The evolution of viviparity and placentae in sharks

Abstract

Most sharks are viviparous, giving birth to live young that complete embryonic development inside of their mother. While we know that viviparity has evolved independently from egg-laying (oviparity) seven times in sharks, the structural and physiological specialisations that support the evolution of pregnancy in sharks are unresolved. In this thesis, I investigate the functional morphology of viviparity in sharks. I begin by reviewing the data on shark reproductive biology, and reveal that embryonic development can be supported by diverse maternal and fetal specialisations during pregnancy. Given that most transitions to viviparity in sharks have resulted in non-placental forms of viviparity, I then use light microscopy to describe the development of vascularised uterine villi during pregnancy in the non-placental dwarf ornate wobbegong shark (Orectolobus ornatus). These uterine villi increase the surface area available for fetomaternal exchange, and likely support embryonic respiratory gas exchange, waste removal and/or water balance, but not organic nutrient transfer during pregnancy. In contrast to O. ornatus, I show that the Australian sharpnose shark, Rhizoprionodon taylori, develops elaborate paraplacental and placental structures for nutrient transfer to developing embryos. The placenta of R. taylori consists of the maternal uterus, an acellular egg capsule and the fetal yolk sac. I discovered that this egg capsule only allows molecules smaller than 1,000 Da to pass across its surface. Additionally, I identify placental specialisations for respiratory gas exchange in R. taylori which are morphologically-similar to those in viviparous amniotes (mammals and reptiles). Through combining transcriptomics with immunohistochemistry, I suggest that amino acid transport is achieved by similar molecular mechanisms in R. taylori and eutherian mammals. These similarities are striking examples of convergent evolution because placentae arise from ancestrally-different tissues in R. taylori and viviparous amniotes. My findings demonstrate the importance of investigations of the reproductive diversity of sharks for understanding how viviparity and placentae evolve across vertebrate taxa.