The genome of the live-bearing fish Heterandria formosa implicates a role of conserved vertebrate genes in the evolution of placental fish
Abstract 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....
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doaj-458ab8ed25c445a39df0c73da719a4b42021-09-02T12:41:40ZengBMCBMC Evolutionary Biology1471-21482019-07-0119111110.1186/s12862-019-1484-2The genome of the live-bearing fish Heterandria formosa implicates a role of conserved vertebrate genes in the evolution of placental fishHenri van Kruistum0Joost van den Heuvel1Joseph Travis2Ken Kraaijeveld3Bas J. Zwaan4Martien A. M. Groenen5Hendrik-Jan Megens6Bart J. A. Pollux7Animal Breeding and Genomics Group, Wageningen UniversityPlant Sciences Group, Laboratory of Genetics, Wageningen UniversityDepartment of Biological Science, Florida State UniversityInstitute for Biodiversity and Ecosystem Dynamics, University of AmsterdamPlant Sciences Group, Laboratory of Genetics, Wageningen UniversityAnimal Breeding and Genomics Group, Wageningen UniversityAnimal Breeding and Genomics Group, Wageningen UniversityExperimental Zoology Group, Wageningen UniversityAbstract 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 live-bearing 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 non-placental 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.http://link.springer.com/article/10.1186/s12862-019-1484-2Heterandria formosaPoeciliidaePlacentaMatrotrophyPositive selectionGene duplication |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Henri van Kruistum Joost van den Heuvel Joseph Travis Ken Kraaijeveld Bas J. Zwaan Martien A. M. Groenen Hendrik-Jan Megens Bart J. A. Pollux |
spellingShingle |
Henri van Kruistum Joost van den Heuvel Joseph Travis Ken Kraaijeveld Bas J. Zwaan Martien A. M. Groenen Hendrik-Jan Megens Bart J. A. Pollux The genome of the live-bearing fish Heterandria formosa implicates a role of conserved vertebrate genes in the evolution of placental fish BMC Evolutionary Biology Heterandria formosa Poeciliidae Placenta Matrotrophy Positive selection Gene duplication |
author_facet |
Henri van Kruistum Joost van den Heuvel Joseph Travis Ken Kraaijeveld Bas J. Zwaan Martien A. M. Groenen Hendrik-Jan Megens Bart J. A. Pollux |
author_sort |
Henri van Kruistum |
title |
The genome of the live-bearing fish Heterandria formosa implicates a role of conserved vertebrate genes in the evolution of placental fish |
title_short |
The genome of the live-bearing fish Heterandria formosa implicates a role of conserved vertebrate genes in the evolution of placental fish |
title_full |
The genome of the live-bearing fish Heterandria formosa implicates a role of conserved vertebrate genes in the evolution of placental fish |
title_fullStr |
The genome of the live-bearing fish Heterandria formosa implicates a role of conserved vertebrate genes in the evolution of placental fish |
title_full_unstemmed |
The genome of the live-bearing fish Heterandria formosa implicates a role of conserved vertebrate genes in the evolution of placental fish |
title_sort |
genome of the live-bearing fish heterandria formosa implicates a role of conserved vertebrate genes in the evolution of placental fish |
publisher |
BMC |
series |
BMC Evolutionary Biology |
issn |
1471-2148 |
publishDate |
2019-07-01 |
description |
Abstract 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 live-bearing 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 non-placental 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. |
topic |
Heterandria formosa Poeciliidae Placenta Matrotrophy Positive selection Gene duplication |
url |
http://link.springer.com/article/10.1186/s12862-019-1484-2 |
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