The placenta is the unique organ of therian mammals, key to their evolution and viability. The chorion is the outermost of the extra-embryonic membranes, and in birds and reptiles it is a simple membrane in contact with the shell allowing gas exchange. But in eutherian mammals the chorion is highly vascularised by the allantois to form the placenta. While the placenta serves the common role in all eutherian mammals of supporting fetal nutrition and oxygenation, serving as the route to excretion and providing an immune barrier between the mother and fetus, there are enormous species differences in the structure of the placenta. A recent paper using a genomic approach (Knox and Baker, 2008) has explored the molecular basis of this divergence. In the mouse, although there is no obvious change in structure in midgestation there is a big shift in the pattern of gene expression. In early embryogenesis, placentally preferentially expressed genes are typified by an orthology with all eukaryotes; after midgestation there is a shift to preferential expression of genes that are rodent lineage-specific. Similarly, in the human, the pattern of gene expression in the term placenta is primate-specific, a finding also found in a separate study (Uddin et al., 2008). These studies suggest that the expression of several placental hormones shows adaptive evolution specific to the ape stem lineage. Thus it would appear that the molecular processes associated with early embryogenesis are well conserved, but in later gestation there has been active selection for lineage-specific patterns of gene expression which may relate to the very variable patterns of pregnancy across mammalia.
Recently the evolution of genomic imprinting has been examined (Edwards et al., 2007). While imprinted genes are not found in monotremes, birds or reptiles, they are found in both marsupial and eutherian mammals, suggesting that imprinting evolved in parallel with the evolution of placentation. The Edwards paper concludes that the imprinting of each imprinted gene/cluster evolved independently rather from a common ancestral locus or chromosome. Haig (1993) used parental imprinting to promote the hypothesis that there is a conflict between maternal and paternal interests in regulating the rate of fetal growth. He argued that the paternal drive was to promote fetal growth whereas maternally expressed alleles acted to limit fetal growth. The imprinted system he used to develop this hypothesis was the IGF-2 system; in the mouse IGF-2 is expressed from the paternal allele in fetal tissues, whereas the IGF-2 clearance receptor is expressed by the maternal allele in the placenta (Haig and Graham, 1991). However, IGF-2 receptors are not imprinted in all mammalian species (Monk et al., 2006). As Bateson has addressed in another recent EMR post, there are considerable difficulties with the underlying concept of a maternal-paternal conflict played out in the placental-fetal unit. Haig’s concept is considerably undermined by a recent and comprehensive review (Keverne and Curley, 2008) which focused on the molecular mechanisms underlying imprinting. They point out that while there are many mechanisms involved for different imprints, it is maternal processes that generally determine paternal gene expression in that there needs to be active silencing of the maternal allele. To quote: “Hence, if genes which extract resources from mother achieve paternal expression by the active process of maternal allele silencing, the question arises as to how natural selection might have initially operated at the maternal locus to effect the foetal-placental phenotype which is [if the conflict theory is accepted] disadvantageous to mothers.” (my own comment in italics). Indeed they illustrate their argument with examples of imprinted genes that suggest that they serve to support co-adaptation rather than conflict. This is a view that I would concur with. Other tecent studies of the evolution of placental biology within the primate lineage have also been interpreted as representing co-evolution rather than conflict (Pijnenborg et al., 2008).
While the literature abounds with reference to “conflict” operating in mammalian pregnancies, it is a concept that may be misleading and a terminology that should therefore be used with caution, if at all.
Edwards, C. A., Rens, W., Clarke, O. et al. (2007). The evolution of imprinting: chromosomal mapping of orthologues of mammalian imprinted domains in monotreme and marsupial mammals. BMC Evol Biol 7: 157. PMID: 17822525
Haig, D. (1993). Genetic conflicts in human pregnancy. Q Rev Biol 68: 495-532. PMID: 8115596
Haig, D., Graham, C. (1991). Genomic imprinting and the strange case of the insulin-like growth factor II receptor. Cell 64: 1045-46. PMID: 1848481
Keverne, E. B., Curley, J. P. (2008). Epigenetics, brain evolution and behaviour. Front Neuroendocrinol 29: 398-412. PMID: 18439660
Knox, K., Baker, J. C. (2008). Genomic evolution of the placenta using co-option and duplication and divergence. Genome Res 18: 695-705. PMID: 18340042
Monk, D., Arnaud, P., Apostolidou, S. et al. (2006). Limited evolutionary conservation of imprinting in the human placenta. Proc Natl Acad Sci USA 103: 6623-28. PMID: 16614068
Pijnenborg, R., Vercruysse, L., Hanssens, M. (2008). Fetal-maternal conflict, trophoblast invasion, preeclampsia, and the red queen. Hypertension Pregnancy 27: 183-96. PMID: 18484423
Uddin, M., Goodman, M., Erez, O. et al. (2008). Distinct genomic signatures of adaptation in pre- and postnatal environments during human evolution. Proc Natl Acad Sci USA 105: 3215-20. PMID: 18305157