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. 2016 Jun 14;16(1):126.
doi: 10.1186/s12862-016-0696-y.

Evidence of positive selection associated with placental loss in tiger sharks

Dominic G Swift  1 , Luke T Dunning  2 , Javier Igea  3 , Edward J Brooks  4 , Catherine S Jones  5 , Leslie R Noble  5 , Adam Ciezarek  6 , Emily Humble  7 , Vincent Savolainen  8
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Evidence of positive selection associated with placental loss in tiger sharks

Dominic G Swift et al. BMC Evol Biol. .

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

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Figures

Fig. 1
Fig. 1
Time-calibrated phylogenetic tree of sharks. Based on analyses of 1,102 genes (1,007,817 bp per species). Species are named along with the orders and families they belong to the non-placental species are shown in red. Each node was annotated with inferred posterior mean times and 95 % highest posterior density credibility intervals in million years. Node 1: 177 and 170–184. Node 2: 142 and 130–163. Node 3: 94 and 59–130. Node 4: 62 and 35–88. Node 5: 28 and 20–37. Node 6: 21 and 15–27. Node 7: 17 and 11–22. Node 8: 14 and 10–17. Each node is supported with a bootstrap value of 100 %
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