Choanoflagellates are the closest single-celled relatives of animals and provide fascinating insights into developmental processes in animals. Two species, the choanoflagellates Monosiga brevicollis and Salpingoeca rosetta are emerging as promising model organisms to reveal the evolutionary origin of key animal innovations. In this review, we highlight how choanoflagellates are used to study the origin of multicellularity in animals. The newly available genomic resources and functional techniques provide important insights into the function of choanoflagellate pre- and postsynaptic proteins, cell-cell adhesion and signaling molecules and the evolution of animal filopodia and thus underscore the relevance of choanoflagellate models for evolutionary biology, neurobiology and cell biology research.

Some organisms in nature have developed the ability to enter a state of suspended metabolism called cryptobiosis when environmental conditions are unfavorable. This state-transition requires execution of a combination of genetic and biochemical pathways that enable the organism to survive for prolonged periods. Recently, nematode individuals have been reanimated from Siberian permafrost after remaining in cryptobiosis. Preliminary analysis indicates that these nematodes belong to the genera Panagrolaimus and Plectus. Here, we present precise radiocarbon dating indicating that the Panagrolaimus individuals have remained in cryptobiosis since the late Pleistocene (~46,000 years). Phylogenetic inference based on our genome assembly and a detailed morphological analysis demonstrate that they belong to an undescribed species, which we named Panagrolaimus kolymaensis. Comparative genome analysis revealed that the molecular toolkit for cryptobiosis in P. kolymaensis and in C. elegans is partly orthologous. We show that biochemical mechanisms employed by these two species to survive desiccation and freezing under laboratory conditions are similar. Our experimental evidence also reveals that C. elegans dauer larvae can remain viable for longer periods in suspended animation than previously reported. Altogether, our findings demonstrate that nematodes evolved mechanisms potentially allowing them to suspend life over geological time scales.

When environmental conditions are unfavorable, such as the complete absence of water or oxygen, high temperature, freezing or extreme salinity, some organisms can enter suspended animation (cryptobiosis)1. This reversible transition is preceded by execution of complex genetic and biochemical programs (preconditioning)2,3,4. Under laboratory conditions, however, animals have only been maintained in a viable cryptobiotic state for a short time. Here we show that desiccation followed by freezing allows C. elegans dauer larvae to retain full viability over very long periods (around 500 days). Consistent with this finding, recently nematode individuals have been reanimated from the Siberian permafrost5, that according to precise radiocarbon dating shows that they remained in cryptobiosis since the late Pleistocene, for about 46,000 years. Phylogenomic inference based on our high-quality genome assembly and morphological analysis demonstrate that these nematodes belong to a novel parthenogenetic species, which we named Panagrolaimus kolymaensis. Genome analysis revealed that the core of the molecular toolkit for cryptobiosis in P. kolymaensis and C. elegans is orthologous. To survive desiccation and freezing under laboratory conditions these two species display similar biochemical responses. Thus, nematodes possess extraordinarily robust adaptive mechanisms that potentially allow them to remain in suspended animation over geological time scales.