Evidence of positive selection associated with placental loss in tiger sharks.
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.



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).



Our results indicate the loss of placenta in tiger sharks may be associated with subsequent adaptive changes in brain development and sperm production.
Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Berkshire, SL5 7PY, UK. dominic.swift@tamucc.edu.
Dominic G
DG
Swift
Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK.
Luke T
LT
Dunning
Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge, CB2 3EQ, UK.
Javier
J
Igea
Shark Research & Conservation Program, Cape Eleuthera Institute, PO Box EL - 26029, Eleuthera, the Bahamas.
Edward J
EJ
Brooks
Institute of Biological and Environmental Sciences, School of Biological Sciences, University of Aberdeen, Zoology Building, Tillydrone Avenue, Aberdeen, AB24 2TZ, Scotland, UK.
Catherine S
CS
Jones
Institute of Biological and Environmental Sciences, School of Biological Sciences, University of Aberdeen, Zoology Building, Tillydrone Avenue, Aberdeen, AB24 2TZ, Scotland, UK.
Leslie R
LR
Noble
Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Berkshire, SL5 7PY, UK.
Adam
A
Ciezarek
Department of Animal Behaviour, University of Bielefeld, Postfach 100131, 33501, Bielefeld, Germany.
Emily
E
Humble
Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Berkshire, SL5 7PY, UK. v.savolainen@imperial.ac.uk.
Vincent
0000-0001-5350-9984
V
Savolainen
D000818:Animals; D001483:Base Sequence; D005260:Female; D008297:Male; D010802:Phylogeny; D010920:Placenta; D011247:Pregnancy; D012098:Reproduction; D012641:Selection, Genetic; D012754:Sharks / Q000235:genetics / Q000502:physiology*; D059467:Transcriptome
Carcharhinids; Elasmobranchs; Galeocerdo; Placenta; Positive selection; RNA-Seq; Reproduction; Transcriptome; Viviparous