Viviparity: The Maternal-Fetal Relationship in Fishes

Abstract

SYNOPSIS. Viviparity in the vertebrate line first makes its evolutionary appearance among fishes. It has independently evolved in a number of divergent piscine lineages. The 54 families of extant fishes that bear living young include 40 families of chondrichthyans (sharks and rays), one montypic family of coelacanths (Latimeria), and 13 families of teleosts. There is fossil evidence for viviparity in holocephalans and chondrosteans. Viviparity predominates among sharks and rays (40 families, 99 genera, 420 species) but is less widespread among teleosts (13 families, 122 genera, 510 species). Following an historical introduction, the organization of the female reproductive system, sites of gestation, developmental sequences and superfetation are considered. The evolution of viviparity establishes specialized maternal-fetal relationships, viz., 1) developmental, 2) morphological, 3) trophic, 4) osmoregulatory, 5) respiratory, 6) endocrinological, and 7) immunological. While the latter four categories are briefly noted the major emphasis is on the trophic relationship and its morphological and developmental basis. First, a general overview is presented and then the maternal-fetal trophic relationships in each of the major groups of fishes are systematically reviewed. Pertinent anatomical, histological, ultrastructural, developmental, physiological, and biochemical studies are considered. Viviparous fishes are either lecithotrophic, i.e., exclusively yolk dependent, or matrotrophic, i.e., in receipt of a continuous supply of maternal nutrients during gestation. Nutrient transfer is accomplished by 1) oophagy and adelphophagy, 2) placental analogues, and 3) the yolk sac placenta. Placental analogues include: external epithelial absorptive surfaces, e.g., skin, fins, gills; trophonemata, modifications of the uterine epithelia for the secretion of histotrophe or “uterine milk”; branchial placentae, close apposition between gill epithelia and either uterine or ovarian epithelial villi; the yolk sac; pericardial amnion and chorion; follicular pseudoplacenta, close apposition between follicle cells and embryonic absorptive epithelia; hypertrophied gut; and trophotaeniae, external rosette or ribbon-like projections of the embryonic gut. Among chondrichthyans, the yolk sac placenta (840–1,050%), trophonematal secretion and embryonic absorbtion of histotrophe (1,680–4,900%) and oophagy and adelphophagy (1.2 × 106%) are the most efficient methods of nutrient transfer. Among teleosts, the follicular pseudoplacenta (1,800–3,900%), trophotaeniae (8,400%) and absorption of ovarian histotrophe through surface epithelia and a hypertrophied gut (1,100–34,000%) are the most efficient. These values stand in contrast to the 30%40% loss of dry weight characteristic of oviparous fishes and viviparous lecithotrophes.