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

Kaczmarek, Ł. , Roszkowska, M. , Fontaneto, D. , Jezierska, M. , Pietrzak, B. , Wieczorek, R. , Poprawa, I. , Kosicki, J. Z., Karachitos, A. and Kmita, H. (2019), Staying young and fit? Ontogenetic and phylogenetic consequences of animal anhydrobiosis. Journal of Zoology, https://doi.org/10.1111/jzo.12677

Anhydrobiosis is commonly defined as desiccation tolerance that denotes the ability to survive almost complete drying (dehydration) without sustaining damages. Thus, it can be regarded as an adaptation to fluctuating environmental conditions, allowing the organisms to survive when conditions are not suitable for active life. In plants, anhydrobiosis mainly occurs in seeds but can sometimes also occur in vegetative parts. Similarly, two modes of anhydrobiosis can be distinguished in animals, i.e. during developmental stages and in adult specimens. The former are described as developmental resting stages and are exemplified by dormant eggs, larvae, and cysts. However, anhydrobiosis occurring at any stage of animal life, including adults, is found only in a few invertebrate phyla i.e. some Arthropoda, nematodes, bdelloid rotifers and tardigrades. Moreover, nematodes, bdelloid rotifers, and tardigrades are the only animals known to be capable of anhydrobiosis as adult individuals.

Echiniscus merokensis (ITALY)
Tardigrade Echiniscus merokensis. Photo credit: Milena Roszkowska, Magdalena Gawlak & Łukasz Kaczmarek

Importantly, it has been shown for nematodes, bdelloid rotifers, and tardigrades that anhydrobiosis during adult life suspend or slow down aging. The latter is illustrated by two models based on experimental data and concerning the invertebrate aging scenarios during anhydrobiosis, namely the “Sleeping Beauty” and “Picture of Dorian Gray” models. According to the “Sleeping Beauty” model, anhydrobiotic organisms do not age during anhydrobiosis, whereas the “Picture of Dorian Gray” model predicts that the anhydrobiotic organism ages, at least during the initial stage of anhydrobiosis. However, although much data are available on aging in nematodes in particular, but also rotifers and tardigrades, until now predictions based on these two models have rarely been tested, namely for one tardigrade and nematode species, and two bdelloid rotifer species. Nevertheless, both these models appear to be applicable. Moreover, available data indicate numerous anhydrobiosis benefits important for individual fitness. Thus, the absence of aging symptoms would be yet another benefit of anhydrobiosis, alongside higher fecundity and increased offspring longevity. This observation allowed for the hypothesis that anhydrobiosis appears to be a winning strategy because during the time of anhydrobiosis, when the conditions are not suitable for active life, no other animal can actually reproduce. Therefore, the demographic advantage to anhydrobiotic animals is that they can recover reproduction and fitness after desiccation.

Mesobiotus obscurus (Spitsbergen)
Tardigrade Mesobiotus obscurus. Photo credit: Milena Roszkowska, Magdalena Gawlak & Łukasz Kaczmarek

To get a better understanding of the aging patterns of anhydrobiotic organisms, we were inspired to conduct a review and synthesis of existing published data to summarise what is known about anhydrobiosis and its impact on aging. The understanding of anhydrobiotic animals and their aging strategies can provide fundamental answers for many branches of basic and applied sciences. Therefore, we started from a general overview of aging and anhydrobiosis, trying to find common points. Then we turned to cellular phenomena, as the cellular mechanisms involved in anhydrobiosis are expected to be linked to the processes of aging, as increased longevity may be a result of resistance and/or protection against external factors. Finally, having in mind the impact of anhydrobiosis on individual fitness, we discuss possible implications of these models for individual longevity and survival as well as phenotypic diversity of taxa and their evolution. We assumed that differences between anhydrobiotic organisms with a “non-aging” strategy (the “Sleeping Beauty” model) and with an “aging” strategy (the “Picture of Dorian Gray” model) could result in differences in their evolution, diversification, and biogeography. Yet, very little is known on the topic because only a few studies can be applied to verify the assumption, and therefore we were condemned to speculations.

Łukasz Kaczmarek

Ramazzottius sp. (ECUADOR)
Tardigrade Ramazzottius sp. Photo credit: Milena Roszkowska, Magdalena Gawlak & Łukasz Kaczmarek

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