Origin, form and function of extraembryonic structures in teleost fishes

Abstract

Teleost eggs have evolved a highly derived early developmental pattern within vertebrates as a result of the meroblastic cleavage pattern, giving rise to a polar stratified architecture containing a large acellular yolk and a small cellular blastoderm on top. Besides the acellular yolk, the teleost-specific yolk syncytial layer (YSL) and the superficial epithelial enveloping layer are recognized as extraembryonic structures that play critical roles throughout embryonic development. They provide enriched microenvironments in which molecular feedback loops, cellular interactions and mechanical signals emerge to sculpt, among other things, embryonic patterning along the dorsoventral and left–right axes, mesendodermal specification and the execution of morphogenetic movements in the early embryo and during organogenesis. An emerging concept points to a critical role of extraembryonic structures in reinforcing early genetic and morphogenetic programmes in reciprocal coordination with the embryonic blastoderm, providing the necessary boundary conditions for development to proceed. In addition, the role of the enveloping cell layer in providing mechanical, osmotic and immunological protection during early stages of development, and the autonomous nutritional support provided by the yolk and YSL, have probably been key aspects that have enabled the massive radiation of teleosts to colonize every ecological niche on the Earth. This article is part of the theme issue ‘Extraembryonic tissues: exploring concepts, definitions and functions across the animal kingdom’.

The development of the digestive system and the fate of the yolk syncytial layer in postembryogenesis of Stenodus leucichthys nelma (Teleostei)

“…The yolk sac consists of ectodermal and mesodermal derivatives and the yolk complex made up of the YSL and maternal reserves. The YSL is a temporary structure performing morphogenetic, nutritional, immune, and probably other functions during embryonic and larval development of Teleostei (Carvalho & Heisenberg, 2010; Concha & Reig, 2022; Jaroszewska & Dabrowski, 2011; Kondakova & Efremov, 2014; Kondakova et al, 2019; Kunz, 2004). The complex and dynamic YSL structure of S. leucichthys nelma was described earlier (Kondakova & Bogdanova, 2021; Kondakova et al, 2017a).…”

A computational framework for testing hypotheses of the minimal mechanical requirements for cell aggregation using early annual killifish embryogenesis as a model

“…Annual killifish have a unique early developmental pattern that differs from most teleost species. Unlike non-annual species, for whom most morphogenetic movements are concomitant, annual killifish have separated epiboly from embryo formation, resulting in an initial phase of cell dispersal that is followed by a process of cell aggregation, with embryonic cells occurring through active cell migration in the confined space between the enveloping layer (EVL) and the yolk syncytial layer (YSL) ( Figure 1 ) ( Dolfi et al, 2014 ; Concha and Reig, 2022 ). The embryonic cells remain undifferentiated, with stem-like properties during epiboly and until the end of the dispersion phase, when the cells start to aggregate at one pole of the embryo and initiate the genetic and morphogenetic processes leading to the formation of germ layers and the establishment of the embryonic axis ( Wourms, 1972 ; Pereiro et al, 2017 ; Márquez et al, 2019 ) ( Figure 1 ).…”

“…The embryonic cells remain undifferentiated, with stem-like properties during epiboly and until the end of the dispersion phase, when the cells start to aggregate at one pole of the embryo and initiate the genetic and morphogenetic processes leading to the formation of germ layers and the establishment of the embryonic axis ( Wourms, 1972 ; Pereiro et al, 2017 ; Márquez et al, 2019 ) ( Figure 1 ). These processes, which span between several hours and a few days depending on the specific killifish species and the environmental conditions ( Dolfi et al, 2014 ; Márquez et al, 2019 ), occur in the context of a nearly spherical egg (about 1 mm diameter) and can be easily visualized in a living animal, as eggs are optically transparent and develop outside the mother ( Wourms, 1972 ; Pereiro et al, 2017 ; Reig et al, 2017 ; Concha and Reig, 2022 ). The dispersion phase is characterized by a random walk of embryonic cells moving at a very low density ( Márquez et al, 2019 ), while the cellular processes and morphogenetic mechanisms that form the aggregate are still unknown.…”

“…It has been proposed that self-organizing processes may break the initial symmetry of the embryo and initiate the aggregation process ( Pereiro et al, 2017 ; Abitua et al, 2021 ), since the molecular signals involved in embryo formation are apparently non-polarized during the stages prior to the aggregate formation. However, it cannot be ruled out that an organizing center, possibly located in extraembryonic structures, provides the signals that initiate the aggregate formation ( Pereiro et al, 2017 ) as has been shown in other non-annual teleost species ( Concha and Reig, 2022 ).…”

Extraembryonic tissues: exploring concepts, definitions and functions across the animal kingdom

“…Extraembryonic tissues in non-mammalian vertebrates are the focus of four additional papers. Concha & Reig [9] give a comprehensive overview of the origin, form, and function of teleost extraembryonic structures, that is, the yolk syncytial layer and the enveloping layer. Wen et al [10] investigate differences in molecular signatures of the chorioallantoic membrane between the live-bearing and egg-laying lizards.…”