Viviparity: The Maternal-Fetal Relationship in Fishes

SYNOPSIS. Viviparity in the vertebrate line first makes itsevolutionary appearance among fishes. It has independently evolvedin a number of divergent piscine lineages. The 54 families ofextant fishes that bear living young include 40 families ofchondrichthyans (sharks and rays), one montypic family of coelacanths(Latimeria), and 13 families of teleosts. There is fossil evidencefor viviparity in holocephalans and chondrosteans. Viviparitypredominates 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 ofgestation, developmental sequences and superfetation are considered.The evolution of viviparity establishes specialized maternal-fetalrelationships, viz., 1) developmental, 2) morphological, 3)trophic, 4) osmoregulatory, 5) respiratory, 6) endocrinological,and 7) immunological. While the latter four categories are brieflynoted the major emphasis is on the trophic relationship andits morphological and developmental basis. First, a generaloverview is presented and then the maternal-fetal trophic relationshipsin each of the major groups of fishes are systematically reviewed.Pertinent anatomical, histological, ultrastructural, developmental,physiological, and biochemical studies are considered. Viviparousfishes are either lecithotrophic, i.e., exclusively yolk dependent,or matrotrophic, i.e., in receipt of a continuous supply ofmaternal nutrients during gestation. Nutrient transfer is accomplishedby 1) oophagy and adelphophagy, 2) placental analogues, and3) the yolk sac placenta. Placental analogues include: externalepithelial absorptive surfaces, e.g., skin, fins, gills; trophonemata,modifications of the uterine epithelia for the secretion ofhistotrophe or "uterine milk"; branchial placentae, close appositionbetween gill epithelia and either uterine or ovarian epithelialvilli; the yolk sac; pericardial amnion and chorion; follicularpseudoplacenta, close apposition between follicle cells andembryonic absorptive epithelia; hypertrophied gut; and trophotaeniae,external rosette or ribbon-like projections of the embryonicgut. 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 x 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 surfaceepithelia and a hypertrophied gut (1,100–34,000%) arethe most efficient. These values stand in contrast to the 30%40%loss of dry weight characteristic of oviparous fishes and viviparouslecithotrophes.