, Volume 38, Issue 1-3, pp 269-294

Maximization of evolutionary trends for placental viviparity in the spadenose shark,Scoliodon taticaudus

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Synopsis

Placental viviparity has evolved inScoliodon taticaudus to a degree that rivals some eutherian mammals. Its eggs are the smallest known of any shark. They have a diameter of 1 mm, a dry weight of 0.0654 ± 0.0100 mg and are nearly yolk-free. Implantation takes place at an early (3 mm) stage of development, and gestation is short (5–6 months). Comparison of the dry weight of the egg (0.065 mg) with the estimated dry weights of a mid-late term 90 mm embryo (910 mg) and a 152 mm neonate (3815.4 mg) reveals weight changes of 14219 × and 58338 ×, respectively. Its normalized brood weight, a measure of maternal nutrient investment, is 49.5 g · kg−1 female body weight for a six-month gestation. Comparisons with other species of placental and nonplacental sharks show thatS. laticaudus has a highly advanced form of matrotrophy. Maternal nutrients appear to be acquired by placental transport and by imbibition of uterine fluid. Hemotrophic placental nutrient transfer occurs across a unique uterine implantation site, termed the trophonematous cup, in which maternal blood appears to bathe the outer epithelium of the embryonic yolksac placenta. The latter is solid and filled with a three-dimensional network of capillaries and many free interstitial cells. The umbilical stalk contains the vitelline vessels but lacks a yolk duct. Its surface is amplified by many long, villous appendiculae, which consist of a vascular core that ramifies into a massive surface capillary network invested by a simple squamous epithelium. The appendiculae ofS. laticaudus most likely are sites of gas exchange and possibly the uptake of small molecules. They are unlike the appendiculae described in any other placental shark and exhibit design principles similar to those of the uterine trophonemata of matrotrophic rays.