Abstract
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.
PNAS
First published April 13, 2020
DOI: 1916251117
Publication webpage.
Authors: Olivia Roth§, Monica Hongrø Solbakken*, Ole Kristian Tørresen*, Till Bayer§, Michael Matschiner*,#, Helle Tessand Baalsrud*, Siv Nam Khang Hoff*, Marine Servane Ono Brieuc*, David Haase§, Reinhold Hanel¤, Thorsten B. H. Reusch§, and Sissel Jentoft*.
* Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Oslo, Norway. See the publication webpage for full author information.
§ Marine Evolutionary Ecology, GEOMAR Helmholtz Centre for Ocean Research Kiel, D-24105 Kiel, Germany;
* 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-8006Zürich, Switzerland
¤ Thünen Institute of Fisheries Ecology, D-27572 Bremerhaven, Germany