The evolution of temperature and desiccation-related protein families in Tardigrada reveals the complex acquisition of extremotolerance.

Tardigrada is an ecdysozoan lineage most famous for its resilience. Tardigrades can tolerate high doses of radiation, low oxygen environments, desiccation and both high and low temperatures under a dormant state called anhydrobiosis, which is a reversible halt of metabolism upon almost complete desiccation. A large amount of research has focused on the genetic pathways related to these capabilities, and a number of genes have been identified and linked to tardigrade's extremotolerant response. However, the history of these genes is unclear, and the origins and history of extremotolerant genes within Tardigrada remain a mystery. Here, we generate the first phylogenies of six separate gene families linked with desiccation and radiation tolerance in Tardigrada: Cytosolic Abundant Heat Soluble Protein (CAHS), Mitochondrial Abundant Heat Soluble Protein (MAHS), Secretory Abundant Heat Soluble Protein (SAHS), Meiotic Recombination 11 Homolog (MRE11) and the newly discovered Echiniscus testudo Abundant Heat Soluble Proteins (EtAHS Alpha and Beta). Our study of the gene duplications suggests a link between the evolution of these genes and aquatic to limno-terrestrial transitions within tardigrades. Our results suggest that tardigrades likely transitioned from the marine to limno-terrestrial environment only twice, once in stem-Eutardigrada and once in Heterotardigrada, which explains the unique adaptations to anhydrobiosis present in both classes.