Figure 2: The three types of brooding structures investigated by Parker et al. (2022), and the simplified corresponding syngnathid phylogeny (from left to right: Nerophis ophidion ,Syngnathus typhle and Hippocampus guttulatus . Photos by Patrick Louisy).
By sequentially monitoring male pregnancy, Parker et al. (2022) were able to highlight, with great detail, striking similarities between male and female pregnancy, ranging from: i) the existence of clear stage-specific gene expression patterns, denoting the necessary morphological and physiological changes that occur in the pregnant parent, ii) the need for an inflammatory process during early pregnancy, likely assisting egg engulfment, or iii) the presence of homologous gene expression profiles. The apparent absence of male pregnancy specific genes is particularly interesting, reinforcing Whittington et al. (2015) observation that pregnancy regulation, despite independently evolving in clearly divergent evolutionary lineages, seems to use a common ‘genes toolkit’.
By contrasting male pregnancy along syngnathids’ gradient of brooding structure complexity, Parker et al. (2022) reinforces the perception that attaining the highest degrees of intimacy between parent and offspring (i.e., gestation in a brood pouch) was only possible with immune modulation. As also observed by Roth et al. (2020), the MHC I downregulation seems to actively contribute to the necessary immunological tolerance that circumvents rejection of developing offspring. While the exact role of MHC II remains ambiguous, we can be tempted to speculate that its simultaneous loss in pouched syngnathids is probably much more than a coincidence. Was MHC II dismantlement a by-product or a prerequisite to the transition from non-pouched to pouched pregnancy? As pipefishes and seahorses differ in the type of genomic rearrangements leading to MHC II impairment (Roth et al., 2020), I presently lean towards the second hypothesis. The future inclusion of additional syngnathid species, from the pool of intermediate pregnancy types positioned between external egg gluing and closed pouches, will surely help shed light on this topic. As an added bonus, a closer look into the most basal branches of syngnathid phylogeny will also help pinpoint the unidentified origin, and mode, of nutrient transfer to (and from) developing embryos. While evidence suggests that pouched species are able to exchange nutrients to and from their brood (Cunha, Berglund, Mendes, & Monteiro, 2018; Sagebakken, Ahnesjö, Mobley, Braga Goncalves, & Kvarnemo, 2009), the limited data on pouchless species (Miranda, Vieira, & Monteiro, 2017; Parker et al., 2022) leads to contradictory conclusions.
Once viewed as mere oddities, the extraordinary life histories of syngnathids have long converted them into model organisms to address a wide array of questions related to the evolution of reproductive complexity… and there are still secrets to uncover. Even if unable to decisively unveil all the cryptic mechanisms occurring during male pregnancy, Parker et al. (2022) work significantly progresses our understanding of the subcellular subtleties resulting from the evolution of an intimate, and apparently sex-undiscriminating, connection between offspring and the pregnant mother or father.
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