Relevance of the regulation of the brain-placental axis to the nocturnal bottleneck of mammals

Evolutionary theory suggests that the ancestors of all placental animals were nocturnal. Visual perceptive function of mammalian brain has evolved extensively, but nearly 70 % of today's mammals are still nocturnal. While placental influence on brain development is known, if placenta plays a role in the visual perceptive function of mammalian brain remains untested. The present study aims to test this hypothesis. In this study, single-nuclei RNA sequencing was performed to identify genes expressed in the pig placenta and fetal brain, and then compared with the orthologous genes expressed in the placenta and fetal brain cells of mouse. Differential gene expression analysis was performed to identify placental genes regulated differentially between nocturnal and diurnal animals. Phylogenetic modeling was performed to test correlated evolution between placenta type, and the nocturnal or diurnal activity among different mammals. The results showed that genes differentially regulated in the fetal brain were related to visual perception whereas the placental genes were related to the nocturnal or diurnal activity in placental animals. Phylogenetic modeling of these genes in thirty-four diverse mammalian species showed evidence for evolutionary link between placenta and the nocturnal/diurnal activity in animals. The findings of this study suggest that the placenta plays a role in the evolution of visual perceptive function of brain to shape the nocturnal or diurnal activity of placental animals. •Single-nuclei gene expression profiles of pig placenta and fetal brain.•Comparative analysis of brain-placental axis between pig and mouse.•Visual perception genes differentially regulated between placenta and fetal brain.•Evidence for correlated evolution between placenta and animal activity.•Genes regulated in the placenta and fetal brain are differentially expressed in eye.