The genome of the live-bearing fish Heterandria formosa implicates a role of conserved vertebrate genes in the evolution of placental fish

Background: The evolution of complex organs is thought to occur via a stepwise process, each subsequent step
increasing the organ’s complexity by a tiny amount. This evolutionary process can be studied by comparing closely
related species that vary in the presence or absence of their organs. This is the case for the placenta in the livebearing fish family Poeciliidae, as members of this family vary markedly in their ability to supply nutrients to their
offspring via a placenta. Here, we investigate the genomic basis underlying this phenotypic variation in Heterandria
formosa, a poeciliid fish with a highly complex placenta. We compare this genome to three published reference
genomes of non-placental poeciliid fish to gain insight in which genes may have played a role in the evolution of
the placenta in the Poeciliidae.

Results: We sequenced the genome of H. formosa, providing the first whole genome sequence for a placental
poeciliid. We looked for signatures of adaptive evolution by comparing its gene sequences to those of three nonplacental live-bearing relatives. Using comparative evolutionary analyses, we found 17 genes that were positively
selected exclusively in H. formosa, as well as five gene duplications exclusive to H. formosa. Eight of the genes
evolving under positive selection in H. formosa have a placental function in mammals, most notably endometrial
tissue remodelling or endometrial cell proliferation.

Conclusions: Our results show that a substantial portion of positively selected genes have a function that
correlates well with the morphological changes that form the placenta of H. formosa, compared to the
corresponding tissue in non-placental poeciliids. These functions are mainly endometrial tissue remodelling and
endometrial cell proliferation. Therefore, we hypothesize that natural selection acting on genes involved in these
functions plays a key role in the evolution of the placenta in H. formosa.