Abstract
Tardigrada, a phylum of meiofaunal organisms, have been at the center of discussions of the evolution of Metazoa, the biology of survival in extreme environments, and the role of horizontal gene transfer in animal evolution. Tardigrada are placed as sisters to Arthropoda and Onychophora (velvet worms) in the superphylum Panarthropoda by morphological analyses, but many molecular phylogenies fail to recover this relationship. This tension between molecular and morphological understanding may be very revealing of the mode and patterns of evolution of major groups. Limnoterrestrial tardigrades display extreme cryptobiotic abilities, including anhydrobiosis and cryobiosis, as do bdelloid rotifers, nematodes, and other animals of the water film. These extremophile behaviors challenge understanding of normal, aqueous physiology: how does a multicellular organism avoid lethal cellular collapse in the absence of liquid water? Meiofaunal species have been reported to have elevated levels of horizontal gene transfer (HGT) events, but how important this is in evolution, and particularly in the evolution of extremophile physiology, is unclear. To address these questions, we resequenced and reassembled the genome of H. dujardini, a limnoterrestrial tardigrade that can undergo anhydrobiosis only after extensive pre-exposure to drying conditions, and compared it to the genome of R. varieornatus, a related species with tolerance to rapid desiccation. The 2 species had contrasting gene expression responses to anhydrobiosis, with major transcriptional change in H. dujardini but limited regulation in R. varieornatus. We identified few horizontally transferred genes, but some of these were shown to be involved in entry into anhydrobiosis. Whole-genome molecular phylogenies supported a Tardigrada+Nematoda relationship over Tardigrada+Arthropoda, but rare genomic changes tended to support Tardigrada+Arthropoda.
Highlights
IntroductionThe superphylum Ecdysozoa emerged in the Precambrian, and ecdysozoans dominated the early Cambrian explosion and are dominant (in terms of species, individuals, and biomass) today
The superphylum Ecdysozoa emerged in the Precambrian, and ecdysozoans dominated the early Cambrian explosion and are dominant today
We explored the comparative biology of anhydrobiosis in 2 species of tardigrade that differ in the mechanisms they use to enter anhydrobiosis
Summary
The superphylum Ecdysozoa emerged in the Precambrian, and ecdysozoans dominated the early Cambrian explosion and are dominant (in terms of species, individuals, and biomass) today. Many species of terrestrial tardigrades are cryptobiotic: they have the ability to survive extreme environmental challenges by entering a dormant state [7]. Common to these resistances is an ability to lose or exclude the bulk of body water, and anhydrobiotic tardigrades have been shown to have tolerance to high and low temperatures (including freezing), organic solvents, X- and gamma-rays, high pressure, and the vacuum of space [8,9,10,11,12,13,14,15]. Many other animals have cryptobiotic abilities, including some nematodes and arthropods [18], and comparison of the mechanisms in different independent acquisitions of this trait will reveal underlying common mechanisms
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