Transplacental nutrient transfer during gestation in the Andean lizard Mabuya sp. (Squamata, Scincidae)

Abstract

Mabuya skinks have the most specialized allantoplacenta and the greatest degree of placentotrophy known among the Reptilia. Their recently ovulated eggs are microlecithal (1-2 mm) and lack fatty yolk platelets; thus, virtually all of the nutrients for embryonic development must pass across the placenta. We quantified the net uptake of nutrients during gestation in an Andean population of Mabuya and compared these results with other matrotrophic skinks and eutherian mammals. Total dry and wet masses, ash and organic content, ions (calcium, potassium, sodium, magnesium, iron), lipids (cholesterol, vitamin E and fatty acids in the major lipid classes-triacylglycerol, phospholipids, cholesteryl ester, free fatty acids), nitrogen (an index of protein) were measured during the different developmental stages throughout gestation, and in neonates. A significant net uptake of inorganic and organic matter was found. This uptake begins slowly during early gestation but accelerates during the last third of gestation when the growth of the embryo is maximal and the allantoplacenta has developed its greatest complexity. The drastic reduction of egg size in this clade is related to the great reduction in the contribution of lecithotrophic nutrients to the embryo, an obligatory placentotrophy from early developmental stages, and the highest placental complexity known in the Reptilia. All of these features converge with features found in eutherian mammals.

The evolution of viviparity: molecular and genomic data from squamate reptiles advance understanding of live birth in amniotes

“…Radioactive and stable isotope tracer studies have documented transport of amino acids, fatty acids, or both, to the developing offspring in species with (Swain & Jones 1997, Jones & Swain 2006, Itonaga et al 2012 and without (Hoffman 1970, Veith 1974, Thompson 1977, Yaron 1977, Van Dyke & Beaupre 2012) complex placentation. In contrast, comparisons of mass composition between eggs and newborn offspring suggest that only species with complex placentae exhibit biologically meaningful transport of amino acids and lipids to offspring (Thompson et al 1999b, 1999c, 2001b, Flemming & Branch 2001, Ramirez-Pinilla 2006, Ramirez-Pinilla et al 2011, while species with simple placentae exhibit net reductions in amino acids and lipids during development (Thompson 1981, Stewart 1989, Blackburn 1994. Paradoxically, species with simple placentae exhibit placental transport of labelled organic nutrient tracers and yet they sustain a net loss of organic nutrients during development.…”

“…Because oviparous squamates utilize the eggshell as a source for 20-80% of their calcium demand (Packard & Packard 1988, Shadrix et al 1994, the loss of the eggshell in viviparous species compromises an important component of embryonic nutrition. As a result, viviparous squamates, even those that are primarily lecithotrophic, transport significant quantities of calcium across placentae during development (Thompson et al 1999b, 1999c, Ramirez-Pinilla 2006, Ramirez-Pinilla et al 2011, Stewart 2013. In oviparous species, calcium ATPase is upregulated in the uterus only during eggshell deposition ), but is upregulated throughout pregnancy in the viviparous skink, Pseudemoia spenceri (Fig.…”

“…1A, B and C). Placental transport of sodium and potassium has been reported from every viviparous species studied, regardless of reliance on placentotrophy (Hoffman 1970, Thompson 1982, Stewart 1989, Ramirez-Pinilla 2006, Ramirez-Pinilla et al 2011. In contrast, the only lecithotrophic species reported to exhibit magnesium transport thus far is Eulamprus tympanum (Thompson et al , 2001a.…”

A single origin of extreme matrotrophy in African mabuyine skinks

“…Skinks with extreme matrotrophy ovulate tiny eggs with yolk sacs that lack yolk mass and have fetal and maternal tissues in close contact which function in nutrient transfer [5,7,10,11,12,31]. These characteristics (i) may be shared, derived characters reflecting a single origin of extreme matrotrophy, (ii) may have evolved once in Neotropical Mabuyinae and separately in the ancestor of Lubuya and Eumecia or (iii) may have evolved independently in all three lineages.…”

“…Nutrient transfer is best understood for several species of Neotropical Mabuyinae that transport large amounts of water, ions, lipids and proteins to the embryo via the placenta and have tiny ovulated eggs indicative of little or no lecithotrophy [7,11,12]. Eumecia and T. ivensii also ovulate tiny eggs with little or no yolk mass, strongly suggesting extreme matrotrophy in each of these lineages [5,6,10].…”