A developmental synapomorphy of squamate reptiles

Abstract

The reptilian clade Squamata is defined primarily by osteological synapomorphies, few of which are entirely unambiguous. Studies of developing squamate eggs have revealed a uniquely specialized feature not known to occur in any other amniotes. This feature-the yolk cleft/isolated yolk mass complex-lines the ventral hemisphere of the egg. During its formation, extraembryonic mesoderm penetrates the yolk and an exocoelom (the yolk cleft [YC]) forms in association with it, cutting off a thin segment of yolk (the "isolated yolk mass" [IYM]) from the main body of the yolk. The YC-IYM complex has been observed and described in more than 65 squamate species in 12 families. In viviparous species, it contributes to the "omphaloplacenta," a type of yolk sac placenta unique to squamates. The only squamates known to lack the IYM are a few highly placentotrophic skinks with minuscule eggs, viviparous species in which it clearly has been lost. Given its absence in mammals, chelonians, crocodylians, and birds, the YC-IYM complex warrants recognition as a developmental synapomorphy of the squamate clade. As in extant viviparous lizards and snakes, the YC-IYM complex presumably contributed to the placenta of extinct viviparous squamates. K E Y W O R D Sisolated yolk mass, lizards, snakes, yolk cleft Daniel G. Blackburn and James R. Stewart contributed equally and should be considered joint senior authors.

Developmental morphology and evolution of extraembryonic membranes of lizards and snakes (Reptilia, Squamata)

“…The function of the yolk cleft/isolated yolk mass complex is unknown. It is a shared derived trait for Squamata, or perhaps Lepidosauria, and likely has been retained in all oviparous squamates (Stewart & Blackburn, 2019). Development of the tissue is known only from histological descriptions of the species included in this review.…”

“…In contrast, development of the yolk sac in the lower, abembryonic hemisphere of the egg produces structures, the yolk cleft/isolated yolk mass complex, unique to squamates (Figure 1a–d; Stewart, 1997; Stewart & Blackburn, 2019). The yolk cleft is a cavity surrounded by yolk that develops within a sheet of mesoderm, intravitelline mesoderm, which has grown into the abembryonic region of the yolk sac cavity (Figure 2).…”

“…The outer allantoic membrane fuses with the chorion forming the vascular chorioallantoic membrane that advances outward from the embryo as the chorion separates from the vascular trilaminar yolk sac. Phylogenetic variation arises in growth of the chorion and expansion of the allantois in the abembryonic hemisphere of the egg as either a response to non‐yolk egg contents, that is, albumen in turtles and birds (Duval, 1884; Hamilton, 1952; Mitsukuri, 1891), or variation in growth of mesoderm in squamates (Stewart & Blackburn, 2019). Nonetheless, by late stages of embryonic growth a chorioallantoic membrane surrounds nearly all the egg contents in all oviparous reptiles.…”

“…Consequently, developmental morphology of extraembryonic membranes of oviparous species has received little attention and there is limited understanding of evolutionary patterns. Nonetheless, there are distinctive characteristics of development of oviparous squamates that challenge conventional understanding of the evolution of the egg of amniotes (Elinson & Stewart, 2014; Elinson, Stewart, Bonneau, & Blackburn, 2014; Powers & Blackburn, 2017a, 2017b; Stewart & Blackburn, 2019). In addition to contributions to broad phylogenetic patterns, an understanding of oviparous eggs is a prelude to deciphering attributes that contribute to reproductive diversity.…”

How do Crocodylian embryos process yolk? Morphological evidence from the American alligator,Alligator mississippiensis

“…For example, sauropsid species show striking differences in such fundamental features as gastrulation and primitive streak formation (Stower et al, 2015; Stower & Bertocchini, 2017). Likewise, aspects of yolk sac development differ markedly between squamates (lizards and snakes) and other sauropsids (Stewart, 1997; Stewart & Blackburn, 2019). Patterns of neural crest development also vary (Diaz Jr., Shylo, Roellig, Bronner, & Trainor, 2019; Goldberg et al, 2020), emphasizing the need to explore non‐avian animal models (Diaz Jr. et al, 2015).…”