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Cited by 26T-cell and B-cell ImmunologyAquaculture disease management and microbiotaGenomics and Phylogenetic Studies

Phylotranscriptomics suggests the jawed vertebrate ancestor could generate diverse helper and regulatory T cell subsets

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Redmond, Anthony K., Macqueen, Daniel J., Dooley, Helen·2018·BMC Evolutionary Biology
DOI 10.1186/s12862-018-1290-2PMC PMC6238376
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Abstract

BACKGROUND: The cartilaginous fishes diverged from other jawed vertebrates ~ 450 million years ago (mya). Despite this key evolutionary position, the only high-quality cartilaginous fish genome available is for the elephant shark (Callorhinchus milii), a chimaera whose ancestors split from the elasmobranch lineage ~ 420 mya. Initial analysis of this resource led to proposals that key components of the cartilaginous fish adaptive immune system, most notably their array of T cell subsets, was primitive compared to mammals. This proposal is at odds with the robust, antigen-specific antibody responses reported in elasmobranchs following immunization. To explore this discrepancy, we generated a multi-tissue transcriptome for small-spotted catshark (Scyliorhinus canicula), a tractable elasmobranch model for functional studies. We searched this, and other newly available sequence datasets, for CD4+ T cell subset-defining genes, aiming to confirm the presence or absence of each subset in cartilaginous fishes. RESULTS: We generated a new transcriptome based on a normalised, multi-tissue RNA pool, aiming to maximise representation of tissue-specific and lowly expressed genes. We utilized multiple transcriptomic datasets and assembly variants in phylogenetic reconstructions to unambiguously identify several T cell subset-specific molecules in cartilaginous fishes for the first time, including interleukins, interleukin receptors, and key transcription factors. Our results reveal the inability of standard phylogenetic reconstruction approaches to capture the site-specific evolutionary processes of fast-evolving immune genes but show that site-heterogeneous mixture models can adequately do so. CONCLUSIONS: Our analyses reveal that cartilaginous fishes are capable of producing a range of CD4+ T cell subsets comparable to that of mammals. Further, that the key molecules required for the differentiation and functioning of these subsets existed in the jawed vertebrate ancestor. Additionally, we highlight the importance of considering phylogenetic diversity and, where possible, utilizing multiple datasets for individual species, to accurately infer gene presence or absence at higher taxonomic levels.

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  • CAT/CATGTR offers improved resilience to long-branch attraction artefacts and is almost always better fitting than standard site-homogeneous amino acid substitution models.

    “CAT/CATGTR offers improved resilience to long-branch attraction artefacts (LBA)22 and is almost always better fitting than standard site-homogeneous amino acid substitution models (e.g. WAG)8–10,23–29.”

    From Evidence for sponges as sister to all other animals from partitioned phylogenomics with mixture models and recoding (2021) · cites this paper as [27]

    The Results section (page unavailable) finds that CAT-based models captured site-specific diversity better than standard models in the immune-gene datasets tested, suggesting greater robustness to phylogenetic error. It does not establish that CAT/CATGTR is almost always better fitting across datasets: Table 4 selects a standard model as best for most datasets listed. The paper discusses potential robustness rather than directly testing resistance to long-branch attraction. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

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Authors
Redmond, A. K., Macqueen, D. J., & Dooley, H.
Affiliations
  • University of Aberdeen (GB)
  • University of Maryland, Baltimore (US)
Corresponding author
Dooley, Helen
ORCID
Venue
BMC Evolutionary Biology
Publisher
Springer Science and Business Media LLC
Published
2018-11-15
Volume
18
Issue
1
Pages
169-169
ISSN
1471-2148 (ISSN-L)
DOI
10.1186/s12862-018-1290-2
PMC
PMC6238376
OpenAlex
W2901165813
Cited by
26
References
7
Citations by year
2025: 1 · 2024: 4 · 2023: 4 · 2022: 4 · 2021: 6 · 2020: 2 · 2019: 5
FWCI
1.40
Type
journal article
Language
en
Open access
Licence
Locations
  • BMC Evolutionary Biology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Edinburgh Research Explorer (University of Edinburgh) (publishedVersion, cc-by)
  • Aberdeen University Research Archive (Aberdeen University) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • The Royal Society (RG130789)
  • Marine Alliance for Science & Technology for Scotland (SG363)
  • University of Aberdeen CGEBM
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
  • Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Keywords
Chondrichthyes, elasmobranchs, CD4+ T cell subsets, T helper cells, regulatory T cells, adaptive immunity evolution, Scyliorhinus canicula, interleukins, interleukin receptors, transcription factors, multi-tissue transcriptome, phylotranscriptomics, elephant shark
MeSH terms
Amino Acid Sequence, Animals, Biological Evolution, Female, Fishes, Jaw, Phylogeny, Sharks, Transcription Factors, Vertebrates, Lymphocyte Subsets, Genome, T-Lymphocytes, Regulatory, Transcriptome

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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

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