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

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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.

LanguageEnglish
Article number156
JournalBMC Evolutionary Biology
Volume19
DOIs
Publication statusPublished - 26 Jul 2019

Fingerprint

placenta
vertebrate
genome
vertebrates
gene
fish
genes
Poeciliidae
cell proliferation
gene duplication
Heterandria formosa
natural selection
phenotypic variation
genomics
mammal
mammals
nucleotide sequences
nutrient
nutrients
tissues

Keywords

  • Gene duplication
  • Heterandria formosa
  • Matrotrophy
  • Molecular evolution
  • Placenta
  • Poeciliidae
  • Positive selection
  • Whole genome sequencing

Cite this

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title = "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. 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.",
keywords = "Gene duplication, Heterandria formosa, Matrotrophy, Molecular evolution, Placenta, Poeciliidae, Positive selection, Whole genome sequencing",
author = "{Van Kruistum}, Henri and {Van Den Heuvel}, Joost and Joseph Travis and Ken Kraaijeveld and Zwaan, {Bas J.} and Groenen, {Martien A.M.} and Megens, {Hendrik Jan} and Pollux, {Bart J.A.}",
year = "2019",
month = "7",
day = "26",
doi = "10.1186/s12862-019-1484-2",
language = "English",
volume = "19",
journal = "BMC Evolutionary Biology",
issn = "1471-2148",
publisher = "Springer Verlag",

}

TY - JOUR

T1 - The genome of the live-bearing fish Heterandria formosa implicates a role of conserved vertebrate genes in the evolution of placental fish

AU - Van Kruistum, Henri

AU - Van Den Heuvel, Joost

AU - Travis, Joseph

AU - Kraaijeveld, Ken

AU - Zwaan, Bas J.

AU - Groenen, Martien A.M.

AU - Megens, Hendrik Jan

AU - Pollux, Bart J.A.

PY - 2019/7/26

Y1 - 2019/7/26

N2 - 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.

AB - 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.

KW - Gene duplication

KW - Heterandria formosa

KW - Matrotrophy

KW - Molecular evolution

KW - Placenta

KW - Poeciliidae

KW - Positive selection

KW - Whole genome sequencing

U2 - 10.1186/s12862-019-1484-2

DO - 10.1186/s12862-019-1484-2

M3 - Article

VL - 19

JO - BMC Evolutionary Biology

T2 - BMC Evolutionary Biology

JF - BMC Evolutionary Biology

SN - 1471-2148

M1 - 156

ER -