Genome rearrangements, male pregnancy and immunological tolerance – the curious case of the syngnathid immune system

Abstract

The syngnathid fish group (seahorses, pipefishes and seadragons) is a fascinating lineage associated with an array of evolutionary peculiarities that include diverse morphologies and their unique male pregnancy. These oddities also extend to their immune systems, with a growing body of research highlighting a range of intriguing immunological characteristics and genomic rearrangements, which pose questions regarding their evolutionary history and immune strategies. The functional loss of the major histocompatibility complex class II pathway (MHC II) in the Syngnathus genus and related pathway components in the seahorse (Hippocampus) were two discoveries that initially piqued interest. This sparked discussions concerning immune capabilities, possible facilitative roles in advanced male pregnancy evolution through means of evoking immunological tolerance, as well as a general re-evaluation of how we interpret vertebrate immunological plasticity. Experimental approaches have attempted to clarify further the impact of immune repertoire loss on the efficacy of the syngnathid immune response, specificities regarding the pathways in play during pregnancy as well as the concept of immunological inheritance. The first characterization of the immune cell repertoire of Syngnathus typhle using scRNA-seq represents the latest step to understanding the immune dynamics of these enigmatic fish. This report serves as a review for the immunological insights into the fascinating syngnathid fish group; encompassing their evolutionary history, immune cell populations, links to male pregnancy, and sex specificity, in addition to highlighting future research opportunities in need of investigation.

Reproductive innovation enabled radiation in the deep sea during an ecological crisis

“…Whereas ogcocephalids, chaunacids, and antennariids show no losses to their immunogenomic loci, lophiids have lost virtually all of the genetic basis of the major histocompatibility complex II 25 . These observations, particularly when considered in the context of the various episodes of immunogenomic degeneration in teleost fishes 21,59 , show that modifications and losses of key genes involved in adaptive immunity predated the origins of deep-sea anglerfishes. Similarly, ancestral state reconstructions for sexual body size dimorphism based on recent observations of diminutive males in frogfishes and the deep sea lophiid Sladenia gardineri 60 suggest that significant body size differences between male and female anglerfishes originated prior to the origin of deep-sea ceratioids (Figure S13).…”

Seahorse Male Pregnancy as a Model System to Study Pregnancy, Immune Adaptations, and Environmental Effects

“…They found that the loss or downregulation of MHC pathway gene expression occurs only in species with a brood pouch pregnancy, and that a decrease in MHC pathway gene expression is limited to the early and middle stages of pregnancy. In late pregnancy and at birth, the expression of immune genes was elevated, suggesting that the late embryos, in contrast to the early embryos, are no longer in direct contact with the paternal immune system [52,53].…”

Sexual antagonism and sex determination in three syngnathid species alongside a male pregnancy gradient

“…Hence, sex bias in expression is more likely to be directly related to the effects of SS and SAS over viability and survival. Indirectly, due to male pregnancy, reproduction would also be affected as eggs require oxygen supply and interact with the father’s mucosal immune system (Whittington et al 2015; Nygård et al 2019; Parker et al 2023). Besides genome wide Fst and genes with sex-biased expression (SBGs), we looked at differential allele expression.…”