Ontogeny, Genetic Control, and Phylogeny of Female Reproduction in Monotreme and Therian Mammals

Overview

In all living groups of mammals, prolonged protection of the developing young is a characteristic strategy of reproduction. Lactation, however, is the only uniquely mammalian characteristic, and all three groups have characteristic adaptations for achieving the transfer of energy from mother to young first via the uterus and placenta, and subsequently via the milk.

In mammals the simple oviduct of lower vertebrates has differentiated into the uterus and vagina. There is a tendency toward fusion of the posterior end of the paired oviducts. The vagina remains paired in monotremes and marsupials, but is a single fused tube in all eutherians; the uterus may be paired, partly fused, or completely fused as in humans. This fusion occurs independently in unrelated mammalian families as a correlate of reduction in litter size. The relative position of the ureters and the genital ducts is the character that most clearly separates the major groups of living mammals. The ureters of monotremes open into the urogenital sinus opposite the urethral openings of the bladder. In therians, the ureters migrate from a dorsal position adjacent to the Wolffian duct to a direct connection to the bladder, but the ureters pass medially between the genital duct in marsupials, not laterally as in eutherians. The conclusion must be that the original selection for the migration of the urinary ducts to the bladder in therian mammals was for an excretory and not a reproductive function, though the subsequent consequences for the development of the reproductive tract were profound. This is a true dichotomy, and allows for no intermediate stage.

When the reproductive processes of the three major groups of mammals are compared, many features emerge as synapomorphies. Examples are the Graafian follicles, functional corpora lutea, bilaminar blastocysts, uterine secretion, yolk sac placentae, mammary glands, and lactation. Although monotremes retain some plesiomorphic characters (e.g, egg laying), which show an early divergence from the stock leading to therians, comparisons between marsupials and eutherians suggest a dichotomy in development from a common ancestral group not a derivation of one from the other. Most of the apomorphic therian characters of marsupial reproduction are associated with the greater emphasis on lactation rather than gestation.

There appears to be a major dichotomy in the control of sexual differentiation in therian mammals. In eutherians, the sexual development of the male and female reproductive tracts has been assumed to be solely the result of the presence or absence of hormones secreted by the fetal testis, but in marsupials, several sexually dimorphic characters (the scrotum, mammary anlagen, gubernaculum, and processus vaginalis) are under direct genetic control. It now appears that certain sexual dimorphisms are also under direct genetic control in eutherians.

Tyndale-Biscoe and Renfree (1987) suggested that the basic mode of mammalian reproduction evolved simultaneously with the origin of mammals in the Triassic, but remained almost unchanged until the late Mesozoic because it was the most appropriate mode for small nocturnal insectivorous mammals. Tyndale-Biscoe and Renfree (1987) have further suggested that the present-day differences appear to have evolved during the adaptive radiation of the therian mammals in response to the metabolic requirement of increasing body size and the constraints imposed as these mammals moved into new ecological niches. Recent comparative studies detailed here on the anatomy and physiology of marsupials support these ideas.