The evolution of amniote gastrulation: the blastopore‐primitive streak transition

Abstract

In the animal kingdom, gastrulation, the process by which the primary germ layers are formed involves a dramatic transformation in the topology of the cells that give rise to all of the tissues of the adult. Initially formed as a mono‐layer, this tissue, the epiblast, becomes subdivided through the internalization of cells, thereby forming a two (bi‐laminar) or three (tri‐laminar) layered embryo. This morphogenetic process coordinates the development of the fundamental body plan and the three‐body axes (antero‐posterior, dorso‐ventral, and left‐right) and begins a fundamental segregation of cells toward divergent developmental fates. In humans and other mammals, as well as in avians, gastrulating cells internalize along a structure, called the primitive streak, which builds from the periphery toward the center of the embryo. How these morphogenetic movements are orchestrated and evolved has been a question for developmental biologists for many years. Is the primitive streak a feature shared by the whole amniote clade? Insights from reptiles suggest that the primitive streak arose independently in mammals and avians, while the reptilian internalization site is a structure half‐way between an amphibian blastopore and a primitive streak. The molecular machinery driving primitive streak formation has been partially dissected using mainly the avian embryo, revealing a paramount role of the planar cell polarity (PCP) pathway in streak formation. How did the employment of this machinery evolve? The reptilian branch of the amniote clade might provide us with useful tools to investigate the evolution of the amniote internalization site up to the formation of the primitive streak. WIREs Dev Biol 2017, 6:e262. doi: 10.1002/wdev.262 This article is categorized under: Early Embryonic Development > Fertilization to Gastrulation Early Embryonic Development > Gastrulation and Neurulation Comparative Development and Evolution > Body Plan Evolution

Filling in the phylogenetic gaps: Induction, migration, and differentiation of neural crest cells in a squamate reptile, the veiled chameleon (Chamaeleo calyptratus)

“…Veiled chameleons ( Chamaeleo calyptratus ), however, provide a new squamate model that overcomes these limitations. At the time of oviposition, veiled chameleon embryos are pre‐gastrula in their development . In addition, veiled chameleon females produce large clutches of eggs (35‐90+) multiple times per year.…”

“…At the time of oviposition, veiled chameleon embryos are pre-gastrula in their development. [5][6][7][8][9][10] In addition, veiled chameleon females produce large clutches of eggs (35-90+) multiple times per year. Chameleons are an important example of how ecological specialization and selective pressure mediate morphological change.…”

On the origin of leeches by evolution of development

“…The PCT resulted from a change of habitat, whereas the OLT arose from a shift in feeding behavior. Major habitat changes have caused large‐scale modifications to embryonic development in many groups of animals, such as in the amniote vertebrates (Stower & Bertocchini, ), in the terrestrial arthropod groups and in the clitellate annelids (Anderson, ). However, with the exception of endoparasitism, changes in feeding behavior rarely evoke such a large‐scale reorganization of embryonic development.…”

On the Enigma of the Human Neurenteric Canal

“…DOI: 10.1159/000493276 the blastopore with its adjacent blastoporal lips in amphibia: both the neurenteric canal and the blastopore are in their cranial part associated with an involution-type cell movement for the formation of the notochordal plate, and this shows striking parallels in primates [this study], bats [van Beneden, 1888], reptiles [Bertocchini et al, 2013;Stower and Bertocchini, 2017], amphibia [Shook and Keller, 2008], and in a number of bird species (including the chick: Charrier et al [1999]; Tsikolia et al [2012]), some of which may also have a notochordal canal ("rudimentary Urdarm") or even a true neurenteric canal [Schauins land, 1903]; in the chick, however, a neurenteric canal next to the HINC-like cellular arrangement within the primitive node [Tsikolia et al, 2012] has not yet been reported. The primitive streak itself would, hence, represent a homologue of the lateral and ventral parts of the blastopore as described before (see Hertwig [1906] and references therein).…”

“…Blastopore and primitive streak have, therefore, repeatedly presented to be functional equivalents derived from a common ancestor and thus to be homologous structures [Arendt and Nübler-Jung, 1999]. A recent focus on reptiles, however, led to the proposal that the avian and the human primitive streak may have developed independently and that reptiles with their narrow canal-like blastopore, which runs more or less perpendicularly through the embryonic plate connecting the amniotic cavity with the yolk sac cavity [Bertocchini et al, 2013], may have an "intermediate blastopore" or "proto-streak" with crucial importance for gastrulation [Stower and Bertocchini, 2017].…”