Adaptation to desiccation and salinity tolerance: what was first, the chicken or the egg?

The new post of Young Limnologists deal with the evolution of aquatic life in extreme environments: salinity and desiccation

Version in Spanish and Portuguese

One of the most fascinating features of life on earth is its capacity to colonize even the most remote or unfavorable spots all over the planet. Evolutionary ecology is the scientific discipline that aims to understand the mechanisms by which organisms tolerate extreme conditions and are able to colonize harsh environments such as deserts, high mountains or highly saline waters.

Saline streams and ponds are a curious example of adaption to extreme stress conditions. To understand how these environments were colonized, we need to travel back in time when life began, in a seawater medium (roughly 35 grams of salts per liter). However, the first colonizers of inland waters had to deal with a salt-poor medium (freshwaters). They therefore developed adaptations for the active intake of salts, because ions, such as sodium, potassium or calcium, are essential for vital functions.

By vagaries of nature, oscillations of sea level left vestiges of ancient seas in many parts of the planet, which currently form rivers, ponds or lagoons of extreme salinity (up to 200 grams per liter). Thus, organisms previously adapted for retaining salts had to manage to get rid of them when colonizing these systems. However, the evolutionary origin of salt-regulation mechanisms still remains unknown for some groups of aquatic insects, such as water beetles. It has been suggested -but never tested, so far- that these mechanisms could have derived from previous adaptations to deal with desiccation, developed by their terrestrial ancestors.

Fig.1 Rambla Salada stream at Fortuna. Picture: Josefa Velasco.

In addition to saline stress, water beetles in saline temporary environments are exposed to periodical droughts during which most species migrate to wet refugia. Beetles and other aquatic insects are exposed to desiccation when they disperse to more appropriate spots, generally by flying, with the associated cellular damage and risk of dehydration, eventually causing death. Salinity and desiccation have similar physiological effects (both stressors cause water loss and an increase of salt concentration in internal fluids) and consequently, trigger similar mechanisms. Therefore, desiccation resistance mechanisms could have facilitated tolerance to salinity, or vice versa, but it is unknown which adaptation occurred first: "the chicken or the egg?".

That was the question that the authors of this recent study tried to address; they explored the evolutionary links between desiccation resistance, salt-regulation capacity and habitat transitions from fresh to saline waters in a group of water beetles (genus Enochrus, family Hydrophilidae).

Fig. 2. Beetle species belonging to the Enochrus group, with phylogenetic tree

Through laboratory experiments, the authors found that the most saline-tolerant species were also highly resistant to desiccation. Furthermore, they also observed that most of the studied freshwater species had a high resistance to desiccation and, surprisingly, they were able to tolerate salinity levels much higher than those occurring at the waters commonly inhabit by them. By combining these experimental data with the phylogeny (dendrogram representing the evolutionary relationships of these species) of this water beetle group, the evolutionary history of these adaptions was reconstructed.

  

Their results suggest that the most recent common ancestor of these species had a relatively high desiccation resistance, which provided the physiological basis for the enhancement of salt-regulation capacity, enabling them to colonize salt waters. Enochrus beetles thus established in habitats with different salinities and diversified yielding different species. The evolutionary rate of salt-regulation capacity was accelerated during geological periods of global aridification, associated to a decrease in precipitation and temperature. Transitions from fresh to saline waters also matched these arid periods, which provides another clue on the close relationship between tolerance to salinity and desiccation.

This study contributes to understanding how aquatic organisms deal with desiccation and salinity stress, something very important given the ongoing and future increasing aridification associated to global change in Mediterranean areas, in which the temporality and salinity of inland waters is expected to increase.

Pallarés, S.; Arribas, P.; Bilton, D.T.; Millán, A.; Velasco, J. & Ribera, I. (2017). The chicken or the egg? Adaptation to desiccation and salinity tolerance in a lineage of water beetles. Molecular Ecology. doi: 10.1111/mec.14334