Stable isotope tracer reveals that viviparous snakes transport amino acids to offspring during gestation

Abstract

SUMMARY Viviparity and placentation have evolved from oviparity over 100 times in squamate reptiles (lizards and snakes). The independent origins of placentation have resulted in a variety of placental morphologies in different taxa, ranging from simple apposition of fetal and maternal tissues to endotheliochorial implantation that is homoplasious with mammalian placentation. Because the eggs of oviparous squamates transport gases and water from the environment and calcium from the eggshell, the placentae of viviparous squamates are thought to have initially evolved to accomplish these functions from within the maternal oviduct. Species with complex placentae have also been shown to rely substantially, or even primarily, on placental transport of organic nutrients for embryonic nutrition. However, it is unclear whether species with only simple placentae are also capable of transporting organic nutrients to offspring. Among viviparous squamates, all of the snakes that have been studied thus far have been shown to have simple placentae. However, most studies of snake placentation are limited to a single lineage, the North American Natricinae. We tested the abilities of four species of viviparous snakes – Agkistrodon contortrix (Viperidae), Boa constrictor (Boidae), Nerodia sipedon (Colubridae: Natricinae) and Thamnophis sirtalis (Colubridae: Natricinae) – to transport diet-derived amino acids to offspring during gestation. We fed [15N]leucine to pregnant snakes, and compared offspring 15N content with that of unlabeled controls. Labeled females allocated significantly more 15N to offspring than did controls, but 15N allocation did not differ among species. Our results indicate that viviparous snakes are capable of transporting diet-derived amino acids to their offspring during gestation, possibly via placentation.

Unlike most vipers, female rattlesnakes (Crotalus atrox) continue to hunt and feed throughout pregnancy

“…However, once thought to be trivial, innovative research over the past 20 years has radically altered dogmatic views regarding placental complexity and nutrient transfer in squamates, especially in several groups of scincid lizards (Thompson & Speake, ; Blackburn & Stewart, ; Murphy & Thompson, ; Blackburn & Flemming, ). In snakes, studies on viviparous species imply a greater role of the placenta with respect to the transfer of energy and nutrients to fetuses (Stewart et al ., ; Blackburn & Stewart, ), including amino acids (Van Dyke & Beaupre, ). Our results here suggest a more complex relationship than capital mode alone (Taylor & DeNardo, ; Taylor et al ., ; Schuett et al ., ), and it is plausible that reproduction in a given season is simultaneously fueled by both stored and current sources of energy and nutrients (Winne et al ., ; Stephens et al ., ; Van Dyke & Beaupre, ).…”

“…In snakes, studies on viviparous species imply a greater role of the placenta with respect to the transfer of energy and nutrients to fetuses (Stewart et al ., ; Blackburn & Stewart, ), including amino acids (Van Dyke & Beaupre, ). Our results here suggest a more complex relationship than capital mode alone (Taylor & DeNardo, ; Taylor et al ., ; Schuett et al ., ), and it is plausible that reproduction in a given season is simultaneously fueled by both stored and current sources of energy and nutrients (Winne et al ., ; Stephens et al ., ; Van Dyke & Beaupre, ). Nevertheless, the role of the placenta in nutrient transfer in C. atrox and other rattlesnake species is not known and remains to be tested.…”

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.…”

Viviparous placentotrophy in reptiles and the parent–offspring conflict

“…These values are equivalent to those of oviparous squamates. Nevertheless, during gestation, placental membranes commonly provide water, calcium, and at least small quantities of organic and other inorganic nutrients (Stewart and Castillo, '84;Stewart et al, '90, 2009Stewart et al, '90, , 2011Stewart and Thompson, 2000;Thompson et al, 2001aThompson et al, , 2001bJones and Swain, 2006;Stewart and Ecay, 2010;van Dyke and Beaupre, 2012). Limited placental provision of nutrients has been called "incipient placentotrophy" (Blackburn, '92, 2000) and can have a facultative component (Stewart, '89, '92, 2013;Jones, 2000a, 2000b;Jones and Swain, 2006).…”