The Single-Celled Ancestors of Animals: A History of Hypotheses

Abstract

Animals, with their complex and obligate multicellularity, evolved from microbial eukaryotes that were likely obligately or facultatively unicellular. The nature of the unicellular progenitors of animals has intrigued biologists since the late 19th century, coinciding with the parallel spread of the cell theory and the theory of evolution. However, views on the ancestry of animals have been extremely varied. The huge diversity of single-celled organisms, the tremendous plasticity of animal cellular phenotypes, and the difficulties of organizing both into clear phylogenies in the pre-molecular era allowed a wide range of hypotheses to flourish, with nearly every major single-celled lineage, at one time or another, having been proposed as the precursor of animals. Most of these hypotheses never gained followers beyond their originator (such as the ideas that animals evolved directly from either bacteria, Volvox or fungi) and will not be discussed here. Three concepts, however, have been enduring and influential: (1) the amoeboid theory; (2) the flagellate theory; and the (3) the ciliate theory – to which a fourth category can now be added: (4) a mixed model, in which the ancestor was phenotypically plastic. We will discuss their origin, history, and current relevance.

Placozoan fiber cells: mediators of innate immunity and participants in wound healing

“…Metazoans are widely thought to be the descendants of a colony of cells similar to modern choanoflagellates 109 , 125 , although alternative scenarios also have been proposed 111 , 112 , 126 . The genomes of the ancestral cells likely contained the large set of genes shared between Metazoa and Holozoa, including some that are absent in modern choanoflagellates 110 , 112 , 127 .…”

Origin and evolution of animal multicellularity in the light of phylogenomics and cancer genetics

“…Animals are also proposed to have evolved via juvenile characters (by paedomorphism) from an organism that resembled a planula, i.e. , a cnidarian larva [ 36 ]. Others suggested that animals derived from an amorphous collection of cells with a gradually developing internal cavity that gave birth to primitive sponge like or a cnidaria-like animal [ 37 ].…”

“…Then, based on the resemblance between choanoflagellates and the choanocytes of sponges, animals were thought to derive from a colony of cells similar to choanoflagellates [35]. Animals are also proposed to have evolved via juvenile characters (by paedomorphism) from an organism that resembled a planula, i.e., a cnidarian larva [36]. Others suggested that animals derived from an amorphous collection of cells with a gradually developing internal cavity that gave birth to primitive sponge like or a cnidaria-like animal [37].…”

A flagellate-to-amoeboid switch in the closest living relatives of animals

“…Nonetheless, the origin of animal amoeboid cells has remained mysterious ( Fritz-Laylin, 2020 ), in part because the closest living relatives of animals, the choanoflagellates ( Ruiz-Trillo et al, 2008 ; King et al, 2008 ), have been thought to exist solely in a flagellate form (except while encysted [ Leadbeater, 2015 ]). The nature of the protozoan ancestor of animals was a matter of debate as early as the 19th century, when the relationship between animals and choanoflagellates was still unknown (reviewed in Brunet and King, 2020 ). Haeckel originally proposed in 1874 that animals descended from amoebae that evolved coloniality and later acquired cilia ( Haeckel, 1874 ).…”