About two-thirds of salamander species have relinquished their lungs, but despite this potential handicap, members of this surprisingly diverse group occupy a variety of habitats in locations around the world, from European caves to Neotropical cloud forests. As aquatic embryos, they can subsist on oxygen taken up from water across their skin, whereas the lungless adults breathe air with the lining of their mouths. In a recent study, Zachary Lewis and a team then based at Harvard University, USA, explored how the larval skin and adult mouth have been repurposed for respiration in lungless salamanders.

The lungs of most air-breathing animals are coated with a thin layer of a wetting agent, know as a surfactant, which helps mucus spread and enhances absorption of oxygen into the blood. Wondering whether surfactants may contribute to breathing in the lungless salamanders, Lewis and his colleagues decided to study the production of mRNA – which is the first step in the production of proteins from genes – from the gene for a crucial surfactant component, surfactant protein C, in salamanders with and without lungs.

In their first breath-taking finding, the Harvard team established that all of the salamanders that were available to them (with and without lungs) were endowed with two genes for this surfactant protein. Some time in early salamander evolution, the gene duplicated, so all salamanders hold a spare copy. Apart from that, the expression of the original gene in a salamander with normal lungs – the axolotl – was typical of that of every other air-breathing vertebrate: mRNA from the original copy of the surfactant protein C gene was exclusively present in the lung and it was produced in the animal's lung throughout embryonic development and adulthood. mRNA from the copied gene was also produced in axolotl lungs, but only at low levels, and only in adults.

However, in the lungless salamanders, the copied gene came into its own. Most strikingly, the embryos produced mRNA from the new copy of the gene all over their skin surface, but as the salamanders grew larger, the mRNA production subsided on the skin surface while it began to appear in the animals’ mouths. The adult lungless salamanders produced the new mRNA exclusively in their mouths and throat. Meanwhile, there was hardly any mRNA produced from the original version of the surfactant protein gene. In other words, the pattern of gene expression mirrored the transition from aquatic to aerial breathing as the amphibians metamorphosed into adults.

The authors believe that the new gene may help lungless salamanders absorb oxygen through their skin and mouths. However, as this study only confirmed that the gene is translated in the mouth to produce mRNA, they must hold their breath until they can confirm that a functional protein is produced. Nevertheless, this work may provide a remarkable example of ‘historical contingency’, an idea popularised by Stephen Jay Gould, which suggests that events in the evolutionary history of an animal group can constrain their future trajectory. Long before the first lungless salamanders evolved, this surfactant protein gene was duplicated, but the copy was not fully exploited at first. This earlier event may then have later facilitated the evolution of lunglessness by helping salamanders breathe through other areas of their bodies.

Z. R.
J. A.
Expression of a novel surfactant protein gene is associated with sites of extrapulmonary respiration in a lungless salamander
Proc. R. Soc. B