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’.