Facultative placentotrophy: half-way house or strategic solution?

Abstract

While yolk is generally the primary source of embryo nutrients in squamates, numerous species supplement this with facultative placentotrophy. We argue that facultative placentotrophy should have selective importance relevant to offspring fitness. In the skink Ni6eoscincus metallicus, the size of ovulated eggs is unrelated to maternal size but large females produce offspring that are larger than is necessary for survival, providing evidence for facultative placentotrophy. We discuss the circumstances in which facultative placentotrophy might be used to supplement the nutritional support provided by yolk and obligate placentotrophy in this species, and present summary data from experiments designed to investigate these circumstances. Clutch reduction by oviduct removal had no effect on neonate mass or snout-vent length, indicating that the number of embryos does not influence allocation of maternal resources once gestation has commenced. Manipulation of maternal basking opportunity in combination with food intake during pregnancy suggested that an important role of facultative placentotrophy is the optimization of embryonic fat reserves. This hypothesis was supported by the observation that larger neonates have larger abdominal fat bodies. These reserves presumably facilitate survival in the relatively short pre-hibernatory period available to newborn animals. Our data indicate that they also play a vital role in maintaining pre-natal condition if birth is delayed by adverse weather, a common circumstance in this species. In such circumstances the yolk has been used up and the placental membranes have degenerated. Experimental induction of premature ovulation of eggs with reduced yolk, achieved by injecting females with FSH, was followed by fertilization using stored sperm. Gestation length was greatly reduced and the resulting neonates were all 575% normal birth mass, with two of the six births being stillborn. Thus facultative placentotrophy does not appear to be a means of compensating for a poor yolk supply. We suggest that facultative placentotrophy in N. metallicus is not a transitional stage en route to greater reliance on obligate placentotrophy, but a uniquely squamate adaptation that provides flexibility in embryonic nutrition, and optimizes offspring fitness in an unpredictable temperate climate.