Abstract

BackgroundAll 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.ResultsWe 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).ConclusionsOur results indicate the loss of placenta in tiger sharks may be associated with subsequent adaptive changes in brain development and sperm production.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0696-y) contains supplementary material, which is available to authorized users.

Highlights

  • All vertebrates initially feed their offspring using yolk reserves

  • We aimed to identify orthologous genes among the transcriptomes of the nine species and determine if there is evidence of genes evolving under positive selection, and possibly associated with the loss of placenta in the tiger shark lineage

  • Sequencing We sequenced the transcriptomes of six placental carcharhinids and the non-placental tiger shark

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Summary

Introduction

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. 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. Viviparity is thought to have first evolved over 350 million years ago (mya), and is an unprecedented example of convergent evolution having independently evolved at least 150 times in mammals, reptiles, amphibians, and fishes [3, 4]. Among these viviparous organisms there are differences. These can be associated with variation in geographic distribution and environmental conditions, as documented in reptiles [8, 9] and amphibians [10]

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