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From PPROM to caul: The evolution of membrane rupture in mammals ☆

View Article: PubMed Central - PubMed

ABSTRACT

Rupture of the extraembryonic membranes that form the gestational sac in humans is a typical feature of human parturition. However, preterm premature rupture of membranes (PPROM) occurs in approximately 1% of pregnancies, and is a leading cause of preterm birth. Conversely, retention of an intact gestational sac during parturition in the form of a caul is a rare occurrence. Understanding the molecular and evolutionary underpinnings of these disparate phenotypes can provide insight into both normal pregnancy and PPROM. Using phylogenetic techniques we reconstructed the evolution of the gestational sac phenotype at parturition in 55 mammal species representing all major viviparous mammal groups. We infer the ancestral state in therians, eutherians, and primates, as in humans, is a ruptured gestational sac at parturition. We present evidence that intact membranes at parturition have evolved convergently in diverse mammals including horses, elephants, and bats. In order to gain insight into the molecular underpinnings of the evolution of enhanced membrane integrity we also used comparative genomics techniques to reconstruct the evolution of a subset of genes implicated in PPROM, and find that four genes (ADAMTS2, COL1A1, COL5A1, LEPRE1) show significant evidence of increased nonsynonymous rates of substitution on lineages with intact membranes as compared to those with ruptured membranes. Among these genes, we also discovered that 17 human SNPs are associated with or near amino acid replacement sites in those mammals with intact membranes. These SNPs are candidate functional variants within humans, which may play roles in both PPROM and/or the retention of the gestational sac at birth.

No MeSH data available.


Related in: MedlinePlus

Evolution of intact and ruptured gestational sacs at parturition. Reconstruction of the evolution of the gestational sac at parturition on a phylogenetic tree of 55 mammal species from 12 orders using maximum parsimony. Blue = species with intact membranes; green = partially intact; black = ruptured membrane at birth; Pac. wh.-sided dolphin = Pacific white-sided dolphin.
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f0010: Evolution of intact and ruptured gestational sacs at parturition. Reconstruction of the evolution of the gestational sac at parturition on a phylogenetic tree of 55 mammal species from 12 orders using maximum parsimony. Blue = species with intact membranes; green = partially intact; black = ruptured membrane at birth; Pac. wh.-sided dolphin = Pacific white-sided dolphin.

Mentions: We mapped the presence of an intact gestational sac on a tree of 55 species spanning the phylogenetic breadth of therian mammals (Fig. 2). We infer that a ruptured gestational sac upon birth is ancestral for therian and eutherian mammals. Based on the data here, we infer that an intact or partially intact sac evolved a minimum of 13 and a maximum of 16 times in mammals. In addition, parturition with purely intact membranes has evolved independently at least eight times. A ruptured gestational sac is ancestral for primates, and all primates with the exception of humans in caul are born with a ruptured sac. Humans are coded here for a sac that is both ruptured and partially intact (although partially intact membranes are rare in humans). A partially intact or intact gestational sac is a consistent feature of the Ruminantia within the order Cetartiodactyla, and is inferred as the ancestral state of this clade.


From PPROM to caul: The evolution of membrane rupture in mammals ☆
Evolution of intact and ruptured gestational sacs at parturition. Reconstruction of the evolution of the gestational sac at parturition on a phylogenetic tree of 55 mammal species from 12 orders using maximum parsimony. Blue = species with intact membranes; green = partially intact; black = ruptured membrane at birth; Pac. wh.-sided dolphin = Pacific white-sided dolphin.
© Copyright Policy - CC BY-NC-ND
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5121252&req=5

f0010: Evolution of intact and ruptured gestational sacs at parturition. Reconstruction of the evolution of the gestational sac at parturition on a phylogenetic tree of 55 mammal species from 12 orders using maximum parsimony. Blue = species with intact membranes; green = partially intact; black = ruptured membrane at birth; Pac. wh.-sided dolphin = Pacific white-sided dolphin.
Mentions: We mapped the presence of an intact gestational sac on a tree of 55 species spanning the phylogenetic breadth of therian mammals (Fig. 2). We infer that a ruptured gestational sac upon birth is ancestral for therian and eutherian mammals. Based on the data here, we infer that an intact or partially intact sac evolved a minimum of 13 and a maximum of 16 times in mammals. In addition, parturition with purely intact membranes has evolved independently at least eight times. A ruptured gestational sac is ancestral for primates, and all primates with the exception of humans in caul are born with a ruptured sac. Humans are coded here for a sac that is both ruptured and partially intact (although partially intact membranes are rare in humans). A partially intact or intact gestational sac is a consistent feature of the Ruminantia within the order Cetartiodactyla, and is inferred as the ancestral state of this clade.

View Article: PubMed Central - PubMed

ABSTRACT

Rupture of the extraembryonic membranes that form the gestational sac in humans is a typical feature of human parturition. However, preterm premature rupture of membranes (PPROM) occurs in approximately 1% of pregnancies, and is a leading cause of preterm birth. Conversely, retention of an intact gestational sac during parturition in the form of a caul is a rare occurrence. Understanding the molecular and evolutionary underpinnings of these disparate phenotypes can provide insight into both normal pregnancy and PPROM. Using phylogenetic techniques we reconstructed the evolution of the gestational sac phenotype at parturition in 55 mammal species representing all major viviparous mammal groups. We infer the ancestral state in therians, eutherians, and primates, as in humans, is a ruptured gestational sac at parturition. We present evidence that intact membranes at parturition have evolved convergently in diverse mammals including horses, elephants, and bats. In order to gain insight into the molecular underpinnings of the evolution of enhanced membrane integrity we also used comparative genomics techniques to reconstruct the evolution of a subset of genes implicated in PPROM, and find that four genes (ADAMTS2, COL1A1, COL5A1, LEPRE1) show significant evidence of increased nonsynonymous rates of substitution on lineages with intact membranes as compared to those with ruptured membranes. Among these genes, we also discovered that 17 human SNPs are associated with or near amino acid replacement sites in those mammals with intact membranes. These SNPs are candidate functional variants within humans, which may play roles in both PPROM and/or the retention of the gestational sac at birth.

No MeSH data available.


Related in: MedlinePlus