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Understanding the evolution of immune genes in jawed vertebrates

Vinkler, Michal, Fiddaman, Steven R., Těšický, Martin, O'Connor, Emily A., Savage, Anna E., Lenz, Tobias L., Smith, Adrian L., Kaufman, Jim, Bolnick, Daniel I., Davies, Charli S., Dedić, Neira, Flies, Andrew S., Samblás, M. Mercedes Gómez, Henschen, Amberleigh E., Novák, Karel, Palomar, Gemma, Raven, Nynke, Samaké, Kalifa, Slade, Joel, Veetil, Nithya Kuttiyarthu, Voukali, Eleni, Höglund, Jacob, Richardson, David S., Westerdahl, Helena·2023·Journal of Evolutionary Biology
DOI 10.1111/jeb.14181PMC PMC10247546
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Abstract

Driven by co-evolution with pathogens, host immunity continuously adapts to optimize defence against pathogens within a given environment. Recent advances in genetics, genomics and transcriptomics have enabled a more detailed investigation into how immunogenetic variation shapes the diversity of immune responses seen across domestic and wild animal species. However, a deeper understanding of the diverse molecular mechanisms that shape immunity within and among species is still needed to gain insight into—and generate evolutionary hypotheses on—the ultimate drivers of immunological differences. Here, we discuss current advances in our understanding of molecular evolution underpinning jawed vertebrate immunity. First, we introduce the immunome concept, a framework for characterizing genes involved in immune defence from a comparative perspective, then we outline how immune genes of interest can be identified. Second, we focus on how different selection modes are observed acting across groups of immune genes and propose hypotheses to explain these differences. We then provide an overview of the approaches used so far to study the evolutionary heterogeneity of immune genes on macro and microevolutionary scales. Finally, we discuss some of the current evidence as to how specific pathogens affect the evolution of different groups of immune genes. This review results from the collective discussion on the current key challenges in evolutionary immunology conducted at the ESEB 2021 Online Satellite Symposium: Molecular evolution of the vertebrate immune system, from the lab to natural populations. Abstract Reviewing current advances in our understanding of molecular evolution underpinning vertebrate immunity, we propose hypotheses to explain differences in selection modes across immune genes and discuss supporting evidence.

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FIGURE 1 A proposed system for the hierarchical classification of immune genes. A gene considered relevant to the immune system will fall into one of three categories: (i) the core immunome, (ii) the peripheral immunome, and (iii) non‐immune resistance genes. Core immunome components are unequivocally (and in many cases, exclusively) related to immune function. Peripheral immune genes contribute to aspects of the immune response, despite also having additional roles in the physiological functioning of other body systems. Non‐immune resistance genes (NIRGs) are genes that do not form part of the immune system but can functionally confer resistance to a pathogen and thus are important to consider as part of an immune phenotype. Examples of such genes (or gene classes/families) are given in each compartment. The dashed line between core and peripheral immune components indicates that there is likely a continuum of genes whose function ranges from exclusively immune to almost entirely for another physiological function, and that some genes may lie ambiguously between the two categories. Abbreviations: ACE‐2, angiotensin converting enzyme‐2; MHC, major histocompatibility complex; AMPs, anti‐microbial peptides; TCR, T‐cell receptor; BCR, B‐cell receptor; IFNs, interferons; PRRs, pattern‐recognition receptors.
FIGURE 1 A proposed system for the hierarchical classification of immune genes. A gene considered relevant to the immune system will fall into one of three categories: (i) the core immunome, (ii) the peripheral immunome, and (iii) non‐immune resistance genes. Core immunome components are unequivocally (and in many cases, exclusively) related to immune function. Peripheral immune genes contribute to aspects of the immune response, despite also having additional roles in the physiological functioning of other body systems. Non‐immune resistance genes (NIRGs) are genes that do not form part of the immune system but can functionally confer resistance to a pathogen and thus are important to consider as part of an immune phenotype. Examples of such genes (or gene classes/families) are given in each compartment. The dashed line between core and peripheral immune components indicates that there is likely a continuum of genes whose function ranges from exclusively immune to almost entirely for another physiological function, and that some genes may lie ambiguously between the two categories. Abbreviations: ACE‐2, angiotensin converting enzyme‐2; MHC, major histocompatibility complex; AMPs, anti‐microbial peptides; TCR, T‐cell receptor; BCR, B‐cell receptor; IFNs, interferons; PRRs, pattern‐recognition receptors.CC BY · PubMed Central
FIGURE 2 Differences in selective pressures in different immune gene sets. Current evidence suggests that groups of immune genes tend to have differing levels of genetic variation as well as strength of selection acting on them. We predict increased pathogen‐mediated natural selection (range from yellow = low to red = high) that drives increased interspecific genetic variation and intraspecific population polymorphism especially in the genes that encode proteins: (I) directly involved with pathogen structures rather than host‐self molecules; (II) involved with a high number of structurally distinct ligands rather than with structurally limited interactions; (III) expressed on the cell‐surface rather than to cytoplasm and (IV) with inducible rather than constitutive expression.
FIGURE 2 Differences in selective pressures in different immune gene sets. Current evidence suggests that groups of immune genes tend to have differing levels of genetic variation as well as strength of selection acting on them. We predict increased pathogen‐mediated natural selection (range from yellow = low to red = high) that drives increased interspecific genetic variation and intraspecific population polymorphism especially in the genes that encode proteins: (I) directly involved with pathogen structures rather than host‐self molecules; (II) involved with a high number of structurally distinct ligands rather than with structurally limited interactions; (III) expressed on the cell‐surface rather than to cytoplasm and (IV) with inducible rather than constitutive expression.CC BY · PubMed Central

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Metadata

Authors
Vinkler, M., Fiddaman, S. R., Těšický, M., O'Connor, E. A., Savage, A. E., Lenz, T. L., Smith, A. L., Kaufman, J., Bolnick, D. I., Davies, C. S., Dedić, N., Flies, A. S., Samblás, M. M. G., Henschen, A. E., Novák, K., Palomar, G., Raven, N., Samaké, K., Slade, J., Veetil, N. K., Voukali, E., Höglund, J., Richardson, D. S., & Westerdahl, H.
Affiliations
  • Department of Zoology Faculty of Science Charles University Prague Czech Republic
  • Department of Biology University of Oxford Oxford UK
  • Department of Biology Lund University Lund Sweden
  • Department of Biology University of Central Florida Florida Orlando USA
  • Research Unit for Evolutionary Immunogenomics Department of Biology University of Hamburg Hamburg Germany
  • Department of Veterinary Medicine University of Cambridge Cambridge UK
  • Department of Ecology and Evolutionary Biology University of Connecticut Storrs Connecticut USA
  • School of Biological Sciences University of East Anglia Norwich UK
  • Department of Botany and Zoology Masaryk University Brno Czech Republic
  • Menzies Institute for Medical Research University of Tasmania Hobart Tasmania Australia
  • Department of Parasitology University of Granada Granada Spain
  • Department of Biological Sciences University of Memphis Memphis Tennessee USA
  • Department of Genetics and Breeding Institute of Animal Science Prague Uhříněves Czech Republic
  • Faculty of Biology Institute of Environmental Sciences Jagiellonian University Kraków Poland
  • Department of Science Engineering and Build Environment Deakin University Victoria Waurn Ponds Australia
  • Department of Genetics and Microbiology Faculty of Science Charles University Prague Czech Republic
  • Department of Biology California State University Fresno California USA
  • Department of Ecology and Genetics Uppsala Universitet Uppsala Sweden
ORCID
Venue
Journal of Evolutionary Biology
Publisher
Oxford University Press (OUP)
Published
2023-06-01
Volume
36
Issue
6
Pages
847-873
ISSN
  • 1420-9101
  • 1010-061X
DOI
10.1111/jeb.14181
PMC
PMC10247546
Cited by
55
References
11
Language
en
Licence
Funders
  • Biotechnology and Biological Sciences Research Council (BB/K004468/1, BB/M011224/1, BB/N023803/1, BB/V000756/1)
  • Department for Environment, Food and Rural Affairs, UK Government (OD0221)
  • Deutsche Forschungsgemeinschaft (437857095)
  • Grantová Agentura České Republiky (19-20152Y, 19‐20152Y)
  • Grantová Agentura, Univerzita Karlova (646119)
  • H2020 European Research Council (ERC-2019-StG-853272-PALAEOFARM, ERC‐2019‐StG‐853272‐PALAEOFARM)
  • John Fell Fund, University of Oxford (0005172)
  • Ministerstvo Školství, Mládeže a Tělovýchovy (SVV 260684/2023)
  • Ministerstvo Zemědělství (MZE-RO0723, MZE‐RO0723)
  • National Institutes of Health (1R01AI123659-01A1, 1R01AI123659‐01A1)
  • Univerzita Karlova v Praze (START/SCI/113 with reg. no. CZ.02.2.69/0.0/0.0/19_)
  • Vetenskapsrådet (2020-04285, 2020‐04285)

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