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Advances in the aquatic sciences
REVIEW

Evolution of placentotrophy: using viviparous sharks as a model to understand vertebrate placental evolution

Alice L. Buddle A , James U. Van Dyke B , Michael B. Thompson A , Colin A. Simpfendorfer C and Camilla M. Whittington D E
+ Author Affiliations
- Author Affiliations

A The University of Sydney, School of Life and Environmental Sciences, Heydon-Laurence Building (A08), NSW 2006, Australia.

B Charles Sturt University, School of Environmental Sciences, Institute for Land, Water and Society, Albury, NSW 2640, Australia.

C James Cook University, College of Science and Engineering and Centre for Sustainable Tropical Fisheries and Aquaculture, Townsville, Qld 4811, Australia.

D The University of Sydney, Sydney School of Veterinary Science, Camperdown, NSW 2006, Australia.

E Correspondence. Email: camilla.whittington@sydney.edu.au

Marine and Freshwater Research 70(7) 908-924 https://doi.org/10.1071/MF18076
Submitted: 2 March 2018  Accepted: 18 June 2018   Published: 20 September 2018

Abstract

Reproducing sharks must provide their offspring with an adequate supply of nutrients to complete embryonic development. In oviparous (egg-laying) sharks, offspring develop outside the mother, and all the nutrients required for embryonic growth are contained in the egg yolk. Conversely, in viviparous (live-bearing) sharks, embryonic development is completed inside the mother, providing offspring with the opportunity to receive supplementary embryonic nourishment, known as matrotrophy. Viviparous sharks exhibit nearly all forms of matrotrophy known in vertebrates, including a yolk-sac placenta, which involves several significant ontogenetic modifications to fetal and maternal tissues. The selective pressures that have driven the evolution of complex placentas in some shark species, but not in others, are unresolved. Herein we review the mechanisms of reproductive allocation and placental diversity in sharks, and consider the application of both adaptive and conflict hypotheses for the evolution of placental nutrient provisioning. Both have likely played roles in placental evolution in sharks, perhaps at different times in evolutionary history. Finally, we recommend sharks as an outstanding model system to investigate the evolution of placentas and mechanisms for fetal nutrition during pregnancy in vertebrates.

Additional keywords: Chondrichthyes, matrotrophy, uterus, viviparity, yolk sac placenta.


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