Staying young and fit? Ontogenetic and phylogenetic consequences of animal anhydrobiosis

Abstract

Although gradual deterioration of life functions with age is not a fundamental rule, it is pervasive among living organisms, regardless of their mode of reproduction and the number of constituent cells. However, deterioration can be temporarily arrested or slowed down due to the process of anhydrobiosis. Two modes of anhydrobiosis can be distinguished for the developmental and adult stages of animals. Developmental resting stages are reported for different animals, including sponges (Porifera), stingers (Cnidaria), flatworms (Platyhelminthes), insects (Insecta), copepods (Copepoda) and branchiopods (Branchiopoda). However, anhydrobiosis occurring at any stage of animal life, including adults, is found only in a few invertebrate phyla, namely roundworms (Nematoda), wheel animals (Rotifera) and water bears (Tardigrada). Notably, in the second group anhydrobiosis has been proposed to eliminate or slow‐down aging symptoms. This, in turn, may correlate with higher fitness and fecundity, and increased offspring longevity. We present available data concerning anhydrobiosis of tardigrades, bdelloid rotifers and nematodes, the only animals known to be capable of anhydrobiosis as adult individuals. The impact of anhydrobiosis on animal aging is illustrated by two models based on experimental data, namely the “Sleeping Beauty” and “Picture of Dorian Grey” models. According to the “Sleeping Beauty” model, anhydrobiotic organisms do not age during anhydrobiosis, whereas the “Picture of Dorian Grey” model predicts that the anhydrobiotic organism ages, at least during the initial stage of anhydrobiosis. Finally, we discuss possible implications of these models for individual longevity and survival as well as phenotypic diversity of taxa and their evolution. A better understanding of life strategies of anhydrobiotic animals both at the ontogenetic and phylogenetic levels can provide answers to many fundamental questions and useful practical outputs in branches of applied sciences.

Meiofauna as a model to test paradigms of ecological metacommunity theory

“…Freshwater meiofauna includes a number of taxa with various phylogenetic origin (e.g., tardigrades, gastrotrichs, rotifers, nematodes, water mites, harpacticoids, and ostracods). Theoretically, meiofauna has unlimited dispersal abilities due to its small size and frequent adaptations against desiccation (Martens et al 2008;García-Roger et al, 2019;Kaczmarek et al, 2019). There is a solid evidence for the frequent occurrence of some meiofauna (bdelloid rotifers, tardigrades, and nematodes) in wind-dispersed samples (Jenkins & Underwood, 1998;Wilson & Sherman, 2013;Ptatscheck et al 2018), suggesting high dispersal rates.…”

Long-term anhydrobiosis in two taxa of moss dwelling Eutardigrada (Tardigrada) desiccated for 12 and 15 years, respectively

“…Guidetti et al 2011a;Møbjerg et al 2011), the most prevalent one is anhydrobiosis, defined as the tolerance to almost complete dehydration (for a review, see e.g. Kaczmarek et al 2019). An anhydrobiotic organism is even able to survive desiccation, with the almost complete loss of body water (e.g.…”

“…Tardigrade anhydrobiosis, besides providing the opportunity to survive in hostile environmental conditions, has another positive aspect. According to the "Sleeping Beauty" hypothesis proposed for rotifers and later tested on tardigrades (for a review see Kaczmarek et al 2019), during anhydrobiosis tardigrades may not age. Anhydrobiosis as well as other forms of cryptobiosis could also slow down the evolution and morphological diversity of animals because of a reduction in environmental selective pressure (e.g.…”

“…Anhydrobiosis as well as other forms of cryptobiosis could also slow down the evolution and morphological diversity of animals because of a reduction in environmental selective pressure (e.g. Kaczmarek et al 2019).…”

The Tardigrade Hypsibius Exemplaris as an Emerging Model to Study the Mitochondrial Alternative Oxidase at Animal Organismal Level

“…They inhabit marine, freshwater and terrestrial habitats, but all are regarded to be aquatic animals because they require a water-lm surrounding the body to be active. The most known feature of tardigrades is the ability to enter cryptobiosis when environmental conditions are unfavorable (for review, see, for example, [40][41][42][43][44][45][46]).…”