Placental specializations in lecithotrophic viviparous squamate reptiles

Abstract

Squamate reptiles have been thought to be predisposed to evolution of viviparity because embryos of most oviparous species undergo considerable development in the uterus prior to oviposition. A related hypothesis proposes that prolonged intrauterine gestation, an intermediate condition leading to viviparity, requires little or no physiological adjustment, other than reduction in thickness of the eggshell. This logical framework is often accompanied by an assumption that mode of parity (oviparity, viviparity) and pattern of embryonic nutrition (lecithotrophy, placentotrophy) are independent traits that evolve in sequence. Thus, specializations for viviparity should be absent in some lecithotrophic viviparous species. Studies of species of lizards with geographic variation in mode of parity challenge this scenario by demonstrating that placental specializations are correlated with viviparity. Uterine specializations for placental transport of calcium to viviparous embryos alter uterine physiology compared to oviparous females. In addition, comparative studies of oviparous and viviparous species, i.e., in which gene flow is disrupted, reveal that both uterine and embryonic structural modifications are commonly associated with viviparity, suggesting relatively rapid evolution of placental specializations. Studies of squamate reproductive biology support two hypotheses: 1) evolution of viviparity requires physiological adjustments of the uterine environment, and 2) evolution of viviparity promotes relatively rapid adaptations for placentation. Models for the evolution of viviparity from oviparity, or for reversals from viviparity to oviparity, should reflect current understanding of squamate reproductive biology and future studies should be designed to challenge these models.

The evolution of the placenta

“…Although estimated by some to have arisen independently more than one hundred times, it is conceivable that there was a single origin of viviparity and multiple subsequent reversions to oviparity (Blackburn 2015, Pyron and Burbrink 2014, Van Dyke, et al 2014). In many species, the embryo, relies on egg contents for nutrition, but, in others, a range of adaptations of the female reproductive tract provides a means to exchange gases and nutrients with the conceptus (Stewart 2015). In squamates the placenta is chorioallantoic, but unlike in mammals, does not develop from an early arising, extraembryonic, trophoblast layer.…”

“…In squamates the placenta is chorioallantoic, but unlike in mammals, does not develop from an early arising, extraembryonic, trophoblast layer. Most squamate placentas demonstrate a simple interdigitation of the chorioallantois with the uterine epithelium (Stewart 2015), but in some skinks the interface is more intimate (Fig. 1).…”

Advancing perspectives on parity‐mode evolution

“…When we submitted our manuscript (Pyron and Burbrink, 2014) on 2 May 2013, I did not anticipate how controversially it would be received, or the magnitude of the response. Articles in this issue (Blackburn, 2015a,b;Duchêne and Lanfear, 2015;Griffith et al, 2015;King and Lee, 2015b;Shine, 2015;Stewart, 2015;Wright et al, 2015) and in other journals (King and Lee, 2015a) have re-examined our data, analyses, and conclusions, drawing a wide range of inferences. Our summary (Pyron and Burbrink, 2015) was written before any of the responses appeared, and merely gives an overview of our original conclusions, with some suggestions for future research.…”

Evolutionary origins of viviparity in Chamaeleonidae

“…A large-scale comparative approach in chameleons, akin to what we have done in this paper for reproductive modes, will help to elucidate the ecological and evolutionary circumstances under which pigmentation of the body cavity has evolved (e.g., Greene & Burghardt, 1978). Chamaeleonidae, in turn, represents an excellent model to test exaptation hypotheses regarding the morphological, physiological and genetic changes that take place during the transition from egg-laying to live-bearing reproduction (Andrews, 2000;Andrews & Mathies, 2000;Blackburn, 1995Blackburn, , 2006Blackburn, , 2015bGriffith et al, 2015;Griffith, Brandley, Belov, & Thompson, 2016;Shine, 2015;Stewart, 2015;Thompson, Stewart, Speake, Hosie, & Murphy, 2002;Van Dyke, Brandley, & Thompson, 2014;Van Dyke & Griffith, 2018). Our results align with the recent body of literature that has coalesced around chameleons as an emerging model system for understanding the evolution of vertebrate reproduction and development (Andrews, 2007(Andrews, , 2008a(Andrews, , 2008bDíaz et al, 2015Díaz et al, , 2017.…”