Pregnancy, the post-fertilization period when embryos are
incubated within the body, is a dynamic multistage process that has
convergently evolved in many vertebrates. To increase independence from
environmental fluctuations and protect offspring from predation,
challenges had to be initially overcome. The most obvious, when
considering such an intimate relation between the parent and its
semi-allogenic offspring, was the pressing need to dodge
immunity-associated embryo rejection. In mammals, immunological
tolerance was found to be dependent on the active modulation of the
immune system. Even though supporting much of the current knowledge on
vertebrate pregnancy, mammals lack extant transitional stages that could
help reconstruct the evolutionary pathway of this fascinatingly complex
reproduction mode. In this issue of Molecular Ecology, Parker et al.
(2022) selected an untraditional model - the seahorse and pipefish
family, whose species evolved male pregnancy across an almost continuous
gradient of complexity, from external oviparity to internal gestation.
By contrasting gene expression profiles of syngnathids with distinct
brooding architectures, this study allowed for the observation of subtle
evolutionary adaptations, while confirming the existence of remarkable
similarities to ‘female’ pregnancy (e.g., the evolution of male
pregnancy in pouched species occurred alongside immune downregulation,
and inflammation seems vital during early pregnancy stages). In a world
where the debate on sex-roles takes centre stage, Parker et al. (2022)
appeasing results hint at the fact that the strongly convergent
evolution of vertebrate pregnancy was seemingly unaffected by which sex
carries the burden of gestation.
Syngnathids (seahorses, pipefishes, pipehorses and seadragons) belong to
a diverse family of bony fish with more than 300 species, primarily
recognized by its unique mode of reproduction: male pregnancy. This
novelty of the syngnathid lineage long attracted attention from the
scientific community and was rapidly recognised as significant to the
evolutionary radiation of the syngnathid lineage. In fact, one of the
first attempts at reconstructing the phylogenetic relationships within
syngnathids, long before the advent of genomics, was partially grounded
on the general architecture of brooding structures (Herald, 1959).
Curiously, recent efforts, backed by current methodologies (Hamilton et
al., 2017; Stiller et al., 2022), still recognise the diversification of
structures involved in male pregnancy as relevant for diagnosing
syngnathid taxa. From an ancestral pipefish, that probably presented a
rather simple brooding structure where eggs were exposed, increasingly
more complex structures evolved up to the sealed seahorse brood pouch
(Figure 1). This apparent gradient of complexity, easily observable in
extant syngnathid species (and almost absent in mammals), renewed the
interest in this family of quirky fish into as an invaluable opportunity
to shed additional light on the evolution of pregnancy.