Structural changes to the brood pouch of male pregnant seahorses (Hippocampus abdominalis) facilitate exchange between father and embryos

• Published in: Placenta (Eastbourne) 2021-10, Vol.114, p.115-123
• Main Authors: Dudley, J.S., Hannaford, P., Dowland, S.N., Lindsay, L.A., Thompson, M.B., Murphy, C.R., Van Dyke, J.U., Whittington, C.M.
• Format: Article
• Language: English
• Subjects: Angiogenesis; Animals; Embryo incubation; Male; Oviparity - physiology; Parental care; Placenta; Respiratory gas exchange; Smegmamorpha - anatomy & histology; Smegmamorpha - embryology; Syngnathid; Vascularity
• ISSN: 0143-4004; 1532-3102
• DOI: 10.1016/j.placenta.2021.09.002

Embryonic growth and development require efficient respiratory gas exchange. Internal incubation of developing young thus presents a significant physiological challenge, because respiratory gas diffusion to embryos is impeded by the additional barrier of parental tissue between the embryo and the environment. Therefore, live-bearing species exhibit a variety of adaptations facilitating respiratory gas exchange between the parent (usually the mother) and embryos. Syngnathid fishes are the only vertebrates to exhibit male pregnancy, allowing comparative studies of the biology and evolution of internal incubation of embryos, independent of the female reproductive tract. Here, we examine the fleshy, sealed, seahorse brood pouch, and provide the first quantification of structural changes to this gestational organ across pregnancy. We used histological analysis and morphometrics to quantify the surface area for exchange across the brood pouch epithelium, and the structure of the vascular bed of the brood pouch. We show dramatic remodelling of gestational tissues as pregnancy progresses, including an increase in tortuosity of the gestational epithelium, an increase in capillary density, and a decrease in diffusion distance between capillaries and the pouch lumen. These changes produce an increased surface area and expansion of the vascular bed of the placenta that likely facilitates respiratory gas exchange. These changes mirror the remodelling of gestational tissue in viviparous amniotes and elasmobranchs, and provide further evidence of the convergence of adaptations to support pregnancy in live-bearing animals. •Brood pouch from male Hippocampus abdominalis undergoes remodelling during pregnancy.•There is increased surface area and expansion of the vascular bed during pregnancy.•The increase in vascularisation likely facilitates respiratory gas exchange.•These changes mirror remodelling of gestational tissues in other viviparous amniotes.•Provides evidence for the convergent evolution of mechanisms to support pregnancy.