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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