Morphology of the avian yolk sac

Abstract

The avian yolk sac is a multifunctional extraembryonic organ that serves not only as a site of nutrient (yolk) absorption, but also for early hemopoiesis, and formation of blood vessels. Although the yolk sac membrane being specialized to function as an extraembryonic absorptive organ, it is neither morphologically nor functionally part of the embryonic gut. Yolk absorption is by the phagocytic activity of the extraembryonic endoderm. I used cryohistology and resin embedding histology of complete developmental series of Japanese quail to document the development of the avian yolk sac and changes of the microscopic anatomy throughout development. This material is complemented by complete series of MRT-scans of live ostrich embryos from beginning of incubation through hatching. Considerable changes of size and shape of the yolk mass are documented and discussed as resulting from water flux from albumen to yolk associated with the biochemical activation of yolk sac proteins.During embryogenesis, the yolk sac endoderm forms villi that increase the absorptive surface and reach into the yolk ball. The histology of the absorptive epithelium is specialized for phagocytic absorption of yolk. During early developmental stages, the extraembryonic endoderm is single layered, but it eventually becomes several layers thick during later stages. The extraembryonic mesoderm forms an extensive layer of hematopoietic tissue; deep in this tissue lie the yolk sac vessels. During late stages of development, the erythropoietic tissue disappears, blood vessels are obliterated, and the yolk sac epithelium becomes apoptotic. Results are discussed in the light of the evolutionary history and phylogeny of the amniote egg. | INTRODUCTIONThe avian egg is an almost paradigmatic model of amniote eggs. However, diverging evolutionary pathways have led to different functional, developmental, and morphological features of the eggs in the diverse groups of amniotes (e.g. Packard & Packard, 1980;Elinson, Stewart, Bonneau, & Blackburn, 2015; Starck, Stewart & Blackburn, this issue of JMOR). However, knowledge of the amniote egg is scattered through the published literature, incomplete for morphology and clades providing the necessary phylogenetic coverage, and rarely comprehensive and integrative in an evolutionary context. While the eggshell and the chorioallantois have been covered to some degree by morphological studies, the analysis of the morphology of the yolk mass and the cellular yolk sac has been neglected. Therefore, this paper focuses on the morphology and histology of the avian yolk sac so that comparisons with other amniote eggs may be made and placed in a phylogenetic and evolutionary framework.The avian egg is a cleidoic egg; that is, a protective layer of eggshell membranes, and a calcified, but semi-conductive eggshell (only water vapor and respiratory gases diffuse across shell membranes and shell) enclose proportionally large volumes of yolk and albumen. Yolk, albumen, and eggshell are the main constituents of the egg. The ovary

Morphological research on amniote eggs and embryos: An introduction and historical retrospective

“…During oviparous development, the yolk material becomes overgrown and surrounded by a cellular yolk sac that processes it for embryonic use (Blackburn, 2020;Blackburn et al, 2020;Freeman & Vince, 1974;Starck, 1998Starck, , 2020Stewart, 2020;Stewart & Thompson, 2017). Another fetal membrane, the chorioallantois, provides for gas exchange across the eggshell (Birchard & Reiber, 1995;Romanoff, 1960;Starck, 1998).…”

“…The eggshell is formed by organic fibers associated with an external layer of calcium carbonate (G. C. Packard & Packard, 1988;Schleich & Kästle, 1988). The shell can be semiflexible ("leathery"), as in most squamates and some turtles, or hard and brittle, as in other turtles plus gekkonids, birds, and crocodilians (Iverson & Ewert, 1991;Kusuda et al, 2013;Starck, 2020). Eggs of oviparous amniotes vary in dependence on the external environment for physiological exchange, in part because of properties of the eggshell.…”

“…To facilitate yolk uptake, the yolk sac lining develops complex ridges that increase the surface area available for yolk absorption (Bellairs, 1964;Juurlink & Gibson, 1973). For the microscopic anatomy of these relevant features in birds, see Starck (2020) in this issue of Journal of Morphology. Recent studies have shown that yolk material is digested extracellularly in the yolk sac cavity, and that its metabolites are absorbed through receptor-mediated uptake of macromolecules (Bauer et al, 2013;Yadgary et al, 2011;Yoshizaki et al, 2004).…”

T. Thomson Flynn and the monotreme egg from oocyte maturation to germ layer formation

“…However, the presence of a latebra in monotremes, lizards and birds seems to be just such a feature. Clearly it has been refined in the avian lineage where it forms a unique character complex with the nucleus of Pander and the chalazae; together they constitute a balancing system that always turns the blastodisc to the upper face of the egg (Starck, 2020).…”

Functional morphology, diversity, and evolution of yolk processing specializations in embryonic reptiles and birds

“…In birds, the yolk material is absorbed by cells that line the inside of the yolk sac (Freeman & Vince, 1974;Lambson, 1970;Romanoff, 1960;Starck, 1998Starck, , 2020. Products of yolk digestion are then released into the vitelline circulation and delivered to the embryo to fuel development.…”