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Evolution of male pregnancy associated with remodeling of canonical vertebrate immunity in seahorses and pipefishes
A fundamental problem for the evolution of pregnancy, the most specialized form of parental investment among vertebrates, is the rejection of the nonself-embryo. Mammals achieve immunological tolerance by down-regulating both major histocompatibility complex pathways (MHC I and II). Although pregnan...
Autores principales: | , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7196912/ https://www.ncbi.nlm.nih.gov/pubmed/32284407 http://dx.doi.org/10.1073/pnas.1916251117 |
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author | Roth, Olivia Solbakken, Monica Hongrø Tørresen, Ole Kristian Bayer, Till Matschiner, Michael Baalsrud, Helle Tessand Hoff, Siv Nam Khang Brieuc, Marine Servane Ono Haase, David Hanel, Reinhold Reusch, Thorsten B. H. Jentoft, Sissel |
author_facet | Roth, Olivia Solbakken, Monica Hongrø Tørresen, Ole Kristian Bayer, Till Matschiner, Michael Baalsrud, Helle Tessand Hoff, Siv Nam Khang Brieuc, Marine Servane Ono Haase, David Hanel, Reinhold Reusch, Thorsten B. H. Jentoft, Sissel |
author_sort | Roth, Olivia |
collection | PubMed |
description | A fundamental problem for the evolution of pregnancy, the most specialized form of parental investment among vertebrates, is the rejection of the nonself-embryo. Mammals achieve immunological tolerance by down-regulating both major histocompatibility complex pathways (MHC I and II). Although pregnancy has evolved multiple times independently among vertebrates, knowledge of associated immune system adjustments is restricted to mammals. All of them (except monotremata) display full internal pregnancy, making evolutionary reconstructions within the class mammalia meaningless. Here, we study the seahorse and pipefish family (syngnathids) that have evolved male pregnancy across a gradient from external oviparity to internal gestation. We assess how immunological tolerance is achieved by reconstruction of the immune gene repertoire in a comprehensive sample of 12 seahorse and pipefish genomes along the “male pregnancy” gradient together with expression patterns of key immune and pregnancy genes in reproductive tissues. We found that the evolution of pregnancy coincided with a modification of the adaptive immune system. Divergent genomic rearrangements of the MHC II pathway among fully pregnant species were identified in both genera of the syngnathids: The pipefishes (Syngnathus) displayed loss of several genes of the MHC II pathway while seahorses (Hippocampus) featured a highly divergent invariant chain (CD74). Our findings suggest that a trade-off between immunological tolerance and embryo rejection accompanied the evolution of unique male pregnancy. That pipefishes survive in an ocean of microbes without one arm of the adaptive immune defense suggests a high degree of immunological flexibility among vertebrates, which may advance our understanding of immune-deficiency diseases. |
format | Online Article Text |
id | pubmed-7196912 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-71969122020-05-06 Evolution of male pregnancy associated with remodeling of canonical vertebrate immunity in seahorses and pipefishes Roth, Olivia Solbakken, Monica Hongrø Tørresen, Ole Kristian Bayer, Till Matschiner, Michael Baalsrud, Helle Tessand Hoff, Siv Nam Khang Brieuc, Marine Servane Ono Haase, David Hanel, Reinhold Reusch, Thorsten B. H. Jentoft, Sissel Proc Natl Acad Sci U S A Biological Sciences A fundamental problem for the evolution of pregnancy, the most specialized form of parental investment among vertebrates, is the rejection of the nonself-embryo. Mammals achieve immunological tolerance by down-regulating both major histocompatibility complex pathways (MHC I and II). Although pregnancy has evolved multiple times independently among vertebrates, knowledge of associated immune system adjustments is restricted to mammals. All of them (except monotremata) display full internal pregnancy, making evolutionary reconstructions within the class mammalia meaningless. Here, we study the seahorse and pipefish family (syngnathids) that have evolved male pregnancy across a gradient from external oviparity to internal gestation. We assess how immunological tolerance is achieved by reconstruction of the immune gene repertoire in a comprehensive sample of 12 seahorse and pipefish genomes along the “male pregnancy” gradient together with expression patterns of key immune and pregnancy genes in reproductive tissues. We found that the evolution of pregnancy coincided with a modification of the adaptive immune system. Divergent genomic rearrangements of the MHC II pathway among fully pregnant species were identified in both genera of the syngnathids: The pipefishes (Syngnathus) displayed loss of several genes of the MHC II pathway while seahorses (Hippocampus) featured a highly divergent invariant chain (CD74). Our findings suggest that a trade-off between immunological tolerance and embryo rejection accompanied the evolution of unique male pregnancy. That pipefishes survive in an ocean of microbes without one arm of the adaptive immune defense suggests a high degree of immunological flexibility among vertebrates, which may advance our understanding of immune-deficiency diseases. National Academy of Sciences 2020-04-28 2020-04-13 /pmc/articles/PMC7196912/ /pubmed/32284407 http://dx.doi.org/10.1073/pnas.1916251117 Text en Copyright © 2020 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | Biological Sciences Roth, Olivia Solbakken, Monica Hongrø Tørresen, Ole Kristian Bayer, Till Matschiner, Michael Baalsrud, Helle Tessand Hoff, Siv Nam Khang Brieuc, Marine Servane Ono Haase, David Hanel, Reinhold Reusch, Thorsten B. H. Jentoft, Sissel Evolution of male pregnancy associated with remodeling of canonical vertebrate immunity in seahorses and pipefishes |
title | Evolution of male pregnancy associated with remodeling of canonical vertebrate immunity in seahorses and pipefishes |
title_full | Evolution of male pregnancy associated with remodeling of canonical vertebrate immunity in seahorses and pipefishes |
title_fullStr | Evolution of male pregnancy associated with remodeling of canonical vertebrate immunity in seahorses and pipefishes |
title_full_unstemmed | Evolution of male pregnancy associated with remodeling of canonical vertebrate immunity in seahorses and pipefishes |
title_short | Evolution of male pregnancy associated with remodeling of canonical vertebrate immunity in seahorses and pipefishes |
title_sort | evolution of male pregnancy associated with remodeling of canonical vertebrate immunity in seahorses and pipefishes |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7196912/ https://www.ncbi.nlm.nih.gov/pubmed/32284407 http://dx.doi.org/10.1073/pnas.1916251117 |
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