Examining adaptive evolution of immune activity: opportunities provided by gastropods in the age of ‘omics’

Parasites threaten all free-living organisms, including molluscs. Understanding the evolution of immune defence traits in natural host populations is crucial for predicting their long-term performance under continuous infection risk. Adaptive trait evolution requires that traits are subject to selec...

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Published inPhilosophical transactions of the Royal Society of London. Series B. Biological sciences Vol. 376; no. 1825; p. 20200158
Main Authors Seppälä, Otto, Çetin, Cansu, Cereghetti, Teo, Feulner, Philine G. D., Adema, Coen M.
Format Journal Article
LanguageEnglish
Published England The Royal Society 24.05.2021
Subjects
Animals
Biological Evolution
Gastropoda - genetics
Gastropoda - immunology
Genetic Variation - immunology
Genomics
Immunity, Innate
Review
Selection, Genetic - immunology
Lymnaea stagnalis
gastropoda
immune function
immunocompetence
heritability
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Abstract Parasites threaten all free-living organisms, including molluscs. Understanding the evolution of immune defence traits in natural host populations is crucial for predicting their long-term performance under continuous infection risk. Adaptive trait evolution requires that traits are subject to selection (i.e. contribute to organismal fitness) and that they are heritable. Despite broad interest in the evolutionary ecology of immune activity in animals, the understanding of selection on and evolutionary potential of immune defence traits is far from comprehensive. For instance, empirical observations are only rarely in line with theoretical predictions of immune activity being subject to stabilizing selection. This discrepancy may be because ecoimmunological studies can typically cover only a fraction of the complexity of an animal immune system. Similarly, molecular immunology/immunogenetics studies provide a mechanistic understanding of immunity, but neglect variation that arises from natural genetic differences among individuals and from environmental conditions. Here, we review the current literature on natural selection on and evolutionary potential of immune traits in animals, signal how merging ecological immunology and genomics will strengthen evolutionary ecological research on immunity, and indicate research opportunities for molluscan gastropods for which well-established ecological understanding and/or ‘immune-omics’ resources are already available. This article is part of the Theo Murphy meeting issue ‘Molluscan genomics: broad insights and future directions for a neglected phylum’.
AbstractList Parasites threaten all free-living organisms, including molluscs. Understanding the evolution of immune defence traits in natural host populations is crucial for predicting their long-term performance under continuous infection risk. Adaptive trait evolution requires that traits are subject to selection (i.e. contribute to organismal fitness) and that they are heritable. Despite broad interest in the evolutionary ecology of immune activity in animals, the understanding of selection on and evolutionary potential of immune defence traits is far from comprehensive. For instance, empirical observations are only rarely in line with theoretical predictions of immune activity being subject to stabilizing selection. This discrepancy may be because ecoimmunological studies can typically cover only a fraction of the complexity of an animal immune system. Similarly, molecular immunology/immunogenetics studies provide a mechanistic understanding of immunity, but neglect variation that arises from natural genetic differences among individuals and from environmental conditions. Here, we review the current literature on natural selection on and evolutionary potential of immune traits in animals, signal how merging ecological immunology and genomics will strengthen evolutionary ecological research on immunity, and indicate research opportunities for molluscan gastropods for which well-established ecological understanding and/or 'immune-omics' resources are already available. This article is part of the Theo Murphy meeting issue 'Molluscan genomics: broad insights and future directions for a neglected phylum'.Parasites threaten all free-living organisms, including molluscs. Understanding the evolution of immune defence traits in natural host populations is crucial for predicting their long-term performance under continuous infection risk. Adaptive trait evolution requires that traits are subject to selection (i.e. contribute to organismal fitness) and that they are heritable. Despite broad interest in the evolutionary ecology of immune activity in animals, the understanding of selection on and evolutionary potential of immune defence traits is far from comprehensive. For instance, empirical observations are only rarely in line with theoretical predictions of immune activity being subject to stabilizing selection. This discrepancy may be because ecoimmunological studies can typically cover only a fraction of the complexity of an animal immune system. Similarly, molecular immunology/immunogenetics studies provide a mechanistic understanding of immunity, but neglect variation that arises from natural genetic differences among individuals and from environmental conditions. Here, we review the current literature on natural selection on and evolutionary potential of immune traits in animals, signal how merging ecological immunology and genomics will strengthen evolutionary ecological research on immunity, and indicate research opportunities for molluscan gastropods for which well-established ecological understanding and/or 'immune-omics' resources are already available. This article is part of the Theo Murphy meeting issue 'Molluscan genomics: broad insights and future directions for a neglected phylum'.
Parasites threaten all free-living organisms, including molluscs. Understanding the evolution of immune defence traits in natural host populations is crucial for predicting their long-term performance under continuous infection risk. Adaptive trait evolution requires that traits are subject to selection (i.e. contribute to organismal fitness) and that they are heritable. Despite broad interest in the evolutionary ecology of immune activity in animals, the understanding of selection on and evolutionary potential of immune defence traits is far from comprehensive. For instance, empirical observations are only rarely in line with theoretical predictions of immune activity being subject to stabilizing selection. This discrepancy may be because ecoimmunological studies can typically cover only a fraction of the complexity of an animal immune system. Similarly, molecular immunology/immunogenetics studies provide a mechanistic understanding of immunity, but neglect variation that arises from natural genetic differences among individuals and from environmental conditions. Here, we review the current literature on natural selection on and evolutionary potential of immune traits in animals, signal how merging ecological immunology and genomics will strengthen evolutionary ecological research on immunity, and indicate research opportunities for molluscan gastropods for which well-established ecological understanding and/or 'immune-omics' resources are already available. This article is part of the Theo Murphy meeting issue 'Molluscan genomics: broad insights and future directions for a neglected phylum'.
Parasites threaten all free-living organisms, including molluscs. Understanding the evolution of immune defence traits in natural host populations is crucial for predicting their long-term performance under continuous infection risk. Adaptive trait evolution requires that traits are subject to selection (i.e. contribute to organismal fitness) and that they are heritable. Despite broad interest in the evolutionary ecology of immune activity in animals, the understanding of selection on and evolutionary potential of immune defence traits is far from comprehensive. For instance, empirical observations are only rarely in line with theoretical predictions of immune activity being subject to stabilizing selection. This discrepancy may be because ecoimmunological studies can typically cover only a fraction of the complexity of an animal immune system. Similarly, molecular immunology/immunogenetics studies provide a mechanistic understanding of immunity, but neglect variation that arises from natural genetic differences among individuals and from environmental conditions. Here, we review the current literature on natural selection on and evolutionary potential of immune traits in animals, signal how merging ecological immunology and genomics will strengthen evolutionary ecological research on immunity, and indicate research opportunities for molluscan gastropods for which well-established ecological understanding and/or ‘immune-omics’ resources are already available. This article is part of the Theo Murphy meeting issue ‘Molluscan genomics: broad insights and future directions for a neglected phylum’.
Author Cereghetti, Teo
Seppälä, Otto
Çetin, Cansu
Adema, Coen M.
Feulner, Philine G. D.
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  givenname: Philine G. D.
  surname: Feulner
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  surname: Adema
  fullname: Adema, Coen M.
  organization: Department of Biology, Center for Evolutionary and Theoretical Immunology, University of New Mexico, Albuquerque, NM, USA
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gastropoda
immune function
immunocompetence
heritability
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Snippet Parasites threaten all free-living organisms, including molluscs. Understanding the evolution of immune defence traits in natural host populations is crucial...
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SubjectTerms Animals
Biological Evolution
Gastropoda - genetics
Gastropoda - immunology
Genetic Variation - immunology
Genomics
Immunity, Innate
Review
Selection, Genetic - immunology
Title Examining adaptive evolution of immune activity: opportunities provided by gastropods in the age of ‘omics’
URI https://www.ncbi.nlm.nih.gov/pubmed/33813886
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https://pubmed.ncbi.nlm.nih.gov/PMC8059600
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