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

Research output: Contribution to journalArticle

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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 languageEnglish
Article number126
Pages (from-to)1-10
Number of pages10
JournalBMC Evolutionary Biology
Volume16
DOIs
Publication statusPublished - 14 Jun 2016

Fingerprint

Galeocerdo cuvier
shark
placenta
sharks
brain
Carcharhinidae
phylogenetics
phylogeny
loss
gene
sexual reproduction
transcriptome
footprint
reproductive strategy
sperm
genes
nutrition
vertebrates
spermatozoa
vertebrate

Keywords

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

Cite this

Swift, D. G., Dunning, L. T., Igea, J., Brooks, E. J., Jones, C. S., Noble, L. R., ... Savolainen, V. (2016). Evidence of positive selection associated with placental loss in tiger sharks. BMC Evolutionary Biology, 16, 1-10. [126]. https://doi.org/10.1186/s12862-016-0696-y

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.

In: BMC Evolutionary Biology, Vol. 16, 126, 14.06.2016, p. 1-10.

Research output: Contribution to journalArticle

Swift, DG, Dunning, LT, Igea, J, Brooks, EJ, Jones, CS, Noble, LR, Ciezarek, A, Humble, E & Savolainen, V 2016, 'Evidence of positive selection associated with placental loss in tiger sharks', BMC Evolutionary Biology, vol. 16, 126, pp. 1-10. https://doi.org/10.1186/s12862-016-0696-y
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. In: BMC Evolutionary Biology. 2016 ; Vol. 16. pp. 1-10.
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AU - Jones, Catherine S.

AU - Noble, Leslie R.

AU - Ciezarek, Adam

AU - Humble, Emily

AU - Savolainen, Vincent

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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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