The gametes of man and some other Eutheria have been manipulated successfully for practical reasons, but many gaps remain in our basic understanding of the way that they function. This situation stems not least from a failure to recognize the extent to which eutherian spermatozoa and eggs, and elements related to their operation, have come to differ from those of other groups. Novel features in the male that reflect this include a radical design of the sperm head with the acrosome seeming to function primarily in egg-coat binding rather than its lysis, a multifaceted post-testicular sperm maturation and an androgen/low-temperature-regulated system of sperm storage – both tied to the epididymis, a variable male accessory sex gland complex, and descent of the testis and epididymis to a scrotum. In the female, such novelties are represented in a need for sperm capacitation, in an unusual regulation of sperm transport within the oviduct, in the cumulus oophorus and character of the zona pellucida around the small egg, and in a unique configuration of gamete fusion.

The collective evidence now suggests that many of these features reflect a new fertilisation strategy or its consequences, with most being causally linked. One initial ‘domino’ in this regard appears to be the small yolkless state of the egg and its intolerance for polyspermy, as determinants of the unusual mode of oviductal sperm transport and possibly the existence and form of the cumulus oophorus. However, a particularly influential first ‘domino’ appears to be the physical character of the eutherian zona pellucida. This differs from the egg coats of other animal groups by virtue of a resilient elasticity and thickness. These qualities allow this primary and often only coat to stretch and so persist during later expansion of the blastocyst, usually until close to implantation. At the same time, the dimensions, physical character, and particularly the relative protease-insensitivity of the zona appear to have had profound effects on sperm form and function and, more indirectly, on sperm-related events in the male and the female tract. Marsupials display some similarities and also some strikingly different features, against which the enigmas of the eutherian situation can be evaluated.