Evolution of the Male Reproductive Tract in Modern Mammals

Evolutionarily, the ancestral stocks of eutherian and marsupial mammals are thought to have diverged about 130 million years ago (Lillegraven 1974, 1975). Despite this long era of separate development, the male reproductive systems in the two groups of mammals show some striking similarities, which indicates that they have probably evolved in response to similar selection pressures. I have already compared the process of sperm maturation in the possum with that found in the Eutheria, and I should like now to use this as a basis for speculation about those very selection pressures, concentrating on three main aspects of the male system, which seem to be most worthy of study: the thermoregulatory scrotum; the epididymis; the role of sperm production in mating systems.

The reasons for the evolution of a thermoregulatory scrotum are intriguing and elusive. Both marsupials and Eutheria show the tendency for testes to move into an outpouching of the peritoneum, yet this has obviously developed after divergence, for not all species develop a scrotum, and in those that do, there are fundamental embryological differences in the mode of descent between the two groups of mammals (Eckstein and Zuckerman 1956; Sharman 1970). Although there is little doubt that testicular function in those animals that have a scrotum is rapidly impaired by raising the testes to the temperature of the body, this may simply reflect secondary adaptation of testicular function to a lower temperature. Carrick and Setchell (1977) have surveyed a wide range of mammals with different degrees of elaboration of a scrotum, and have found little relationship between the effectiveness of spermatogenesis and testicular temperature. In view of this, attention has now swung away from the testis to the epididymis, and Glover (1973, 1974) and Bedford (1977) have examined in page 32 detail the possibility that a major factor in the evolution of the scrotum has been the need to provide a cool storage zone for the mature spermatozoa. It is noteworthy that the Terminal Segment (or cauda epididymidis) invariably lies in the coolest extremity of the scrotum. Although this idea clearly needs further study, it has nevertheless refreshed our interest in the selection pressures behind the evolution of the modern male tract.

When considering the epididymis, it is clear that again there are marked similarities between eutherian and marsupial mammals, although, as yet, data for marsupials are scanty. I have shown here that in the common brushtail possum, as in Eutheria, we can clearly identify an Initial Segment concerned with fluid resorption, a Middle Segment where spermatozoa complete maturation, and a Terminal Segment where the mature gametes are stored (Glover and Nicander 1971). The area in which the possum seems to be unique seems to be that of sperm maturation, for the degree of morphological modelling of the spermatozoa which occurs in the epididymis is much greater than that seen in Eutheria.

It is impossible to consider the factors behind the evolution of the scrotum and epididymis without studying the roles of those structures in sperm production. Yet, when we examine the facts of sperm production in mammals, we are confronted with what seems to be a paradox: males in general produce far more spermatozoa than are needed to effect fertilization, and yet the female tract has evolved a number of mechanisms designed to prevent too many spermatozoa from reaching the ova and thus increasing the risks of polyspermic fertilization (see Cohen 1969). What are the reasons for this seeming wastage of gametes? The answer most probably lies in the reproductive strategies evolved by males to ensure breeding success. Although an examination of the evolution of reproductive behaviour is beyond the scope of this article (see Wilson 1975), it is clear that the ability to produce extremely large numbers of spermatozoa must have been a successful trait in early mammals, otherwise it would not have persisted. In mammalian breeding systems, there is considerable division of labour between the sexes, with the females carrying the major energy-consuming tasks of gestation, lactation and caring for offspring (Dawkins 1976; Grodzinski 1975).

Clutton-Brock and Harvey (1978) have pointed out that in such breeding systems, the reproductive success of females is limited by the number of young they can produce, while the success of males is largely limited by competition between them to impregnate females. Thus, mammals on the whole tend to be page 33 polygynous rather than polyandrous, and competition between males tends to select not just for vigour in breeding behaviour, but also for the ability to produce large numbers of fertile spermatozoa. The energy demands of mammalian sperm production per se are not known, however they are probably minor in terms of overall energy budgets (Sadleir 1969). In contrast, female mammals invest a large proportion of their energy budget in breeding; small rodents, for example, need to increase metabolic effort by about 60% during gestation and lactation (Grodzinski 1975). In evolutionary terms, the advantages to males of producing large numbers of spermatozoa must have outweighed the disadvantages of 'wastage' of excess gametes.

If these suppositions are correct, then the need to produce excesses of spermatozoa must have placed increasing metabolic and mechanical demands upon the testis; demands accentuated by the increasing importance of the testis as an endocrine gland. These stresses could be eased, and sperm output maximized, if spermatozoa could be released from the testis shortly after the completion of meiosis, with a minimum of maturation. I suggest that the epididymis, in the evolution of modern mammals, played an increasingly important part in overseeing the final steps of sperm maturation; a maturation which, in turn, was becoming biochemically more complex as the spermatozoa faced the rigours of an extensive female tract designed for viviparity.

Viewed in this context, we can now see that the epididymis of the possum would appear to have assumed greater control over sperm maturation than in comparable eutherian mammals. Certainly the morphological changes are much more overt and dramatic, and this should ease the way for investigations into factors which control the process. A side issue of this observation is that the reproductive tract of the possum can in no way be considered 'primitive', for it may in some ways be even more complex than that of the supposedly more 'advanced' Eutheria. Whether or not the reproductive biology of marsupials is in general 'primitive' is still a matter of hot debate. Lillegraven (1975) inclines to the view that, in general, it is, or at least that it is less evolutionarily flexible than that developed by placental mammals. On the other hand, several recent authors have pointed out that in many ways, the marsupial pattern of viviparity, with a short gestation and long lactation, is a highly successful strategy which minimises risk to the mother and also makes best use of potentially variable supplies of nutrition (Gould 1977; Kirsch 1977; Parker 1977).

page 34

The suggestion that the marsupial epididymis may be relatively more important in sperm maturation than that of eutherian mammals is still only an hypothesis. In order to test it, there seem to be three main areas where research should be directed: first, the relative durations of spermatogenesis and sperm maturation; second, the biochemical changes occurring in the epididymal plasma around the maturing spermatozoa; and third, the nature of the changes in the spermatozoa and their control. Some data are already available to show that the timing of spermatogenesis and epididymal transit in marsupials may be comparable to that of Eutheria (Setchell and Carrick 1973; Carrick and Setchell 1977), but in general the field for experimentation is virtually untouched.