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Evidence of positive selection associated with placental loss in tiger sharks

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 (Gal...

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Autores principales: Swift, Dominic G., Dunning, Luke T., Igea, Javier, Brooks, Edward J., Jones, Catherine S., Noble, Leslie R., Ciezarek, Adam, Humble, Emily, Savolainen, Vincent
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4906603/
https://www.ncbi.nlm.nih.gov/pubmed/27296413
http://dx.doi.org/10.1186/s12862-016-0696-y
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author Swift, Dominic G.
Dunning, Luke T.
Igea, Javier
Brooks, Edward J.
Jones, Catherine S.
Noble, Leslie R.
Ciezarek, Adam
Humble, Emily
Savolainen, Vincent
author_facet Swift, Dominic G.
Dunning, Luke T.
Igea, Javier
Brooks, Edward J.
Jones, Catherine S.
Noble, Leslie R.
Ciezarek, Adam
Humble, Emily
Savolainen, Vincent
author_sort Swift, Dominic G.
collection PubMed
description 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0696-y) contains supplementary material, which is available to authorized users.
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spelling pubmed-49066032016-06-15 Evidence of positive selection associated with placental loss in tiger sharks Swift, Dominic G. Dunning, Luke T. Igea, Javier Brooks, Edward J. Jones, Catherine S. Noble, Leslie R. Ciezarek, Adam Humble, Emily Savolainen, Vincent BMC Evol Biol Research Article 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0696-y) contains supplementary material, which is available to authorized users. BioMed Central 2016-06-14 /pmc/articles/PMC4906603/ /pubmed/27296413 http://dx.doi.org/10.1186/s12862-016-0696-y Text en © The Author(s). 2016 Open AccessThis 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.
spellingShingle Research Article
Swift, Dominic G.
Dunning, Luke T.
Igea, Javier
Brooks, Edward J.
Jones, Catherine S.
Noble, Leslie R.
Ciezarek, Adam
Humble, Emily
Savolainen, Vincent
Evidence of positive selection associated with placental loss in tiger sharks
title Evidence of positive selection associated with placental loss in tiger sharks
title_full Evidence of positive selection associated with placental loss in tiger sharks
title_fullStr Evidence of positive selection associated with placental loss in tiger sharks
title_full_unstemmed Evidence of positive selection associated with placental loss in tiger sharks
title_short Evidence of positive selection associated with placental loss in tiger sharks
title_sort evidence of positive selection associated with placental loss in tiger sharks
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4906603/
https://www.ncbi.nlm.nih.gov/pubmed/27296413
http://dx.doi.org/10.1186/s12862-016-0696-y
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