Male Pregnancy: A Miracle of Nature?

Shreejita Bhowmick, Techno India University

Introduction

Pregnancy itself is a beautiful journey of a highly regulated cascade of events, ones which we generally relate with a woman. But what if this role is switched and the males are the ones giving birth?
Nature always amuses us and in our surroundings, we can observe a few instances where the male plays the same biological role as a female. Though it seems to be an alienated or a mysterious concept for us mammals, such cases of male pregnancy can be observed in seahorse, pipefish, and sea dragons of the Syngnathidae family which consists of more than 200 species.
Paternal care is common in cardinal fishes where they hold fertilized eggs in their mouth and in giant water bugs and midwife toads where they carry the fertilized eggs on their body. But in the case of the species of the Syngnathidae family, they seem to have reached an extreme level of paternal care.

Male Pregnancy in the Syngnathidae Family

Seahorse (Hippocampus): 

In seahorses, the males have brood pouches, a small pocket-like area in front of their bodies. The females drop their eggs in these brood pouches where the male fertilizes the egg by providing enough oxygen and nutrients, till they hatch. The eggs are deeply embedded in the walls of these brood pouches and covered by pouch tissue for protection. After fertilization, it takes two to four weeks for the babies to hatch and just like in mammals, contractions occur in these male seahorses during hatching the eggs which may last up to 12 hours! At once, 50 to 1000 baby seahorses can hatch. But these baby seahorses spend two to three weeks drifting with the plankton in the ocean which makes them susceptible to predators, so, only 1 in 1000 offspring can survive till adulthood.

Pipefish (Syngnathinae):

Alongside seahorses, pipefishes that belong to the same family also show male pregnancy. Pipefishes are more or less similar to seahorses but as the name suggests, it is just a bit stretched out than seahorses. Instead of a brood pouch, pipefishes have slits, grooves, and flaps on their body which serves as the home for the eggs for fertilization. Offspring hatch after a couple of weeks of fertilization.

Male pipefish can carry between 5 and 40 eggs. An interesting fact about the male pipefish, they do not take care of eggs coming from the females they aren’t very fond of and only put resources from larger, attractive female counterparts. They also don’t put much effort into the survival of the offspring after successful and healthy hatching. But not just the male, there’s also an interesting fact about the female pipefishes.

The female pipefish also takes responsibility to provide nutrition to the eggs and even sometimes, these female pipefish leave their male counterparts after mating so that they don’t see them again, mostly when they find the male pipefish to be irresponsible. This isn’t found in the case of seahorses where the female frequently checks on the male who’s carrying the eggs.

Sea Dragons (Phycodurus eques): 

The third one in the Syngnathidae family that shows almost similar male pregnancy is the sea dragons. The sea dragons are often confused with some tropical fish due to their colorful and leaf-like appendages. But all three species of sea dragons can only be found on cool water on southern Australia’s coast. According to Leslee Matsushige, associate curator at the Birch Aquarium at Scripps Institution of Oceanography, University of California, San Diego, among these three species, the weedy sea dragons can reproduce in aquariums, the leafy ones never bred in captivity while the ruby sea dragons are only known to science since 2015.

Sea dragons also don’t have brood pouches to keep the eggs, but they wrinkle their tails where there are tiny cups for the females to deposit about hundreds of eggs. The eggs stay in these cups securely for four to six weeks before hatching. For years at the Birch aquarium, Matsushige and her team created optimal conditions for both male and female sea dragons in a controlled tank away from aquarium visitors for a successful transfer of eggs from the females to the males, but they weren’t successful. Later in 2017, after watching a YouTube video of a diver who captured the mating of sea dragons, Matsushige finally understood that these sea dragons need a bigger tank for successful mating.

Delving deep into the modifications in their Immune System

Genome Size:

The Syngnathidae family contains species with very divergent genome sizes. It varies from 347 Mbp (Syngnathus rostellatus) to 1.8 Gbp (Entelurus aequoreus). The species of this family that lack the ability of male pregnancy shows larger genome size than the ones showing the ability of male pregnancy while the Nerophinae pipefishes which have external male pregnancy, have significantly larger genomes. Most probably, this is due to the expansion of transposable elements in Nerophinae during 50 million years of evolution.

MHC 2 Modifications:

Now coming to the immune system, the major histocompatibility complex, that is, MHC class 1 and MHC class 2 are essential for the recognition process of nonself-peptides by presenting them to CD8+ and CD4+ T cells, respectively. But in the case of these species displaying male pregnancy, significant modifications, be it losses or changes in the key genes of the MHC class 2 pathway can be observed.

It is seen that the invariant chain of MHC 2 (CD74) displays sequence substitution at exon 6b in seahorses and divergent exon 3 in both seahorses and pipefishes, impairing the function of CD74. Moreover, it is found that the genes encoding the MHC 2 α- and β-chains have been lost in all Syngnathidae species. This implies that the presentation of antigens to the T cell receptor on CD4+ T lymphocytes is disabled. Exons 3, 4, 5, 6, and 12 of AIRE are either lost or substituted in seahorse and pipefishes thus inferring an almost complete loss of the MHC 2 pathway in Syngnathidae family species. However, an alternate function not related to MHC 2 pathway might be observed especially in seahorses since the genes of the MHC 2 pathway are under positive selection in them.

MHC 1 Modifications:

In the case of the MHC 1 pathway, by assessing the copy number of the exon 4, it is found that the copy number is higher in all species showing male pregnancy than that of the species which don’t display male pregnancy.

In Syngnathids, the sequences of MHC 1 are of U lineage and their distinct cluster supports coevolution of MHC 1 with male pregnancy. Beta 2 microglobulin, important for the availability of MHC 1 light chain proteins, CD8, important for activation of CD8+ T lymphocytes, RAG1, important for facilitating V(D)J recombination, and TAP1/TAP2, important for antigen transportation, are under positive selection in Syngnathids. This expanded MHC1 pathway in Syngnathidae species may compensate for the modifications in MHC 2 pathway.

Haemoglobin gene Modifications:

To meet the oxygen requirement of the eggs, shifts in the haemoglobin gene are also seen in these species. All the species of the Syngnathidae family have lost the haemoglobin alpha 6 gene and in addition to this, sea horses and pipefish have also lost the haemoglobin alpha 5 gene. Moreover, fully pregnant species have gained haemoglobin alpha 1 and alpha 2 genes.

Gene Expression Modifications:

Coming to differences in gene expression, a total of 141 genes are up or down regulated in the case of male pregnancy in these species. 116 genes that cover important pathways in female pregnancy like prostaglandin, mammalian target of rapamycin (mTOR), and progesterone pathways, in corpus luteum degradation, parent–embryo transport, placenta development, conceptus implantation, and embryo growth are differentially expressed in these species.

There are several other instances of up or down regulation of immune gene expression in these species which are quite different from female pregnancy in mammals but facilitates male pregnancy.

Conclusion

Among Homo sapiens, male pregnancy can potentially be possible amongst transgender men and non-binary people, provided they are able to prepare their bodies with a uterus and other related biological parameters that are necessary for child birth. New research involving uterine transplants may mean some possibility of male pregnancy in the future. But for now, the only males who can bear child birth in their natural course of life are the seahorses, pipefishes, and similar other species of their family.

Also read: Cathepsins: Lysosomal Proteases that are Vital and Lethal

References

1. Jones, A. G., & Avise, J. C. (2003). Male pregnancy. Current Biology, 13(20), R791. https://doi.org/10.1016/j.cub.2003.09.045
2. Sequin, M. (2016). These are the only 3 animals on earth who produce offspring this way. Business Insider. https://www.businessinsider.in/science/these-are-the-only-3-animals-on-earth-who-produce-offspring-this-way/articleshow/53565377.cms
3. Bodin, M. (2020). The mystery of male pregnancy and birth in Seahorses. Discover Magazine. https://www.discovermagazine.com/planet-earth/the-mystery-of-male-pregnancy-and-birth-in-seahorses
4. Roth, O., Solbakken, M. H., Tørresen, O. K., Bayer, T., Matschiner, M., Baalsrud, H. T., Hoff, S. N. K., Brieuc, M. S. O., Haase, D., Hanel, R., Reusch, T. B. H., & Jentoft, S. (2020). Evolution of male pregnancy associated with remodeling of canonical vertebrate immunity in seahorses and pipefishes. Proceedings of the National Academy of Sciences, 117(17), 9431–9439. https://doi.org/10.1073/pnas.1916251117

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