Polyspermy is a major puzzle in reproductive biology. In some taxa, multiple sperm enter the ovum as part of the normal fertilisation process, while in others, penetration of the ovum by more than one sperm is lethal. In birds, several sperm typically enter the germinal disc, yet only one fuses with the female pronucleus. It is unclear whether supernumerary sperm play an essential role in the avian fertilisation process and, if they do, how females regulate the progression of sperm through the oviduct to ensure an appropriate number reach the ovum. Here we show that when very few sperm penetrate the avian ovum, embryos are unlikely to survive beyond the earliest stages of development. We also show that when the number of inseminated sperm is limited, a greater proportion than expected progresses to the site of fertilisation, indicating that females compensate for low sperm numbers in the oviduct. Our results confirm an essential role for supernumerary sperm in the processes of fertilisation and early embryogenesis, providing an exciting expansion of our understanding of sperm function in birds.