The yolkless egg and the evolution of eutherian viviparity.

Abstract

All vertebrate follicles have the same basic structure. Viviparity also occurs in all vertebrates except birds, but it is the only form of reproduction in eutherians ("placental mammals"). Their mature follicles are vesicular, and their oocytes are yolkless. Clues to the origin of these unique characteristics are in the incidence of atresia and the role of yolk in reproduction. In broadcast spawning, atresia is as rare as it is common among eutherians and other nonspawning vertebrates. In all but the eutherians, at least the initial-and in most cases all-stages of embryogenesis depend crucially on the zygote's yolk. Eutherian reproduction, therefore, must have evolved in connection with genetic changes that caused fragility of the oocyte, instability of the follicle, and loss of the ability to produce vitellogenin (VTG), the main lipoprotein of yolk. Mutations can result in adaptations by uncovering hidden properties in a trait and/or its environment. Useful mutations in recessive alleles can spread through a population as heterozygotes, invisible until the number of homozygotes for the mutation is large enough for them to suddenly appear and form the nucleus of a new breeding population. Such a mutation probably truncated a long, oviductal-based, aplacental gestation of a small, lightly yolked zygote in an endothermic, mammal-like reptile and converted it into an early monotreme or marsupial-like mammal (pantothere). Against tremendous odds, another mutation later caused loss of the genes for VTG. The resultant yolkless zygote survived because 1). the mutation also affected a network of homeiotic genes controlling the ontogeny of the entire reproductive system and 2). the system contained enough hidden properties for the mutation to change the character of the oocyte, its granulosa cells and corpus luteum, the zygote, and the uterus in a way that virtually assured the new zygote's survival. Eutherian reproduction, however, is neither better nor worse than other forms; it is only different.