Evolution of male pregnancy associated with remodeling of canonical vertebrate immunity in seahorses and pipefishes.

comparative genomics immunological tolerance major histocompatibility complex male pregnancy seahorse

Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
28 04 2020
Historique:
pubmed: 15 4 2020
medline: 11 8 2020
entrez: 15 4 2020
Statut: ppublish

Résumé

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 (

Identifiants

pubmed: 32284407
pii: 1916251117
doi: 10.1073/pnas.1916251117
pmc: PMC7196912
doi:

Banques de données

figshare
['10.6084/m9.figshare.11499360']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

9431-9439

Informations de copyright

Copyright © 2020 the Author(s). Published by PNAS.

Déclaration de conflit d'intérêts

The authors declare no competing interest.

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Auteurs

Olivia Roth (O)

Marine Evolutionary Ecology, GEOMAR Helmholtz Centre for Ocean Research Kiel, D-24105 Kiel, Germany; oroth@geomar.de.

Monica Hongrø Solbakken (MH)

Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, NO-0371 Oslo, Norway.

Ole Kristian Tørresen (OK)

Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, NO-0371 Oslo, Norway.

Till Bayer (T)

Marine Evolutionary Ecology, GEOMAR Helmholtz Centre for Ocean Research Kiel, D-24105 Kiel, Germany.

Michael Matschiner (M)

Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, NO-0371 Oslo, Norway.
Department of Palaeontology and Museum, University of Zurich, CH-8006 Zürich, Switzerland.

Helle Tessand Baalsrud (HT)

Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, NO-0371 Oslo, Norway.

Siv Nam Khang Hoff (SNK)

Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, NO-0371 Oslo, Norway.

Marine Servane Ono Brieuc (MSO)

Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, NO-0371 Oslo, Norway.

David Haase (D)

Marine Evolutionary Ecology, GEOMAR Helmholtz Centre for Ocean Research Kiel, D-24105 Kiel, Germany.

Reinhold Hanel (R)

Thünen Institute of Fisheries Ecology, D-27572 Bremerhaven, Germany.

Thorsten B H Reusch (TBH)

Marine Evolutionary Ecology, GEOMAR Helmholtz Centre for Ocean Research Kiel, D-24105 Kiel, Germany.

Sissel Jentoft (S)

Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, NO-0371 Oslo, Norway.

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