Although all domestic chicken breeds originate from their wild relatives, the red junglefowl, they have been selectively bred for high yields in egg or meat production， or both. Some breeds are highly efficient in egg production, while others perform poorly, due to long-term selection aimed for different purposes. Female primordial germ cells (PGCs) are the precursors of eggs and the population size of PGCs will ultimately determine ovarian reserve of hens. In this study, we observed that the layers exhibit greater proliferation capacity and a higher number of PGCs compared to the broilers before meiosis. By comparing the PGC transcriptomes between layers and broilers, we identified potential genes that regulate cell proliferation. We further confirmed that FOXO3 expression is higher in broilers, where it inhibits the PGC proliferation both in vivo and in vitro. However, in layers, the upstream BMP signaling stimulate the phosphorylation of AKT and suppress FOXO3 activity. Consequently, the elevated BMP signaling and reduced FOXO3 co-operatively promote more robust PGC proliferation in layers compared to broilers and result in a greater number of PGCs in layers. Our data not only reveal molecular mechanisms underlying PGC growth, but also provide new clues to improve the laying performance in chicken.