The evolution of air-breathing is the adaptive response to high environmental temperatures

Abstract

The transition to air breathing is the key innovation during evolution of terrestrial animal life from aquatic ancestors in a huge variety of taxa. This transition has happened numerous times and independently in all animal phyla. Especially in fishes and crabs, the proximate factors of this physiological innovation were poorly understood. A previous paradigm saw hypoxia in estuarine and fresh waters as an initial driver of the transition from water- to air-breathing but was not able to explain the geographical distribution of extant genera of amphibious fish and crabs, a long standing puzzle in evolutionary biology. Here we provide evidence that high temperature extremes act as a key and universal driver for this transition, and that thermal extremes can explain the present phylogenetic knowledge and distribution of amphibious and terrestrial crabs. Our results demonstrate that breathing air rather than water saves energy and extends aerobic performance to a wider thermal niche. These findings provide a mechanistic explanation of the recurrent and repeated evolution of air-breathing in response to the effects of temperature demonstrating that the emergence of this novel respiratory mode has a direct benefit for improving thermal tolerance by enhancing the oxygen provision.