Abstract

Polyspermy is a major puzzle in reproductive biology. In some taxa, multiple sperm enter the ovum as part of the normal fertilization process, whereas 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 fertilization 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 reach and penetrate the ovum, indicating that females compensate for low sperm numbers in the oviduct. Our results suggest a functional role for supernumerary sperm in the processes of fertilization and early embryogenesis, providing an exciting expansion of our understanding of sperm function in birds.

Highlights

  • Males typically inseminate many more sperm than females need to fertilize their ova

  • Ensuring that sufficient sperm are available for fertilization is important for birds, in which several sperm typically enter the ovum in a process known as physiological polyspermy [15]

  • We have shown that when female birds are inseminated with low sperm numbers, a greater number of sperm than expected reach and penetrate ova

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Summary

Introduction

Males typically inseminate many more sperm than females need to fertilize their ova. Insemination of high sperm numbers increases a male’s chance of success in sperm competition [1], but for females, high sperm numbers can be a problem; penetration by multiple sperm ( polyspermy) is potentially destructive to the ovum [2]. In vitro studies of fertilization in Japanese quail Coturnix japonica demonstrated that the amount of avian sperm extract (containing ovum-activating proteins) required for normal post-fertilization development is greater than can be provided by a single sperm [21]. This suggests that under natural conditions, a minimum number of sperm must enter the ovum to ensure zygote formation and development. Our results indicate that when inseminated sperm numbers are low, female birds compensate by allowing a greater proportion of sperm to reach the site of fertilization This ensures that sufficient supernumerary sperm enter the germinal disc, so that both fertilization and development proceed normally. Our results support the hypothesis that supernumerary sperm play an essential role in avian embryogenesis

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