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Holosteans contextualize the role of the teleost genome duplication in promoting the rise of evolutionary novelties in the ray-finned fish innate immune system

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Abstract

Over 99% of ray-finned fishes (Actinopterygii) are teleosts, a clade that comprises half of all living vertebrate species that have diversified across virtually all fresh and saltwater ecosystems. This ecological breadth raises the question of how the immunogenetic diversity required to persist under heterogeneous pathogen pressures evolved. The teleost genome duplication (TGD) has been hypothesized as the evolutionary event that provided the substrate for rapid genomic evolution and innovation. However, studies of putative teleost-specific innate immune receptors have been largely limited to comparisons either among teleosts or between teleosts and distantly related vertebrate clades such as tetrapods. Here we describe and characterize the receptor diversity of two clustered innate immune gene families in the teleost sister lineage: Holostei (bowfin and gars). Using genomic and transcriptomic data, we provide a detailed investigation of the phylogenetic history and conserved synteny of gene clusters encoding diverse immunoglobulin domain-containing proteins (DICPs) and novel immune-type receptors (NITRs). These data demonstrate an ancient linkage of DICPs to the major histocompatibility complex (MHC) and reveal an evolutionary origin of NITR variable-joining (VJ) exons that predate the TGD by at least 50 million years. Further characterizing the receptor diversity of Holostean DICPs and NITRs illuminates a sequence diversity that rivals the diversity of these innate immune receptor families in many teleosts. Taken together, our findings provide important historical context for the evolution of these gene families that challenge prevailing expectations concerning the consequences of the TGD during actinopterygiian evolution.

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Data availability

All data used in this study are publicly available on NCBI, Ensembl, or the PhyloFish database (http://phylofish.sigenae.org/). Publicly available bowfin sequences accessed during this study are also provided as full length fasta formatted sequences and partitioned sequences linked to the delimitations of domains (e.g., NITR-I, NITR-V) in the Supplementary Materials.

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Acknowledgements

We thank Thomas Near (Yale University) for helpful discussions about bowfin biology and the consequences of the teleost genome duplication and Madhusudhan Gundappa (@fish_lines) for illustrations of bowfin and spotted gar.

Funding

This research was supported, in part, by grants from the National Science Foundation (IOS-1755242 to AD and IOS-1755330 to JAY), a grant from the Triangle Center for Evolutionary Medicine (TriCEM) to AD and JAY, and funding from the National Institutes of Health (R01OD011116 to IB).

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Authors and Affiliations

  1. Department of Bioinformatics and Genomics, University of North Carolina At Charlotte, Charlotte, NC, USA

    Alex Dornburg & Katerina Zapfe

  2. Department of Molecular Biomedical Sciences, North Carolina State University, Raleigh, NC, USA

    Dustin J. Wcisel & Jeffrey A. Yoder

  3. North Carolina Museum of Natural Sciences, Raleigh, NC, USA

    Emma Ferraro & Lindsay Roupe-Abrams

  4. Department of Integrative Biology, Michigan State University, East Lansing, MI, USA

    Andrew W. Thompson & Ingo Braasch

  5. Ecology, Evolution & Behavior Program, Michigan State University, East Lansing, MI, USA

    Andrew W. Thompson

  6. Department of Evolutionary Studies of Biosystems, SOKENDAI (The Graduate University for Advanced Studies), Hayama, Japan

    Tatsuya Ota

  7. Comparative Medicine Institute, North Carolina State University, Raleigh, NC, USA

    Jeffrey A. Yoder

  8. Center for Human Health and the Environment, North Carolina State University, Raleigh, NC, USA

    Jeffrey A. Yoder

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  1. Alex Dornburg
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Contributions

AD and JAY conceived of and designed the study. EF, KZ, AWT, IB, LRA, TO, DJW, and AWT assembled sequence data. AD, JAY, TO, EF, LRA, KZ, AWT, IB, and DJW analyzed the data. AD and JAY wrote the first draft of the manuscript. All authors contributed to the writing of the final manuscript.

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Correspondence to Alex Dornburg or Jeffrey A. Yoder.

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Dornburg, A., Wcisel, D.J., Zapfe, K. et al. Holosteans contextualize the role of the teleost genome duplication in promoting the rise of evolutionary novelties in the ray-finned fish innate immune system. Immunogenetics 73, 479–497 (2021). https://doi.org/10.1007/s00251-021-01225-6

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