Evidence of positive selection associated with placental loss in tiger sharks

Abstract

Background: All vertebrates initially feed their offspring using yolk reserves. In some live-bearing species these yolk reserves may be supplemented with extra nutrition via a placenta. Sharks belonging to the Carcharhinidae family are all live-bearing, and with the exception of the tiger shark (Galeocerdo cuvier), develop placental connections after exhausting yolk reserves. Phylogenetic relationships suggest the lack of placenta in tiger sharks is due to secondary loss. This represents a dramatic shift in reproductive strategy, and is likely to have left a molecular footprint of positive selection within the genome. Results: We sequenced the transcriptome of the tiger shark and eight other live-bearing shark species. From this data we constructed a time-calibrated phylogenetic tree estimating the tiger shark lineage diverged from the placental carcharhinids approximately 94 million years ago. Along the tiger shark lineage, we identified five genes exhibiting a signature of positive selection. Four of these genes have functions likely associated with brain development (YWHAE and ARL6IP5) and sexual reproduction (VAMP4 and TCTEX1D2). Conclusions: Our results indicate the loss of placenta in tiger sharks may be associated with subsequent adaptive changes in brain development and sperm production.

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Item Type:	Article
Authors/Creators:	Swift, D.G. Dunning, L.T. Igea, J. Brooks, E.J. Jones, C.S. Noble, L.R. Ciezarek, A. Humble, E. Savolainen, V.
Copyright, Publisher and Additional Information:	© 2016 The Author(s). This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated
Keywords:	Reproduction; Viviparous; Placenta; Transcriptome; RNA-Seq; Positive selection; Elasmobranchs; Carcharhinids; Galeocerdo
Dates:	Published: 14 June 2016 Published (online): 14 June 2016 Accepted: 2 June 2016
Institution:	The University of Sheffield
Academic Units:	The University of Sheffield > Faculty of Science (Sheffield) > School of Biosciences (Sheffield) > Department of Animal and Plant Sciences (Sheffield)
Depositing User:	Symplectic Sheffield
Date Deposited:	13 Jul 2016 10:14
Last Modified:	13 Jul 2016 11:27
Published Version:	http://dx.doi.org/10.1186/s12862-016-0696-y
Status:	Published
Publisher:	BioMed Central
Refereed:	Yes
Identification Number:	10.1186/s12862-016-0696-y
Open Archives Initiative ID (OAI ID):	oai:eprints.whiterose.ac.uk:102411

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Evidence of positive selection associated with placental loss in tiger sharks

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