Structure and permeability of the egg capsule of the placental Australian sharpnose shark, Rhizoprionodon taylori

Alice L Buddle,Margot L Day,Michael B Thompson,James U Van Dyke,Christopher R Murphy,Colin A Simpfendorfer,Camilla M Whittington

doi:10.1007/s00360-021-01427-0

Alice L Buddle, Margot L Day + Show 5 more

Open Access

https://doi.org/10.1007/s00360-021-01427-0

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Abstract

Shark placentae are derived from modifications to the fetal yolk sac and the maternal uterine mucosa. In almost all placental sharks, embryonic development occurs in an egg capsule that remains intact for the entire pregnancy, separating the fetal tissues from the maternal tissues at the placental interface. Here, we investigate the structure and permeability of the egg capsules that surround developing embryos of the placental Australian sharpnose shark (Rhizoprionodon taylori) during late pregnancy. The egg capsule is an acellular fibrous structure that is 0.42 ± 0.04 μm thick at the placental interface between the yolk sac and uterine tissues, and 0.67 ± 0.08 μm thick in the paraplacental regions. This is the thinnest egg capsule of any placental shark measured so far, which may increase the diffusion rate of respiratory gases, fetal wastes, water and nutrients between maternal and fetal tissues. Molecules smaller than or equal to ~ 1000 Da can diffuse through the egg capsule, but larger proteins (~ 3000–26,000 Da) cannot. Similar permeability characteristics between the egg capsule of R. taylori and other placental sharks suggest that molecular size is an important determinant of the molecules that can be exchanged between the mother and her embryos during pregnancy.

Highlights

Shark reproduction is diverse: some species lay fertilised eggs, but most species give birth to fully-developed young
The egg capsule is filled with luminal fluid and lies opposed to the paraplacental regions of these uterine compartments (Fig. S2)
The acellular egg capsule that is incorporated into the placental interface of late pregnant R. taylori is similar in structure to the egg capsule that lies opposed to the paraplacental uterine epithelium

Summary

Introduction

Shark reproduction is diverse: some species lay fertilised eggs (oviparous), but most species give birth to fully-developed young (viviparous; Buddle et al 2019; Hamlett et al.Communicated by Philip Withers.2005b). Shark reproduction is diverse: some species lay fertilised eggs (oviparous), but most species give birth to fully-developed young The majority of viviparous sharks develop without a placenta and are primarily reliant on yolk for embryonic nourishment during pregnancy (Hamlett et al 2005b; Buddle et al 2019). The oviducal gland is divided into four morphologically and functionally distinct zones: the club, papillary, baffle and terminal zones (Hamlett et al 1998, 2005b). The terminal zone stores sperm in some sharks

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