The extended analogy of extraembryonic development in insects and amniotes

Abstract

It is fascinating that the amnion and serosa/chorion, two extraembryonic (EE) tissues that are characteristic of the amniote vertebrates (mammals, birds and reptiles), have also independently evolved in insects. In this review, we offer the first detailed, macroevolutionary comparison of EE development and tissue biology across these animal groups. Some commonalities represent independent solutions to shared challenges for protecting the embryo (environmental assaults, risk of pathogens) and supporting its development, including clear links between cellular properties (e.g. polyploidy) and physiological function. Further parallels encompass developmental features such as the early segregation of the serosa/chorion compared to later, progressive differentiation of the amnion and formation of the amniotic cavity from serosal–amniotic folds as a widespread morphogenetic mode across species. We also discuss common developmental roles for orthologous transcription factors and BMP signalling in EE tissues of amniotes and insects, and between EE and cardiac tissues, supported by our exploration of new resources for global and tissue-specific gene expression. This highlights the degree to which general developmental principles and protective tissue features can be deduced from each of these animal groups, emphasizing the value of broad comparative studies to reveal subtle developmental strategies and answer questions that are common across species. This article is part of the theme issue ‘Extraembryonic tissues: exploring concepts, definitions and functions across the animal kingdom’.

Evolution of the insect Hox gene cluster: Comparative analysis across 243 species

“…In insects these membranes consist of two distinct layers: the amnion and serosa (these form a single epithelium known as the amnioserosa in higher flies) [47] , [48] . The amnion is the inner membrane which surrounds the ventral side of the developing embryo, while the serosa is an outer membrane which lies just inside the chorion and envelops the embryo, amnion and yolk [49] , [50] , [51] . This structure is hypothesised to be involved in a wide range of functions unrelated to development of body form, such as a general protective role including structural stability, water regulation and desiccation resistance [52] , [53] , [54] , and innate immune response [55] , [56] , [57] .…”

Single-cell RNA sequencing of mid-to-late stage spider embryos: new insights into spider development

“…Indeed, in arthropods, the so-called extraembryonic tissues (sensu lato) are involved in providing immune response (recently reviewed in e.g. [ 143 , 184 ]. In-situ hybridization shows that the three top markers of this cluster all exclusively are expressed in cells underlying the germ band (and possibly also the dorsal field and ventral sulcus), and thus the cells/tissue that connects the developing embryo (sensu stricto) with the yolk (Fig.…”

Tissue-level integration overrides gradations of differentiating cell identity in beetle extraembryonic tissue

“…Abbreviations: for angles of view: D, dorsal; DL, dorsal-lateral; L, lateral; VL, ventral-lateral; V, ventral; for landmark stages: DB, differentiated blastoderm; PP, primitive pit; AF, amniotic fold; SW, serosal window. Morphogenesis schematics modified from [13].…”

“…These tissues are among the earliest to differentiate. Their rapid maturation is implicated in the evolutionary success of the amniote vertebrates and the insects, due to their essential roles in protecting and provisioning the embryo [11][12][13]. Specific properties of the fully differentiated tissues are tightly linked to their protective functions.…”