Interspecies control of development during mammalian gastrulation

Abstract

Gastrulation represents a pivotal phase of development and aberrations during this period can have major consequences, from minor anatomical deviations to severe congenital defects. Animal models are used to study gastrulation, however, there is considerable morphological and molecular diversity of gastrula across mammalian species. Here, we provide an overview of the latest research on interspecies developmental control across mammals. This includes single-cell atlases of several mammalian gastrula which have enabled comparisons of the temporal and molecular dynamics of differentiation. These studies highlight conserved cell differentiation regulators and both absolute and relative differences in differentiation dynamics between species. Recent advances in in vitro culture techniques have facilitated the derivation, maintenance and differentiation of cell lines from a range of species and the creation of multi-species models of gastrulation. Gastruloids are three-dimensional aggregates capable of self-organising and recapitulating aspects of gastrulation. Such models enable species comparisons outside the confines of the embryo. We highlight recent in vitro evidence that differentiation processes such as somitogenesis and neuronal maturation scale with known in vivo differences in developmental tempo across species. This scaling is likely due to intrinsic differences in cell biochemistry. We also highlight several studies which provide examples of cell differentiation dynamics being influenced by extrinsic factors, including culture conditions, chimeric co-culture, and xenotransplantation. These collective studies underscore the complexity of gastrulation across species, highlighting the necessity of additional datasets and studies to decipher the intricate balance between intrinsic cellular programs and extrinsic signals in shaping embryogenesis.

A single-cell atlas of pig gastrulation as a resource for comparative embryology

“…We harnessed this resource to investigate the major temporal signalling and differentiation events, which direct primary gastrulation in bilaminar disc embryos. Our findings underscore the nuanced heterochrony in embryonic development across mammals, evidenced by asynchrony in cell type maturation 63 . Further, these heterochronic differences combined with comparisons between pigs, monkeys and mice reinforce the idea that extraembryonic tissues may be less conserved than their embryonic counterparts 3 , 25 , 27 .…”

A mathematical framework for measuring and tuning tempo in developmental gene regulatory networks

“…During each one of these processes, the same genes are expressed in the same sequential manner, but at different speeds. Drawing an analogy from music, the species-specific execution speed of otherwise analogous genetic programmes has been termed the tempo of the system ( Rayon et al, 2020 ; Diaz-Cuadros and Pourquié, 2023 ; Rayon, 2023 ; Simpson and Alberio, 2023 ).…”

A Mathematical Framework for Measuring and Tuning Tempo in Developmental Gene Regulatory Networks

“…During each one of these processes, the same genes are expressed in the same sequential manner, but at different speeds. Drawing an analogy from music, the species-specific execution speed of otherwise analogous genetic programs has been termed the tempo of the system [13, 17, 18, 19].…”