diversity and composition differences were found among the hybrid stocks. Furthermore, additive genetic variance components varied among hybrid stocks, indicative of population-specific heritability patterns, suggesting the potential to select for specific gut microbiota composition for aquaculture purposes. Determining the role of host genetics in shaping their gut microbiota has important implications for predicting population responses to environmental changes and will thus impact conservation efforts for declining populations of Chinook salmon.

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Fig. 1: Map showing the stock source of the male Chinook salmon used for fertilization of eight pure and hybrid crosses used in this study.
Fig. 2: Relative abundance of the major taxa of the gut microbial community of Chinook salmon.
Fig. 3: Alpha diversity using Chao1, Shannon, and Simpson indices across all hybrid-crosses.
Fig. 4: Principal coordinate analysis (PCoA) plot with the principal coordinates (PCs) explaining the highest percent variance.
Fig. 5: Representation of unique ASVs across the hybrid-crosses used in the study, accompained by their corresponding taxonomic desgination.
Fig. 6: Identification of LEfSe Biomarkers associated with statistically significant ASVs (indicated by FDR P-values of KW sum-rank test) across all hybrid crosses and their associated effect size (represented by LDA scores).
Fig. 7: Histograms showing relative frequencies of candidate gut microbiota taxa across all eight Chinook salmon hybrid crosses.

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Acknowledgements

This study is part of a larger cooperative project that involved the dedicated work of many researchers, and for their assistance in the field, we would like to acknowledge the following: N. Bernier, J. Camaj, E. Deck, A. Forest, X. He, K. O’Hagan-Wang, J. Drown, J.W. Heath, V.A. Heath, and J. Smit. We would like to thank Yellow Island Aquaculture, Ltd. for their invaluable logistical, financial, and technical support. This study was funded by a Natural Science and Engineering Research Council (NSERC) of Canada Strategic Partnership Grant and an NSERC Discovery Grant to DDH.

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Authors and Affiliations

  1. Great Lakes Institute for Environmental Research (GLIER), University of Windsor, 401 Sunset Avenue, Windsor, Ontario, N9B 3P4, Canada

    Mubarak Ziab & Daniel D. Heath

  2. Cooperative Institute for Great Lakes Research, University of Michigan, Ann Arbor, MI, 48109, USA

    Subba Rao Chaganti

  3. Department of Integrative Biology, University of Windsor, 401 Sunset Avenue, Windsor, Ontario, N9B 3P4, Canada

    Daniel D. Heath

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  1. Mubarak Ziab
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Contributions

DDH conceived and planned the experiments. DDH and SRC carried out field work. MZ carried out the wet laboratory sample preparations and experiments. All authors contributed to selecting the models and the computational framework for the data analysis. MZ, SRC, and DDH contributed to the interpretation of the results. MZ took the lead in performing the research, analyzing data and writing the manuscript. All authors provided critical feedback and helped shape the research, analysis, and manuscript.

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Correspondence to Subba Rao Chaganti or Daniel D. Heath.

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Ziab, M., Chaganti, S.R. & Heath, D.D. The effects of host quantitative genetic architecture on the gut microbiota composition of Chinook salmon (Oncorhynchus tshawytscha). Heredity 131, 43–55 (2023). https://doi.org/10.1038/s41437-023-00620-x

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