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Background   Pregnancy-specific glycoprotein  ( PSG ) genes belong to the  carcinoembryonic antigen  ( CEA ) gene family, within the immunoglobulin gene superfamily. In humans, 10  PSG  genes encode closely related secreted glycoproteins. They are exclusively expressed in fetal syncytiotrophoblast cells and represent the most abundant fetal proteins in the maternal blood. In recent years, a role in modulation of the maternal immune system possibly to avoid rejection of the semiallogeneic fetus and to facilitate access of trophoblast cells to maternal resources via the blood system has been suggested. Alternatively, they could serve as soluble pathogen decoy receptors like other members of the CEA family. Despite their clearly different domain organization, similar functional properties have also been observed for murine and bat PSG. As these species share a hemochorial type of placentation and a seemingly convergent formation of  PSG  genes during evolution, we hypothesized that hemochorial placentae support the evolution of  PSG  gene families.    Results  To strengthen this hypothesis, we have analyzed  PSG  genes in 57 primate species which exhibit hemochorial or epitheliochorial placentation. In nearly all analyzed apes some 10  PSG  genes each could be retrieved from genomic databases, while 6 to 24  PSG  genes were found in Old World monkey genomes. Surprisingly, only 1 to 7  PSG  genes could be identified in New World monkeys. Interestingly, no PSG genes were found in more distantly related primates with epitheliochorial placentae like lemurs and lorises. The exons encoding the putative receptor-binding domains exhibit strong selection for diversification in most primate  PSG  as revealed by rapid loss of orthologous relationship during evolution and high ratios of nonsynonymous and synonymous mutations.    Conclusion  The distribution of trophoblast-specific PSGs in primates and their pattern of selection supports the hypothesis that PSG are still evolving to optimize fetal-maternal or putative pathogen interactions in mammals with intimate contact of fetal cells with the immune system of the mother like in hemochorial placentation.    Supplementary Information  The online version contains supplementary material available at 10.1186/s12864-021-07413-8.

The immune-modulating pregnancy-specific glycoproteins evolve rapidly and their presence correlates with hemochorial placentation in primates