Reflections on the Evolution of Piscine Viviparity (1992)

Viviparity first makes its evolutionary appearance within the craniate-vertebrate line among fishes. We estimate that it has independently evolved at least 42 times in five of the nine major groups of fishes. Viviparity is the dominant mode of reproduction among the cartilaginous sharks and rays, i.e., 55% of approximately 900 living species. It is less prevalent among the five major groups of bony fishes, i.e., 2–3% of an estimated 20,000 or more species. The evolution of viviparity from oviparity involves: 1) a shift from external to internal fertilization; 2) retention of embryos in the female reproductive system; 3) utilization of the ovaryor oviduct as sites of gestation; 4) structural and functional modification of the embryo and the female reproductive system and; 5) modification of extant endocrine mechanisms controlling reproduction. Viviparity offers selective advantages to parents and offspring, such as: 1) enhanced survival of offspring; 2) compensation for low fecundity; 3) amplification of reproductive niches to reduce competition; 4) exploitation of pelagic niches; 5) colonization of new habitats; and 6) increased energetic efficiency in viviparous matrotrophes. Its principal disadvantages include: 1) reduced fecundity; 2) cost to the female; and 3) risk of brood loss through maternal death. Acquisition of viviparityestablishes new maternal-embryonic relationships, namely: 1) trophic; 2) osmoregulatory and excretory; 3) respiratory; 4) endocrinological; and 5) immunological. In sharks, rays, and the coelacanth, gestation takes place in the oviduct, but in teleosts gestation occurs either in the ovarian follicle or ovarian lumen. The cystovarian teleostean ovary is hypothesized to function both as ovary and oviduct. Oviductal, ovarian lumenal, andfollicular epithelial cells are the maternal sites of metabolic exchange. Metabolic exchange inembryos takes place across the epithelia of the general body surface and its derivatives or across the gut epithelium and its derivatives. Four patterns of piscine placentation have evolved,namely: 1) yolk sac; 2) follicular; 3) branchial; and 4) trophotaenial placentae. The pericardial amniochorion, the embryonic portion of the follicular placenta, occurs in poeciliids and several other teleostean groups. Developmental, it is nearly identical to the anterior aminochorionic fold of tetrapod vertebrates. Trophotaeniae are external rosette or ribbon-like structuresthat have evolved in four orders of teleosts by heterochrony, i.e., accelerated outgrowth and differentiation of the embryonic hind gut. With the possible exception of the coelacanth, theyolk sac placenta occurs only in sharks. We estimate that it has independently evolved between 11 and 20 times. It displays considerable diversity. Evolution of the yolk sac placenta entails retention of the yolk sac and secondary differentiation of its distal portion for implantation and maternal tissue-embryonic tissue metabolic exchange and its proximal portion for oviductal fluid-embryonic tissue exchange. The yolk stalk lengthens, is modified into an umbilical stalk, and establishes a site of autotomy at the embryo-umbilical stalk junction. The lumenal wall of the oviduct becomes competent to function as a site of implantation.