Mapping single-cell atlases throughout Metazoa unravels cell type evolution

Abstract

Comparing single-cell transcriptomic atlases from diverse organisms can provide evolutionary definition of cell types, elucidate the origins of cellular diversity, and transfer cell type knowledge between species. Yet, comparison among distant relatives, especially beyond a single phylum, is hindered by complex gene histories, lineage-specific inventions, and cell type evolutionary diversifications. Here, we develop a method to enable mapping cell atlases throughout Metazoa spanning sponge to mouse. Within phyla, we identify homologous cell types, even between distant species, with some even emerging from distinct germ layers. Across phyla, we find ancient cell type families that form densely interconnected groups, including contractile and stem cells, indicating they likely arose early in animal evolution through hierarchical diversifications. These homologous cell types often substitute paralog expressions at surprising prevalence. Our findings advance the understanding of cell type diversity across the tree of life and the evolution of associated gene expression programs.

A muscle-related contractile tissue specified by myocardin-related transcription factor activity in Porifera

“…Our interpretation of the endopinacoderm as being muscle-related is consistent with single-cell sequencing data from the related freshwater species, Spongilla lacustris, which indicate that pinacocytes (data for the endopinacoderm were not disaggregated from other pinacodermal tissues) and another cell type, myopeptidocytes, cluster with myocytes from other animals 18,30 .…”

“…Our interpretation of the endopinacoderm as being muscle-related is consistent with single-cell sequencing data from Spongilla lacustris, which indicate that pinacocytes (data for the endopinacoderm were not disaggregated from other pinacodermal tissues) and another cell type, myopeptidocytes, cluster with myocytes from other animals (14,31). Myopeptidocytes are solitary cells in the interstitial extracellular matrix (mesohyl) and express contractile genes including nmMyHC, but nothing else is yet known about their developmental specification, contractile behavior, or possible regulatory mechanisms.…”

Elementary nervous systems

“…Among bilaterians, whole-body single-cell datasets have been reported for the annelid Platyynereis [ 22 ] and the planarian Schmidtea [ 23 , 24 ] and likewise exhibit heterogeneous populations of neurons. As of now, it has been difficult to relate neuronal cell populations between species [ 25 , 26 ]—which may improve with ongoing methodological progress in the comparison of single-cell genomics datasets across larger taxonomic distances [ 76 ]. In any case, the diversity of neuronal types that is manifest in early branching metazoans would suggest that the evolutionary transition from non-neural to neural may have taken place more than once in distinct tissues—and, possibly, in distinct evolutionary lineages.…”

Multiple Origins of Neurons From Secretory Cells

“…This view does not prevent establishing evolutionary lineages of homologous cell types within particular taxonomical units such as classes, subclasses, orders, families, and genera. The cell-lineage-specific homologies across phyla are still a challenge (Tarashansky et al, 2020). 3) What is a neuron?…”