Evidence of positive selection associated with placental loss in tiger sharks

Dominic G. Swift; Luke T. Dunning; Javier Igea; Edward J. Brooks; Catherine S. Jones; Leslie R. Noble; Adam Ciezarek; Emily Humble; Vincent Savolainen

doi:10.1186/s12862-016-0696-y

Evidence of positive selection associated with placental loss in tiger sharks

Dominic G. Swift, Luke T. Dunning, Javier Igea, Edward J. Brooks, Catherine S. Jones, Leslie R. Noble, Adam Ciezarek, Emily Humble, Vincent Savolainen

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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.

Original language	English
Article number	126
Pages (from-to)	1-10
Number of pages	10
Journal	BMC Evolutionary Biology
Volume	16
DOIs	https://doi.org/10.1186/s12862-016-0696-y
Publication status	Published - 14 Jun 2016

Bibliographical note

Acknowledgements
We thank staff at the Cape Eleuthera Institute for assistance in the field, Dominique Barthelemy and Jean Goasdoue for providing samples, and Helen Hipperson for assistance in the lab.

Keywords

Reproduction
Viviparous
Placenta
Transcriptome
RNA-Seq
Positive selection
Elasmobranchs
Carcharhinids
Galeocerdo

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10.1186/s12862-016-0696-yLicence: CC BY

Evidence of positive selection associated with placental loss in tiger sharks
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.
Final published version, 682 KBLicence: CC BY

Catherine Jones
- Biological Sciences, Aberdeen Centre For Environmental Sustainability - Senior Lecturer
- Marine Alliance for Science and Technology for Scotland (MASTS)
Person: Academic

Cite this

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title = "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.",

keywords = "Reproduction, Viviparous, Placenta , Transcriptome, RNA-Seq, Positive selection, Elasmobranchs, Carcharhinids, Galeocerdo",

author = "Swift, {Dominic G.} and Dunning, {Luke T.} and Javier Igea and Brooks, {Edward J.} and Jones, {Catherine S.} and Noble, {Leslie R.} and Adam Ciezarek and Emily Humble and Vincent Savolainen",

note = "Acknowledgements We thank staff at the Cape Eleuthera Institute for assistance in the field, Dominique Barthelemy and Jean Goasdoue for providing samples, and Helen Hipperson for assistance in the lab.",

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doi = "10.1186/s12862-016-0696-y",

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AU - Dunning, Luke T.

AU - Igea, Javier

AU - Brooks, Edward J.

AU - Jones, Catherine S.

AU - Noble, Leslie R.

AU - Ciezarek, Adam

AU - Humble, Emily

AU - Savolainen, Vincent

N1 - Acknowledgements We thank staff at the Cape Eleuthera Institute for assistance in the field, Dominique Barthelemy and Jean Goasdoue for providing samples, and Helen Hipperson for assistance in the lab.

PY - 2016/6/14

Y1 - 2016/6/14

N2 - 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.

AB - 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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KW - Galeocerdo

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JO - BMC Evolutionary Biology

JF - BMC Evolutionary Biology

M1 - 126

ER -

Evidence of positive selection associated with placental loss in tiger sharks

Abstract

Bibliographical note

Keywords

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